Abstract
In general, potassium in soil greatly reduces radiocesium uptake by plants. Using four extraction methods, we investigated forms of potassium retained in soils from Quercus serrata (Konara oak) forests in nine regions across Japan to investigate the effect of potassium on the transfer factor of cesium in oaks. Of the potassium extracted with ammonium acetate (exchangeable K), hydrogen peroxide (H2O2-K), boiling nitric acid (HNO3-K), and tetraphenyl boric acid (TPB-K), HNO3-K, which is considered to be an indicator of nonexchangeable K content, showed the highest correlation with the transfer factor of cesium in Konara oak. H2O2-K showed the second highest correlation coefficient with cesium concentration in Konara oak. On the other hand, no significant correlation was found for exchangeable K with ammonium acetate solution, which is used to determine cesium uptake characteristics of crops. In addition, large variations were observed for all four forms of K. To determine characteristics of cesium uptake and transfer to trees, it is necessary to consider various forms of K, including nonexchangeable K.
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15.1 Introduction
Following the accident at the Fukushima Daiichi Nuclear Power Plant (FNDPP) in 2011, radiocesium (134Cs, 137Cs) spread widely, contaminating forests in Fukushima Prefecture and surrounding prefectures. Unfortunately, 137Cs has a long half-life of 30.2 years, and because forests circulate nutrients through biogeochemical cycles, it is difficult for radionuclides to flow out of these systems (Yamaguchi et al. 2012). Therefore, contamination by 137Cs will be a challenge for the forest industry for a long time (IAEA 2002). The log production industry for cultivating Shiitake mushrooms suffered some of the greatest damage caused by the Fukushima disaster. The Forestry Agency in Japan has ruled that logs containing radiocesium above an index value of 50 Bq kg−1 should not be distributed to markets in order to ensure that the radiocesium concentration in Shiitake mushrooms grown on the logs is below the standard limit for general food in Japan; 100 Bq kg−1 (Ministry of Agriculture, Forestry and Fisheries 2012).
Konara oak (Quercus serrata Murray) was cultivated for mushroom log production in some areas of Fukushima Prefecture and its surrounding prefectures, but shipments of logs are still stopped, because their radiocesium concentrations may exceed the index value. To resume log production in these areas, reducing the radiocesium concentration in Konara oak trees is an urgent issue. Suppressing radiocesium uptake by roots could prevent contamination of seedlings to be planted in the future and new shoots grown from stumps.
One possible solution to reduce root uptake of radiocesium is to increase the amount of potassium (K) in the soil. Plants take up cesium (Cs), because K transporters, especially under low K, can transport Cs, which has similar chemical properties (Nieves-Cordones et al. 2017; Qi et al. 2008). Therefore, higher concentrations of potassium ions (K+) in the rhizosphere compete more effectively with Cs+, so that the transporter preferentially absorbs K+, thereby reducing absorption of Cs+ (Fujimura et al. 2014; Zhu and Smolders 2000). The effect of high K+ concentrations on Cs uptake suppression was also observed in hydroponically cultivated Konara oak seedlings (Kobayashi et al. 2019). Similarly, a pot experiment confirmed that Konara oak seedlings treated with K had lower Cs concentrations than untreated control pots (Kobayashi, unpublished). Consistent with these reports, outdoor K fertilization experiments using cypress (Chamaecyparis obtusa) seedlings and coconut palms (Cocos nucifera L.) confirmed that K addition to the soil suppresses uptake of radiocesium (Komatsu et al. 2017; Robison et al. 2009). As for K in soil, many studies have defined K extracted with 1Â M ammonium acetate solution as exchangeable K and analyzed its suppression of Cs uptake. When exchangeable K concentration in soil is high, plants grown there absorb less radiocesium (Yamamura et al. 2018). Addition of K fertilizer such as potassium chloride to paddies can suppress the transfer of radiocesium to rice plants even when the original exchangeable K concentration of the soil is low (Fujimura et al. 2013; Kato et al. 2015).
On the other hand, there was reportedly no relation between the exchangeable K concentrations and 137Cs uptake at several investigated sites (Kubo et al. 2018). Similarly, for Konara oak, a preliminary analysis of several-year-old native seedlings and rhizosphere soils throughout Japan showed no significant correlation between exchangeable K concentrations in soils and the transfer factor of stable Cs (133Cs), indicating the degree of Cs uptake. Therefore, in addition to exchangeable K, the influence of nonexchangeable K has attracted attention. Nonexchangeable K is a form that is held between layers of clay minerals such as mica, or is incorporated into the structure of the minerals. When there is no relationship between exchangeable K and Cs uptake, the effect of nonexchangeable K should be taken into account to better explain Cs uptake. Eguchi et al. (2015) and Ogasawara et al. (2019) used sodium tetraphenylborate (TPB) and boiling nitric acid (HNO3) respectively, as methods to extract K from soils. While no correlation was found between exchangeable K concentration and 137Cs uptake of rice (Oryza sativa L.), it was shown that the concentration of K extracted by these methods correlated with Cs uptake. These findings indicate that in Konara oak, not only exchangeable K, but also nonexchangeable K could be involved in suppressing Cs uptake.
In this study, we analyzed seedlings of Konara oak and their rhizospheric soils in order to clarify effects of nonexchangeable K as well as exchangeable K in determining Cs uptake by Konara oak. Hydrogen peroxide (H2O2), boiling HNO3, and TPB were used to extract K from soils, and the relationship between these K concentrations and Cs uptake by Konara oak was examined. Because the three methods extract different amounts of K from different fractions of soils, we tried to find the optimal K extraction method to evaluate Cs uptake of Konara oak. In this study, we collected samples not only in Fukushima Prefecture, but also in other uncontaminated areas; thus, we measured 133Cs instead of radiocesium.
15.2 Materials and Methods
15.2.1 Sampling of Native Seedlings and Soils
We used pairs of current-year shoots of native Konara oak seedlings and soils around their roots collected from 36 sites in nine prefectures from February 7th to April 19th, 2017 (Fig. 15.1). Sampling sites were not limited to mountain forests, but were widely distributed in places where acorns of Konara oak were thought to have grown naturally: 1–5-year-old seedlings less than waist high were collected. Soils were collected at three points within a radius of 30 cm from the seedlings to a depth of 10 cm after completely removing litter. These three samples were mixed. The number of sample replicates ranged from 1 to 5, mostly 3, for each site; thus, the total number of pairs of shoots and soils we collected came to 106. Collected current-year shoots and soils were dried in a 70 °C dryer. Dried shoots were cut into pieces 5 mm in length and dried soils were passed through a 2-mm sieve. Carbon and nitrogen in soil samples were determined by the dry combustion method (SUMIGRAPH NC-22F, Sumika Chemical Analysis Service, Tokyo, Japan).
15.2.2 Extraction of K and 133Cs from Soil
Potassium was extracted from soil samples using the four methods. Exchangeable K was extracted with 1 M ammonium acetate for 1 h at a soil:solution ratio of 1:10. To extract K derived from organic matter, 30 wt% H2O2 solution, adjusted to pH 2.0, was added to 1 g of soil, and heated at 85 °C for 8 h. After cooling, 10 mL of 1 M ammonium acetate was added to yield a supernatant after 1 h of shaking. This extract was designated as H2O2-K. Then, the residue was subsequently subjected to boiling HNO3 decomposition. One molar HNO3 was added to the residue and the mixture was heated at 115 °C for 20 min after boiling. After allowing the solution to cool, the supernatant was taken, and 10 mL of 100 mM HNO3 was added to the residue to obtain another supernatant. This operation was performed again, and the three supernatants were mixed. This extract was identified as HNO3-K. Potassium extraction using TPB was performed according to Carey et al. (2011), and the extract was labeled TPB-K. The concentration of exchangeable K was measured using an inductively coupled plasma optical emission spectrometer (ICP-OES) (Optima 7300 DV, PerkinElmer, Waltham, Massachusetts), and concentrations of H2O2-K, HNO3-K, and TPB-K were measured using atomic absorption spectrophotometry (Z-6100, Hitachi High-Technologies Corporation, Tokyo, Japan). In addition, 133Cs concentration in the solution extracted with HNO3 was measured using an inductively coupled plasma mass spectrometer (ICP-MS) (NexION 350, PerkinElmer, Waltham, Massachusetts), and was designated as HNO3-Cs.
15.2.3 Decomposition of Current-Year Shoots and Measurement of 133Cs Concentrations
To determine cesium and potassium concentrations in current-year shoots, about 0.3 g of shoots was digested with 10 mL of HNO3 (60%) using a microwave digester (Multiwave 3000, Anton Parr, Graz, Austria) for 60 min. Concentrations of 133Cs and K in the extracts were measured using ICP-MS and ICP-OES, respectively. The transfer factor (TF), which describes the extent of radiocesium transfer from soil to plants, is usually expressed as the content of radiocesium in the plant (Bq kg−1) divided by the concentration of radiocesium in the soil (Bq kg−1). In this study, however, we analyzed 133Cs, and total 133Cs concentration was not measured, because a dedicated facility was required for the measurement. Therefore, TF was defined by the following equation, and the 133Cs uptake of Konara oak was evaluated using this equation. The reason for using the concentration of HNO3-Cs is to calculate TF with a value close to the 133Cs concentration of the whole soil, such as the TF of radiocesium, and because Cs cannot be extracted by the TPB extraction method.
15.3 Results
15.3.1 Relationship Between Soil K Concentrations and TF
Mean values of TF were calculated for each of the 36 sampling sites, revealing a wide variation with a maximum value of 1.5 and a minimum value of 0.04. Figure 15.2 shows the relationship between each K concentration and TF. Each plot represents the mean and standard deviation at each sampling site. Correlation coefficients (r) are shown in the figures. The correlation coefficient between logarithmic TF and logarithmic exchangeable K concentration was −0.28, and it was nonsignificant (Fig. 15.2a). Relationships among logarithmic TF, logarithmic H2O2-K concentration, and logarithmic HNO3-K concentration were significant (p < 0.05). The correlation coefficients between them were larger than that of the exchangeable K concentration: −0.41 for logarithmic H2O2-K, −0.51 for logarithmic HNO3-K (Fig. 15.2b, c). On the other hand, the correlation coefficient between logarithmic TPB-K concentration and logarithmic TF was −0.29, and the correlation was not statistically significant (Fig. 15.2d).
15.3.2 Relationships Between Soil K Concentrations
The exchangeable K concentration ranged to 7.4 from 40.0Â mg K2O/100Â g soil for 36 values, averaged by sampling site for 106 soils. Relationships between exchangeable K concentration and H2O2-K, HNO3-K, and TPB-K concentrations are shown in Fig. 15.3. Exchangeable K concentration and H2O2-K concentration had the strongest correlation among all combinations, with a correlation coefficient of 0.91 (Fig. 15.3a). The H2O2-K concentration was distributed in the same range as the exchangeable K concentration, compared to the HNO3-K and TPB-K concentrations. The slope of the regression coefficient was 1.2, indicating that the concentration of H2O2-K was 20% greater than the exchangeable potassium concentration, on average.
The correlation coefficient between exchangeable K and HNO3-K was 0.36. In the range of HNO3-K concentrations below 70Â mg K2O/100Â g soil, a linear relationship can be observed with exchangeable K, but the site with higher HNO3-K concentration was not on that line (Fig. 15.3b), which weakened the correlation of the two variables.
The TPB-K concentration tended to increase as the exchangeable K concentration increased at most sites, but a few sites showed very high TPB-K concentrations, despite the low exchangeable K concentrations (Fig. 15.3c). The correlation coefficient between these variables was 0.25. Figure 15.4 shows the relationship between HNO3-K concentration and TPB-K concentration, both of which are often used to evaluate nonexchangeable K. From this figure, we found that the site having the highest HNO3-K concentration and the site with the highest TPB-K concentration were not the same. Excluding these sites, the two variables were generally positively correlated.
15.3.3 Soil HNO3-Cs Concentration and Its Relationship with 133Cs Contents in Shoots
Soil HNO3-Cs concentrations ranged from a maximum of 1.5 μg g−1 to a minimum of 0.11 μg g−1, a 15-fold variation. On the other hand, the 133Cs content of current-year shoots of Konara oak showed a maximum value of 0.48 μg g−1 and a minimum value of 0.01 μg g−1, which was about 50 times different. Figure 15.5 shows the relationship between HNO3-Cs concentration in soils and 133Cs content in shoots. There was no significant correlation between the two variables.
15.3.4 Relationships Between Soil K Concentrations and K Contents of Shoots
Figure 15.6 shows the relationship between the K content in current-year shoots of Konara oak and K concentrations in soil. K concentrations in the soil ranged from 7.4 to 40Â mg K2O/100Â g soil for exchangeable K and from 6.0 to 343Â mg K2O/100Â g soil for TPB-K, whereas the K content in current-year shoots did not differ much, ranging from 2.1 to 3.9 (Fig. 15.6). When the exchangeable K concentration and H2O2-K concentration were high, the K content in current-year shoots tended not to be low, but there were sites in which the K content of shoots was still high, even when the soil K concentration was low.
15.3.5 Relationship Between TF and Soil Carbon and Nitrogen Contents
Soil carbon content ranged from 0.80 to 16.9% and nitrogen content ranged from 0.04 to 1.11%. Figures 15.7 and 15.8 show the relationships between TF and carbon or nitrogen contents, respectively. Except for the two points that specifically showed large TF values, there was no site at which TF was high and carbon or nitrogen content was low, but no clear correlation was observed.
15.4 Discussion
Correlations between TF for 133Cs of current-year shoots and K concentrations in soils extracted by four methods revealed that exchangeable K concentration, which is most commonly used for predicting TF, had little correlation with TF. On the other hand, the concentration of HNO3-K, which extracts nonexchangeable K as well as exchangeable K, had the strongest correlation with TF. Therefore, in Konara oak, 133Cs uptake is thought to be strongly affected not only by exchangeable K, which readily dissolves in soil solution to be available to plants, but also by nonexchangeable K that is sandwiched between clay mineral layers or incorporated into the mineral structure.
In this study, the correlation between TF and TPB-K concentration was weaker than that with HNO3-K concentration. TPB can extract nonexchangeable K such as HNO3, but TPB nondestructively extracts K between clay mineral layers to mimic the K uptake process by plants (Cox et al. 1999), while some K is extracted by destroying the mineral structure when using HNO3 (Li et al. 2015). Although TPB is generally considered to extract more K than HNO3 (Moritsuka 2009), Fig. 15.4 shows that the concentrations of TPB-K and HNO3-K do not always match. Thus, the strength of the correlation with TF differed between HNO3-K concentration and TPB-K concentration, because the extraction source and the extraction amount of two methods are different. Although some studies have measured soil nonexchangeable K concentrations using either HNO3 or TPB and showed that they explained TF better than exchangeable K concentrations (Eguchi et al. 2015; Ogasawara et al. 2019), no previous studies have used multiple methods to extract nonexchangeable K and none have examined their relationships with TF of stable cesium. Although the relationship between HNO3-K concentration and TF of current-year shoots of Konara oak was highly variable among samples, we expect that the multiple extraction methods employed in this study will improve the accuracy of predicting TF of Konara oak by characterizing adsorption of potassium in soil.
The variability of 133Cs content in current-year shoots of Konara oak was larger than the variability of HNO3-Cs concentration in soil, suggesting that 133Cs uptake in Konara oak may be affected by factors other than just soil 133Cs concentration (Fig. 15.5). This is because there was no correlation between HNO3-Cs concentration in the soil and 133Cs content in current-year shoots. Similarly for radiocesium, 137Cs uptake is independent of soil 137Cs concentration (Kanasashi et al. 2020).
Focusing on the relationship between K concentrations in soils and K contents of current-year branches of Konara oak, the variation in K content of the shoots was very small compared to the wide range of K concentrations in the soil, which varied by one to two orders of magnitude. This suggests that the function of exchangeable or nonexchangeable K in the soil on the uptake of K and Cs by Konara oak differs between K, which is an essential element, and Cs, which is not. No clear relationship between TF and either carbon or nitrogen content in the soil was found, suggesting that the effect of soil nutrient status on Cs uptake is small.
Chemical forms of soil K are diverse, influenced by clay mineral composition. Correspondingly, even within the range of the same species, Quercus serrata, differences in Cs uptake and transfer range from one to three orders of magnitude, depending on the environment. In order to improve the accuracy of predicting future radiocesium concentrations in Konara oak, further analysis should focus attention on nonexchangeable K, which has been little studied to date.
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Acknowledgements
We are grateful to Dr. Shoichiro Hamamoto and Mr. Yusuke Akiyama, Graduate School of Agricultural and Life Sciences, The University of Tokyo, for their guidance on soil analytical methods. We express our gratitude to all those who helped in collecting the samples, especially Mr. Tomoyuki Maruyama, Tochigi Prefecture Forest Research Center, Mr. Fukuda Kensuke, Ibaraki Prefectural Government Forestry Technology Center, Mr. Masami Iwasawa, Chiba Prefectural Agriculture and Forestry Research Center, Forestry Research Institute, Mr. Haruki Nakajima, Toyama Prefectural Agricultural, Forestry and Fisheries Research Center, Forest Research Institute, Mr. Jiro Kodani, Ishikawa Agricultural and Forestry Research Center, Forestry Experiment Station, Ms. Yumiko Yamashita, Wakayama Prefectural Forestry Experiment Station, Mr. Nobuyuki Toyota, Ehime University, Faculty of Agriculture, Dr. Kazunori Shimada, Forestry and Forest Products Research Institute, Tama Forest Science Garden, and Dr. Tatsuya Tsurita and Dr. Tsutomu Kanasashi, Forestry and Forest Products Research Institute.
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Kobayashi, R., Masumori, M., Tange, T., Tanoi, K., Kobayashi, N.I., Miura, S. (2023). Effect of Exchangeable and Nonexchangeable Potassium in Soil on Cesium Uptake by Quercus serrata Seedlings. In: Nakanishi, T.M., Tanoi, K. (eds) Agricultural Implications of Fukushima Nuclear Accident (IV). Springer, Singapore. https://doi.org/10.1007/978-981-19-9361-9_15
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