Environmental Materials and Protocols Section: Short Communication Environ. Control Biol., 54 (1), 6569, 2016 DOI: 10.2525/ecb.54.65 Comparison of Potentials of Higher for of Radioactive Cesium from Contaminated Soil

12 1 2 1 3 Masanori TAMAOKI ,TohruYABE ,JunFURUKAWA , Mirai WATANABE , Kosuke IKEDA , 3 4 Izumi YASUTANI and Toru NISHIZAWA

1 Center for Environmental Biology and Ecosystem Studies, National Institute for Environmental Studies, Ibaraki 3058506, Japan 2 Faculty of Life and Environmental Sciences, University of Tsukuba, Ibaraki 3058577, Japan 3 Biotechnology & Afforestation Business Division, TOYOTA Motor Corporation, Aichi 4700201, Japan 4 Faculty of Education and Regional Studies, University of Fukui, Fukui 9108507, Japan

(Received September 1, 2015; Accepted November 9, 2015)

Sixteen species were tested for their potential to remove radioactive cesium from contaminated soil with the Fukushima Daiichi nuclear disaster. There was a large difference of transfer factor (TF) of radiocesium (137Cs) from the soil to plants. Among the examined plants, Hollyhock belonging to Malvaceae showed the highest TF but the efficiency of phytoremediation, such as total 137Cs absorption of a plant or 137Cs removal from unit area, was not proportionally high. According to the evaluation criteria (uptake of 137Cs per plant and/or area), Kochia was shown to be the best plant species among 16 plants investigated here. Analysis of correlation showed that there was positive relationship between the total 137Cs absorption and plant biomass, and contribution rate of plant biomass in total 137Cs uptake by plant was scored to be 91.3%. These results indicate that selection of plant species that shows high biomass on site is important for 137Cs-targeted phytoremediation rather than the plants’ ability in 137Cs-uptake. On the other hand, our results also suggested that the TF value should be considered in order to evaluate the plant ability for 137Cs-targeted phytoremediation. From this point of view, the present study suggests that field-grown Kochia could be used as a potential candidate plant for phytoremediation of 137Cs from soil. Keywords : Kochia, phytoremediation, plant biomass, radiocesium, screening, transfer factor

2012), reduced abundance in common birds (Møller et al., INTRODUCTION 2012), and decrease in blood cell number in wild Japanese monkeys (Ochiai et al., 2014). Therefore, clean-up of In 2011, the Fukushima Daiichi Nuclear Power Plant radionuclides from the contaminated soil becomes a big (FDNPP) accident occurred following the Great East Japan issue in reconstruction and revitalization of Fukushima Earthquake at March 2011. As a result, a huge amount of area. radionuclides, such as 131I, 134cesium (Cs) and 137Cs, were Previous studies relevant to Chernobyl accident discharged to the surrounding environment from the site of showed that soil-penetrated 137Cs binds strongly to the clay accident (Tokyo Electric Power Company, 2012). and showed low mobility. For example, Kirk and Staunton Agricultural lands and forests were heavily contaminated (1989) showed that migration rate of 137Cs was less than 1 with these radionuclides, consequently, commercial distri- cm per year. Thus, the major portion of the 137Cs must be bution of many crops cultivated (and to be cultivated) in se- distributed in the upper 10 cm-thick surface layer of the soil verely contaminated area, chiefly in Fukushima prefecture, column in most types of soils even seven years after of the have been restricted since agricultural products from these accident (Arapis et al., 1997). In the FDNPP accident, con- area often exceeded the regulatory level of radioactivity de- tamination of 137Cs occurred in vast land area especially in fined by laws in Japan (100 Bq kg1). Fukushima prefecture. Because of the high cost, decon- Among the soil-contaminating radionuclides, 137 Cis tamination of the large area polluted with 137Cs by conven- the major radionuclide to be concerned since its half-life is tional engineering methods remains an intractable problem. relatively long (30.1 years; Chino et al., 2011) in compari- Furthermore, these methods often encompass negative ef- son to other radionuclides released from the FDNPP. In fects for physical properties of the soil and also wreak eco- addition, 137 Cs can emit gamma ()-ray, hence long-term system and landscape. biological effects by the -ray released from 137Cs in biota Phytoremediation, the use of higher plants to clean-up including wild animals might also be concerned. Indeed, the contaminants from soil through accumulation of con- following adverse effects in ecosystem in Fukushima have taminants in plants, is an alternative technology to conven- been reported; increased frequency of morphological ab- tional methods (Pilon-Smits and Freeman, 2006). The normality in the pale grass blue butterfly (Hiyama et al., behavior of Cs in soil and plants is similar to that of potas-

Corresponding author : Masanori Tamaoki , fax: 81298502466, e-mail : [email protected]

Vol. 54, No. 1 (2016)  M. TAMAOKI ET AL.

sium (K) and is available for uptake by plants (Smith et al., cv. Redore). One or two young plants were transplanted 2000). Indeed, Cs uptake by plants is consider to be into a pot (0.05 m2 surface area and 0.015 m3) filled with achieved through K transporters, therefore the ratio of contaminated soils on 17th July, 2011. Plants were grown Cs:K in soil is an important parameter to determine the at the experimental field of National Institute for 137 Cs activity in plants (Zhu and Smolders, 2000). The Environmental Studies (NIES; Tsukuba, Ibaraki, 36°03N, transfer factor (TF) is an essential measure in estimating 140°04E) until end of flower stage. The experimental field the ability of plants to transfer polluting chemicals from the is 174.7 km Southwest from FDNPP. To avoid dilution of soil to the plants (Smolders and Tsukada, 2011). The high soil 137Cs concentration, pots were kept under a transparent level of TF indicates that the plant of interest has highly roof that can prevent the direct exposure to precipitation ability in absorption of pollutants from the soil. Therefore, (rain) without blocking sunlight. After the end of flower- plants with high TF, referred to as hyper-accumulator ing, above ground portion of plants were collected for plants, are useful in the context of phytoremediation. In measurement of 37Cs concentration. Fresh weight of each case of heavy metal hyperaccumulators, the plants are plant was measured and plants were dried at 65°C for 1 known to accumulate Cd and As at least at 100 mg g1 and week. Dried plants were porphyrized with a blender some other trace metals such as Co, Cu, Cr, Ni and Pb at (Milser, IFM-800DG, Iwatani Co., Japan) and were en- 1,000 mg g1 (Watanabe, 1997; Reeves and Baker, 2000). closed into 100 mL polystyrene containers for measure- Thus, TFs for heavy metals often attains 100 to 10,000 in ment of 137Cs activity. hyperaccumulator plants. Although several studies showed Collection of 137Cs contaminated soil that higher plants possess the ability for accumulation of Our preliminary experiment showed that 137Cs’s radio- 137Cs in shoot, the TFs of 137Cs in plants are often less than activity was found within 5 to 10 cm depth of soil in the ex- 1 (Entry et al., 1996; Lasat et al., 1998), suggesting the dif- perimental field. Thus, we collected the surface (within 5 ficulty in phytoremediation of 137Cs. cm) of soil from the experimental field of NIES by a snow On the other hand, White et al. (2003) pointed out that blower on 11th July, 2011. Weeds were eliminated from plant ability for 137Cs uptake is affected by various condi- the soil and the collected soil was mixed well in a soil tions such as physicochemical properties of soil, climate blender. The resultant soil mixture was designated as 137Cs conditions, and/or land utilization on the site of contaminated soil in this study, and was used for further ex- phytoremediation. Thus, it is important to evaluate the periments. The soil was also used for chemical analysis, 137Cs-uptake by plants in a similar environmental conditions and the data from which are presented in Table 1. A part found in the 137Cs-contaminated area. To our knowledge, of soil was dried at 65°C for 1 week, and was enclosed into there is only one report that investigates a possibility of 100 mL polystyrene containers for measurement of 137Cs 137 Cs decontamination with various plants in Fukushima activity. (Kobayashi et al., 2014). Measurement of 137Cs raidoactivity in soil and plants In this study, we examine potential of 137 Cs uptake and calculation of TF with higher plants using 16 plant species in an experimental Prepared samples enclosed in 100 mL container were field, which is relatively close to FDNPP. A possibility of used for analysis of 137Cs. The 137Cs radioactivities in the decontamination of 137Cs by means of phytoremediation in samples were measured according to Mimura et al. (2014). Fukushima or other introduction of 137Cs into terrestrial en- In brief, -rays emitted from samples were detected with a vironment is discussed. high-purity germanium (HpGe) detector GC3019 (Canberra Industries Inc., CT, USA). We used software of Gamma MATERIALS AND METHODS Explorer (Canberra Japan KK, Japan) to analyze the -ray spectra. Standard source (MX033U8PP, The Japan Plant materials Radioisotope Association, Japan) was used for the effi- Following seedlings or saplings of 16 plant species ciency calibration. The radioactivities of 137Cs were cor- were purchased from domestic floral shops; Amaranthus rected for radioactive decay to obtain values normalized to Amaranthus tricolor), Chamomile (Matricaria recutita), the sampling date. After the measurement of 137Cs concen- Cherry sage (Salvia microphylla), Cockscomb (Celosia trations, the TF was calculated using the following equa- 137 137 137 argentea), Hollyhock (Althaea rosea), Ice plant (Mesem- tion; TF=[ Cs]p/[ Cs]s, where [ Cs]p is the concentration 137 1 137 bryanthemum crystallinum), Indian spinach (Basella alba), of Cs in planta (Bq kg dry weight) and [ Cs]s is the Kochia ( scoparia), Okra (Abelmoschus esculentus), concentration of 137Cs in soil (Bq kg1 dry weight). Reed (Phragmites australis), Rumex (Rumex obtusifolius), The total 137Cs absorption in each plant was computed Salvia (Salvia splendens), Scarlet rose mallow (Hibiscus by multiplying the concentration of 137Cs in planta (Bq kg1 coccineus), Sunchoke (Helianthus tuberosus), Sunflower dry weight) by plant biomass (kg dry weight). Helianthus annuus), and Tomato (Solanum lycopersicum Furthermore, evaluation of phytoremediation efficiency,

Table 1 Characteristics of the soil using the experiments. pH Water content EC Total carbon Total nitrogen 1 1 1 C/N ratio (H2O) (%) (mS m ) (gC kg DW) (gN kg DW) 6.00.1 2323.80.4 31.80.3 2.70.0 11.70.1 Values are meanSD (n5).

 Environ. Control Biol. POTENTIAL RADIOCESIUM-TARGETED PHYTOREMEDIATION

which is represented by removal of 137Cs per unit area, was of environmental factors such as temperature, soil water calculated from the values of total 137Cs (Bq), pot size (0.05 condition, and other physicochemical properties of soil m2), and planting rate in a pot. (White et al., 2003; Quadir et al., 2011). In the present ex- periments, all plants were grown under the identical condi- RESULTS AND DISCUSSION tion by employing the same soil type, pot size, exposure to same weather conditions, and so on. The only factor dif- Broadley et al. (1999) carried out a literature search on fered among plants was the cultivation period. The plants 14 reports dealing with absorption of radioactive Cs by were grown until the end of flowering, and therefore, culti- plants, and they ranked 136 plant species based on the rela- vation periods ranged from 50 d in Amaranthus to 144 d in tive 137Cs concentrations in shoot. As a result, they showed Reed. We assessed the correlation between 137Cs concen- that shoot 137 Cs concentration in two plant families, tration in planta and cultivation period, but no significant Amarantgaceae and Chenopodiaceae were relatively correlation was found between these parameters (data not higher than that in other plant families. Yamagami et al. shown). Therefore, the large variation in 137Cs concentra- (2010) investigated the accumulation of non-radioactive Cs tion observed in the plants must be reflecting the difference in 50 plant species at Aomori prefecture and listed the in plant species-specific 137Cs-uptake ability. families of Amarantgaceae and Polygonaceae as the candi- To investigate the ability of 137Cs-absorption in each dates for 137 Cs phytoremediation plants in the field. plant species, the TF was calculated using the measured Therefore, we selected the plants for the present experi- 137Cs concentrations in plants and soil. The 137Cs concentra- ments by focusing on the families of Amarantgaceae, tion in the model soil was 1,00493 Bq kg1 (meanSD, Chenopodiaceae and Polygonaceae. Accordingly, Ama- n5), and the TF was calculated based on this value. As ranthus (Amarantgaceae), Cockscomb (Amarantgaceae), in the case with 137Cs concentration in plants, the TF values Kochia (Chenopodiaceae), and Rumex (Polygonaceae), are highly variable between species. The highest TF was were selected as candidates for 137 Cs phytoremediation observed in Hollyhock (average TF0.360) which was plants. significantly higher than the scores in other plants (Fig. 1). For comparison, plants belonging to Malvaceae family Previous study showed that relative in planta concentra- such as Hollyhock, Scarlet rose mallow and Okra were in- tions of Cs in Malvaceae family were at relatively low or cluded in the list of plants since member of Malvaceae moderate level compared to the members of other plant family are reportedly relatively inactive in accumulation of families (Broadley et al., 1999). Therefore, this is the first radiocesium (Broadley et al., 1999). Sunflower is also report showing that a plant belonging to Malvaceae family added as a standard plant in order to normalize the data possesses relatively high ability for absorption of 137 Cs. from published data since some studies have documented Although the reason why Hollyhock can uptake high level the accumulation of 137Cs in this species (Dushenkov et al., of 137Cs remains to be elucidated, this might be specific to 1997; 1999). In addition, agriculturally introduced crops this plant species, because TF values recorded for other such as Ice plant, Indian spinach, tomato, and Okura (as plants belonging to Malvaceae family were not high (ie. the mentioned above) were also used to investigate their poten- average TF in Scarlet rose mallow and Okra are 0.035 and tial for 137Cs accumulation. 0.077, respectively). High range of TF scored after Using selected 16 plant species, concentrations of 137Cs Hollyhock was observed in Amaranthus (average in plants were measured. The 137Cs concentration in plant TF0.279), Ice plant (average TF0.278), Chamomile ranged from 33.4 Bq kg1 in Reed to 361.8 Bq kg1 in (average TF0.271), and Kochia (average TF0.240), Hollyhock. The 137Cs concentration in plants showed large which were all significantly higher than the scores recorded difference indeed; the largest 137Cs concentration was 10 in other plants including a standard plant, Sunflower (aver- times higher than the smallest. Previous studies showed age TF0.187). Previous studies showed that the families that accumulation of 137Cs in plants is affected by a variety of Amarantgaceae have higher ability of Cs absorption in

Fig. 1 Transfer factor (TF) for 137Cs in the 16 plants examined. The TFs in each plant is arranged according to average value in descending order. Bars indicate standard deviation (n3to9).

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comparison to other plant families (Broadley et al., 1999; even though the plant did not show the highest TF among Yamagami et al., 2010), suggesting that the higher ability the plants examined here. In general, total absorption of for Cs-absorption in Amarantgaceae can be maintained 137Cs in a plant is determined by its TF and biomass. As under the meteorological condition on site as Amaranthus, shown in Fig. 1, Kochia showed relatively high score in a member of Amarantgaceae family, ranked high with re- both TF and dry biomass. In fact, among the plant species spect to TF in the present experiments. Shinano et al. scored top 5 in TF, namely, Hollyhock, Amaranthus, Ice (2014) surveyed radiocesium uptake in 33 species/varieties plant, Chamomile, and Kochia, only two species (Kochia within . They found that a large difference and Hollyhock) are also ranked high for uptake of 137Cs per of TF was observed within the same genus, and the highest plant, and among these five plants, biomass is highest in TF (TF0.170) was observed in Amaranthus Kochia (66 g) while biomass of other plants ranges be- hypochondriacus. tween 1437 g. These results may indicate that plant In this study, we used Amaranthus tricolor as model biomass rather than TF could be more important factor for member of the genus Amaranthaceae and the TF in this scoring the plants ability for uptake of 137Cs. In support of species was scored to be at moderate level (between 0.05 to this view, we found that Indian spinach, Tomato, and 0.1) in the previous paper (Shinano et al., 2014). However, Cockscomb all rated high for uptake of 137 Cs (Fig. 2) TF in Amaranthus recorded in our experiment was calcu- showed only moderate TF values (Fig. 1). Individual dry lated to be 0.279, which was higher than the reported TF in biomass in Indian spinach, Tomato, and Cockscomb were Amaranthus hypochondriacus (TF0.170). 149 g, 61 g, and 60 g, respectively. As in the case with The following reasons are presumed in the difference Kochia, these plants showed high level of growth during in TF between our result and previous study. First, we per- cultivation. formed the evaluation of 137Cs uptake by plants on pots by Taken together, these data indicate that plant growth fully bedding the contaminated soil, but Shinano et al. (2014) cultivated plants in Fukushima, at the level 15 cm below the surface of soil. As described above, it is ex- pected that main portion of 137Cs in Fukushima is layered only within upper 10 cm of surface soil (Arapis et al., 1997), thus the difference in TF between our experiments and previous study conducted in Fukushima could be attrib- uted to the access of root system to the layer of soil rich in 137Cs. Second reason is the difference in total concentration of 137Cs in contaminated soil on site. In previous study, 137Cs concentration in the soil from experimental field was  about 2.8-fold (2,770140 Bq kg 1) as compared with our Fig. 2 Efficiencies for 137Cs phytoremediation in the examined experiment. The TF value tends to decrease as plants are plants. (a) Comparison of 137Cs uptake in each plant. 137 grown on highly contaminated soil, possibly due that con- Levels of Cs uptake in each plant species were calcu- lated and average values of top 5 plants are repre- taminant level attained the saturated level for plants. In sented. Bars indicate standard error (n3 to 6). (b) fact, TF values in Amaranthus tricolor recorded in our ex- Comparison of 137 Cs phytoremediation efficiency. periment and previous one differs by 2.8 to 5.6-fold, which Levels of 137Cs uptake per unit area were calculated as is almost proportional to the difference in soil 137Cs concen- an indication of phytoremediation efficiency. Average values of top 5 plants are presented. Bars indicate stan- tration in these experiments (2.8 times difference). dard deviation (n3to6). Although cultivation system employed in our experiment differs from other experiments (Kobayashi et al., 2014; Shinano et al., 2014), our results can be applicable for phytoremediation of soil derived from the decontamination activity as discussed above. In the present experiments, we aimed to evaluate a possibility to perform 137Cs-targeted phytoremediation. In this point, quantifications of total 137Cs absorption by a sin- gle plant as well as the efficiency of 137Cs-uptake from soil, are of great importance. Therefore, we calculated 137Cs up- take in each plant (Fig. 2a) and absorption of 137Cs per unit area (Fig. 2b). Despite of a moderate score in TF, Kochia was shown to be the best plant according to our evaluation criteria (uptake of 137Cs per plant and/or area). This plant can take up about 15 Bq per plant of 137Cs and therefore it Fig. 3 Relationship between the total 137Cs uptake by plants can remove 137Cs from soil about 270 Bq m2 in one round and the total plant biomass. Each data point represents individual plants used in the experiments. The average of cultivation by considering the density of plants over unit values are exhibited (n3 to 9). The thin gray arrow area. It is noteworthy to consider why Kochia showed and the thick gray arrow denote Sunflower and Kochia, most excellent potential for 137Cs-targeted phytoremediation respectively.

 Environ. Control Biol. POTENTIAL RADIOCESIUM-TARGETED PHYTOREMEDIATION

seems to be more important than the TF value in the con- with low concentration of radionuclides. Water Air Soil text of 137Cs phytoremediation. To confirm this indication, Pollut. 88:167176. analysis of correlation between total 137Cs uptake and plant Hiyama, A., Nohara, C., Kinjo, S., Taira, W., Gima, S., Tanahara, A., Otaki, J. M. 2012. The biological impacts of the biomass was carried out (Fig. 3). The result showed that Fukushima nuclear accident on the pale grass blue butterfly. 2  there is positive relationship between these values (R Sci. Rep. 2: 570. 0.79). Moreover, statistical analysis also showed that con- Kirk, G. J., Staunton, S. 1989. On predicting the fate of radioac- tribution rate of plant biomass in total 137Cs uptake by plant tive caesium in soil beneah grassland. J. Soil. Sci. 40:7184. was calculated to be 91.3% (P0.001). These suggest that Kobayashi, D., Okouchi, T., Yamagami, M., Shinano, T. 2014. Verification of radiocesium decontamination from farmlands ability for 137Cs phytoremediation is largely dependent on by plants in Fukushima. J. Plant Res. 127:5156. plant biomass. Lasat, M. M., Fuhrmann, M., Ebbs, S. D., Cornish, J. E., Kochian, However, values of TF and plant biomass are not inde- L. V. 1998. Phytoremediation of a radiocesium- pendent; high biomass is often associated with lower TF contaminated soil: Evaluation of Cesium-137 bioaccumulation because of growth dilution effects. We could find an ex- in the shoots of three plant species. J. Environ. Qual. 27: 165 169. ample showing the importance of TF in 137 Cs phytore- 137 Mimura, T., Miura, M., Komiyama, C., Miyamoto, M., Kitamura, mediation in our result. Both TF and total amount of Cs A. 2014. Measurements of gamma ()-emitting taken up in Kochia were at the similar level in Sunflower radionuclides with a high-purity germanium detector: the despite the biomass of Kochia was about half of Sunflower methods and reliability of our environmental assessments on (Fig. 3). This indicates that TF should be considered in the Fukushima 1 Nuclear Power Plant accident. J. Plant Res.  part in order to evaluate the plant ability of 137Cs phytore- 127:91 97. 137 Møller, A. P., Hagiwara, A., Matsui, S., Kasahara, S., Kawatsu, K., mediation. To achieve successful Cs-targeted phytore- Mishiumi, I., Suzuki, H., Ueda, K., Mousseau, T. A. 2012. mediation, it is necessary to screen a plant that possesses Abundance of birds in Fukushima as judged from Chernobyl. unusually high abilities for 137 Cs uptake coping with Environ. Pollut. 164:3639. growth. 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