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Radiocesium contamination behavior and its effect on potassium absorption in tropical or subtropical plants
Journal of Environmental Radioactivity 86 (2006) 241e250 www.elsevier.com/locate/jenvrad
Radiocesium contamination behavior and its effect on potassium absorption in tropical or subtropical plants C. Carvalho, R.M. Anjos*, B. Mosquera, K. Macario, R. Veiga Instituto de Fı´sica, Universidade Federal Fluminense, Av. Litoraˆnea s/n, Gragoata´, Nitero´i, Rio de Janeiro, Cep 24210-340, Brazil Received 19 May 2005; received in revised form 7 September 2005; accepted 7 September 2005 Available online 25 October 2005
Abstract The accumulation and long-term decline of radiocesium contamination in tropical plant species was studied through measurements of gamma-ray spectra from pomegranate (Punica granatum) and chili pepper (Capsicum fructescens) trees. The plants were originally grown at a 137Cs contaminated site (where a radiological accident occurred in the city of Goiaˆnia, Brazil, in 1987), and transplanted to uncontaminated soil, so that the main source of contamination of the new leaves and fruits would be the fraction of the available radiocesium in the body of the plants. Measurements of 137Cs and 40K concentrations along the roots, main trunk, twigs, leaves and fruits before and after the transplant process of both plant species indicated a direct competition between Cs and K ions, suggesting that these elements could have a common accumulation mechanism. Cesium transfer factors from soil to pomegranate, green and red chili pepper fruits were evaluated as 0.4 G 0.1, 0.06 G 0.01 and 0.05 G 0.01, respectively. Biological halflife values due to 137Cs translocation from the tree reservoir (BHLT) were calculated as 0.30 years for pomegranate, 0.12 years and 0.07 years for red and green peppers, respectively. Ó 2005 Elsevier Ltd. All rights reserved. Keywords: Long-term decline;
137
Cs and
40
K distributions; Pomegranate and chili pepper trees
* Corresponding author. Tel.: C55 21 2629 5770; fax: C55 21 2629 5887. E-mail address: [email protected] (R.M. Anjos). 0265-931X/$ - see front matter Ó 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.jenvrad.2005.09.003
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1. Introduction In recent years, there has been a growing interest in the evaluation of nutrient fluxes and radioactive contaminants in forest and agricultural ecosystems (Shaw and Bell, 1989, 1991; Myttenaere et al., 1993; Schell et al., 1996; Simon et al., 2002; Zhu et al., 2002; Mosquera et al., in press). In order to contribute to the understanding of the relative behavior of KC and CsC ions, the purpose of this work was to examine the concentration levels of 40K and 137Cs in pomegranate (Punica granatum) and chili pepper (Capsicum fructescens) trees in two different situations in the context of a nuclear accident: first, investigating the 137Cs contamination by root uptake from contaminated soil, and then, when the plant is transferred to ‘‘uncontaminated’’ soil (i.e. soil free from the specific 137Cs contamination caused by the radiological accident) so that the main source of the contamination of new leaves and fruits is the fraction of the available radiocesium in the body of the plant. Biological half-lives (BHL) of 137Cs for this second special situation, and analysis of how these radionuclides are distributed throughout these tropical plants are shown in this paper. Additionally, as there are no measurements available in the literature for pepper or pomegranate species, cesium transfer factors from soil to fruits are presented.
2. Material and methods Four chili pepper trees, around 80 cm high, and a pomegranate tree around 2 m high, which had been cultivated in the garden of one of the sites where the Goiaˆnia radiological accident occurred (IAEA, 1988; Health Physics, 1991) were collected. The ground where the chili pepper trees had been planted (except from the fourth one) was composed of a red soil containing construction remains with sandyeclayeloam texture. Features of the 137Cs contaminated soils are given in Table 1. Total potassium was low, 0.5 G 0.1 g kg1. In contrast, the ground where the pomegranate tree and the fourth chili pepper tree had been planted was composed of a black soil, also a sandyeclayeloam texture, but with a higher total potassium concentration, 2.9 G 0.3 g kg1. In order to obtain a soil sampling that would be representative of the cesium available to each plant, about 10 samples of about 200 g of soil were collected within the rooting zone for each plant. Samples were taken from root, trunk, twigs, leaves and fruits of two chili pepper trees (referred to as CCP1 and CCP2), from the leaves and fruits of a third chili pepper tree (CCP3), and from a pomegranate tree (referred to as CPG). A fourth chili pepper tree (CCP4) was planted on the same kind of soil where CPG had been planted and had only its fruits sampled. Table 1 Overview of the main features of
pH (KCl) Sand (%) Clay (%) Silt (%) C (%) CEC (cmolc kg1) K (g kg1)
137
Cs in accidentally contaminated and uncontaminated soils
Contaminated soil (CCP1, CCP2 and CCP3 trees)
Contaminated soil (CCP4 and CPG trees)
Uncontaminated soil (DCP and DPG trees)
6.300 G 0.005 70.4 G 2.6 6.6 G 0.4 20.0 G 0.7 1.5 G 0.1 5.4 G 0.2 0.5 G 0.1
5.761 G 0.005 80.8 G 2.3 5.9 G 0.2 13.3 G 0.4 1.7 G 0.1 5.3 G 0.2 2.9 G 0.3
5.808 G 0.005 55.2 G 1.4 10.0 G 0.3 34.8 G 0.9 2.1 G 0.1 10.8 G 0.4 3.3 G 0.3
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243
Each sampling of roots, main trunks, twigs and leaves, was taken from five replicates for CCP1 and CCP2. Since chili peppers produce simultaneously both green and red fruits (red pepper is a green fruit ripened), about 150 units of each were collected, such that three replicates of green and three of red fruits were produced for each plant CCP1, CCP2, CCP3 and CCP4. Each sampling of soil, twigs and leaves, was taken from five replicates for CPG. For each fruit sample of the pomegranate tree five fruits were used, producing five replicates. The chili pepper tree CCP3 and the pomegranate tree CPG were transplanted to another site with uncontaminated soil. This soil was black, with a sandyeclayeloam texture, and a total potassium concentration of 3.3 G 0.3 g kg1. Soil characteristics are also given in Table 1. The transplanted CCP3 and CPG trees are referred to as DCP and DPG, respectively. Samples of green and red peppers from DCP were simultaneously collected during one year. About 100 units of green and red chili peppers were collected in each sampling, resulting in three replicates from each of them. Samples of pomegranate from DPG were collected during three years. About five fruits were collected in each sampling. At the end of this period, samples of root, trunk, twig, leaves and fruit of these plants were also analyzed. Sample preparation and analysis were carried out at the Laboratory of Radioecology (LARA) of the Physics Institute of the Universidade Federal Fluminense. The root, main trunk, twig, leaf and fruit samples were first washed with distilled water, while the soil samples were sieved through a 1-mm screen. Then they were submitted to a drying process, at 110 C. Additionally, the vegetable samples were ground to powder. Afterwards, all samples were packed into cylindrical plastic containers, dryweighed and sealed. The dry weights of each vegetable and soil samples were about 10 and 200 g, respectively. The amount of 137Cs and 40K in the samples was determined by standard gamma-ray spectroscopy using a well-type, 3 ! 3 inch NaI(Tl) detector. Placing samples inside appropriate shielding for low-level counting, the measurement time for each sample was about 1.5 ! 104 s. Radionuclide concentrations in soil and plants were determined as described by Mosquera et al. (in press). The uncertainties of the specific 137Cs activity of soil samples were below 5% and between 5e10% for plant samples. The uncertainties of the specific 40K activity of plant samples were between 10e15%. The detection limit was estimated to be 7.0 Bq kg1 for 137Cs and 75 Bq kg1 for 40K.
3. Results The soil to plant transfer factor (TF) is a parameter that gives the transfer rate of radionuclides from soil to plants. TF is expressed as the ratio between the radionuclide concentration in the dried edible part of the plant and that in the oven dried soil and is calculated as follows (IAEA, 1994): TF Z (Bq kg1 dry fruit weight)/(Bq kg1 dry soil weight). According to Carini (2001), TF values for soil to fruit transfer of cesium (converted to Bq kg1 dry weight fruit to Bq kg1 dry weight soil) show a wide range of values covering five orders of magnitude, from 103 to 101, and are higher in tropical rather than in temperate fruits. Woody trees and herbaceous plants from tropical and subtropical regions show a range of values from 9.0 ! 103 to 1.9 ! 101. The small number of plants studied in this work could be considered a drawback, as well as the limited number of soil systems with variable mineral composition, pH, K concentration, organic matter, etc. Despite this, there is such a lack of information considering radiocesium transfer factors for tropical and subtropical plants, that this work does add important data, providing TF values for the plants. Using the mean 137Cs concentration in the contaminated ground where the pomegranate was planted (73 G 10 kBq kg1) and the measured 137Cs concentration in pomegranate fruits presented in Table 2, cesium TF value from soil to pomegranate was calculated as 0.36 G 0.09.
C. Carvalho et al. / J. Environ. Radioactivity 86 (2006) 241e250
244 Table 2 Mean values of
137
Sample
Cs and
40
K concentrations in the younger and older parts of a pomegranate tree (Punica granatum)
Contaminated plant (CPG)
Roots Main trunk Twigs Leaves Fruit
Decontaminated plant (DPG)
137
Cs (Bq kg1)
40
K (Bq kg1)
137
Cs/40K
e e 23 332 G 3054 64 987 G 9421 26 650 G 3238
e e 242 G 30 654 G 72 414 G 68
e e 96.4 99.4 64.4
137
Cs (Bq kg1)
40
K (Bq kg1)
137
Cs/40K
1252 G 100 800 G 66 190 G 40 338 G 60 226 G 22
134 G 13 91 G 10 187 G 20 543 G 60 471 G 65
9.3 8.8 1.0 0.6 0.5
CPG samples were analyzed when this tree was planted in 137Cs contaminated site and DPG samples were analyzed three years after this pomegranate tree had been transplanted to a site with uncontaminated soil. The sampling of roots, tree trunks, twigs, leaves and fruits was taken from five replicates from each plant. The uncertainties represent the standard deviation from the mean.
Similarly, using the mean 137Cs concentration in the soil from CCP1 (17 G 1 kBq kg1), CCP2 (42 G 2 kBq kg1), and CCP3 (32 G 2 kBq kg1), along with 137Cs concentrations in chili pepper fruits CCP1 and CCP2 (Table 3), green pepper fruits (1.8 G 0.2 kBq kg1) and red peppers (1.7 G 0.3 kBq kg1) from CCP3, the mean cesium TF values from soil to green and red chili peppers were calculated as 0.063 G 0.006 and 0.053 G 0.006, respectively. As potassium content in different soils could be interfering in the accuracy of 137Cs TFs obtained, in order to verify its variability we determined for plant CCP4 the TFs from soil to green and red chili peppers finding as 0.060 G 0.009 and 0.050 G 0.008, respectively. Since 21 G 0.2 kBq kg1 of 137Cs was observed in the ground from CCP4, and 1.2 G 0.1 kBq kg1 in green and 1.0 G 0.1 kBq kg1 in red chili pepper fruits, there are no tangible indications that the soil would be influencing the TF directly, and so these TF results suggest that higher transfer in pomegranate is an intrinsic feature of this kind of plant and not due to the higher concentration and availability of potassium and cesium in the soil. Table 3 Mean values of fructescens) Sample
137
Cs and
40
K concentrations in the younger and older parts of two chili pepper trees (Capsicum
Contaminated plant
Decontaminated plant
CCP1 137
Cs (Bq kg1) Roots Main trunk Twigs Leaves Green pepper Red pepper
961 G 78 442 G 38
CCP2 40
K (Bq kg1)
137
40
Cs/ K
137
Cs (Bq kg1)
DCP 40
K (Bq kg1)
137
40
Cs/ K
137 40 Cs K (Bq kg1) (Bq kg1)
137
127 G 11 275 G 20
0.30 0.54
245 G 14 3.9 236 G 20 1.9
2096 G 167 241 G 38 8.7 1108 G 89 214 G 32 5.2
1042 G 86 473 G 43 2.2 3073 G 518 1060 G 99 2.9 1225 G 102 370 G 36 3.3
2489 G 195 472 G 53 5.3 6149 G 474 935 G 10 6.6 2548 G 239 342 G 48 7.4
82 G 7 1232 G 243 0.07 40 G 10 2200 G 421 0.02 8 G 1 1328 G 197 0.006
1021 G 84
1933 G 198 612 G 92 3.2
16 G 2
814 G 80 1.2
450 G 50 505 G 60
Cs/40K
1001 G 184 0.016
CCP1 and CCP2 were analyzed immediately after being collected from a 137Cs contaminated site and DCP was analyzed one year after being transplanted to a site with uncontaminated soil. The sampling of roots, tree trunks, twigs and leaves was taken from five replicates from each plant. The uncertainties represent the standard deviation from the mean.
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Additionally, these TF values are in agreement with the range of soil to fruit transfer factors for tropical and subtropical fruits observed by Carini (2001), showing a higher transfer of cesium to pomegranate when compared to chili peppers. Furthermore, the results for chili peppers revealed an interesting behavior. Although both green and red peppers were produced simultaneously by the same plant, the observed TFs seem to be slightly different. This observation compelled us to study the distribution of salts in the different parts of the plant. Therefore, 137Cs and 40K concentrations along the roots, main trunk, twigs, leaves and fruit of these two plants were evaluated. Table 2 shows the mean values of specific activities of these radionuclides for the younger (twigs, leaves and fruit) and older parts (main trunk) of a pomegranate tree, where CPG samples were analyzed while the pomegranate tree was still planted on 137 Cs contaminated site and DPG samples were analyzed three years after the pomegranate tree had been transplanted to a site with uncontaminated soil. Similarly, Table 3 shows 137Cs and 40 K concentrations in the different parts of the three chili pepper trees. CCP1 and CCP2 were analyzed immediately after being collected from a 137Cs contaminated site and DCP was analyzed one year after being transplanted to a site with uncontaminated soil. Even though there are no roots and main trunk sampling from pomegranate in the contaminated soil, it is possible to observe a similar distribution of Cs and K in the other components of CPG and CCP1 and CCP2 (Tables 2 and 3): the younger parts present higher 137Cs and 40K concentrations than the older parts. The concentration of these radionuclides in the different organs of the plant decreases on the whole according to foliage O fruits O twigs O wood or main trunk. This behavior has also been observed for other tropical and temperate trees (Myttenaere et al., 1993; Mosquera et al., in press). Furthermore, results shown in Table 3 for the fruit samples suggest that for CCP1 and CCP2, the green fruits have higher 137Cs concentration than the red ones, corroborating that 137Cs concentrations in plant organs are greater in younger tissues. Potassium levels also seem to depend on the age of the plant organ, but unlike Cs its concentration increases as the pepper fruits aged (turn red). These differences between 137Cs and 40 K distribution suggest that the elements could be competing within plant tissues as a function of tissue age. Competition phenomenon appears even clearer when the distribution of these radionuclides is investigated from tissues of DCP and DPG. These plants were transplanted to uncontaminated soil so that the 137Cs contamination of leaves and fruits would only occur from the radiocesium available in the body of the plant. Fig. 1 shows the 137Cs and 40K distributions in pomegranate fruits with time. The empty squares represent the fruits sampled when the pomegranate tree was still planted on contaminated soil, whereas the filled squares represent the fruits sampled after it was transplanted to uncontaminated soil. The analysis of Table 2 together with Fig. 1 discloses a new situation where there is an inversion of 137Cs levels in the different organs of the plant, as the available radionuclide was being redistributed to the younger parts of the plant. In the end, the youngest parts of DPG present lower specific 137Cs activity than other older parts, whereas the mean distribution of 40K has not changed. This last result is expected, since potassium is still available in the uncontaminated soil. On the other hand, cesium behavior suggests that there is an amount of radiocesium in the body of the plant that will remain retained in the main trunk and will just end up by the physical decay of 137Cs. This same behavior can also be observed in Fig. 2 and Table 3 for 137Cs and 40K distributions in chili pepper tree DCP. Furthermore, relative 137Cs and 40K levels in green and red peppers show a new configuration: the 137Cs concentration is now higher in the red
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Fig. 1. Time dependence of radionuclides concentrations in pomegranate fruits: (a) 137Cs, where the solid line represents a single exponential function fit which provides lT value of 0.19 G 0.01 months1 (R2 Z 0.99); (b) 40K, empty squares represent the fruit sampled when the pomegranate tree was planted on contaminated soil, whereas the filled squares represent the fruit sampled after this tree was transplanted to uncontaminated soil. This tree was transplanted to uncontaminated soil during fruit sampling of third point. The samplings of fruits were taken from five replicates of one fruit each. The error bars represent the standard deviation of the mean.
than in the green peppers, while the 40K concentration is higher in the green than in the red peppers. Slower cesium loss in red chili pepper fruits is likely because the chili is not growing to the extent the green chili is and therefore the cesium is not being moved as fast to other parts of the
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247
Fig. 2. Time dependence of radionuclides concentrations in green and red chili peppers: (a) 137Cs, where solid and dotted lines represent single exponential function fits which provide lT values of 0.89 G 0.06 months1 (R2 Z 0.91) and 0.47 G 0.02 months1 (R2 Z 0.92) for green and red chili peppers, respectively; (b) 40K, where solid and dotted lines represent fits of Eq. (2) which provides k values of 0.26 G 0.05 months1 (R2 Z 0.97) and 0.49 G 0.02 months1 (R2 Z 0.95) for green and red chili peppers, respectively. About 100 units of green and red chili peppers were collected from each sampling, resulting in three replicates from each of them. The error bars represent the standard deviation of the mean.
plant and the mass of the red chili is not changing. The green chili is still growing, the mass increases, the potassium is still being picked up and placed in the chili and the cesium concentration decreases. The potassium increases in the green chili because it is placed in a higher potassium soil and it is still growing. The red chili is not growing as quickly and therefore you do not see the increase in potassium that was seen in the green chili pepper.
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These results suggest that with the decrease in 137Cs levels in the body of the plant, the potassium tends to return and be redistributed by the different organs of the plant, which had formerly been occupied by cesium. Such behavior confirms the occurrence of a direct competition between Cs and K ions during the accumulation process throughout the plant indicating that the two elements have a common accumulation mechanism and this competition could be described by means of the number of sites available to the ion. If the percentage of sites occupied by cesium is the same as the percentage of cesium in the total amount of cesium C potassium, then it is likely that site availability would be determining cesium levels. It is important to notice that if on the one hand the isotope 137Cs represents all the cesium in the plant, being product of contamination, on the other hand the isotope 40K represents just a fraction of the total amount of potassium in the plant. The natural abundance of such isotope is 1.17 ! 104. Also, the half-life of 40K is much greater than that of 137Cs. These two factors together make the relation between the numbers of Cs atoms in a sample with same activity of both radioisotopes 2.7 ! 1012 of the total K atoms. Even though the number of atoms of cesium and potassium is of such a different order of magnitude the competition still seems to occur as potassium concentration grows during decontamination process. The biological half-life of 137Cs after a nuclear fallout can be evaluated, for the soil system investigated, from Fig. 1 for pomegranate and Fig. 2 for both red and green chili peppers, because the main source of the contamination of new leaves and fruits is the fraction of the available radiocesium in the body of the plant. It is expected for 137Cs concentrations to decrease faster than its physical half-life because of the loss of 137Cs by leaves or fruits, plant growth, transfer back to the soil, etc. This loss estimate can be estimated using a compartment model for long-term radiocesium contamination of fruit trees proposed by Antonopoulos-Domis et al. (1990, 1991, 1996). According to this model, the loss of 137Cs concentration in fruits or leaves can be described by the sum of two exponentials: CCs ðtÞZA expð lT tÞCB expð lU tÞ
ð1Þ
where, A, B, lT O 0 and lU O 0 are constants. The first term of Eq. (1) corresponds to the translocation of cesium from the tree reservoir, and the second is due to root uptake. Given that this experiment was performed with the aim of investigating how a fraction of the available radiocesium in the body of the plant can be redistributed to other permanent organs, the second term can be neglected. This assumption can be confirmed analyzing the data fit showed in Fig. 1, for instance. The solid line represents a single exponential function fit which provides the equation Y Z 57 356 exp(0.19t) with a correlation coefficient R2 Z 0.99. If a double exponential function fit is performed the equation becomes Y Z 67 468 exp(0.21t) C 196 exp(0.02t); with R2 Z 0.96. This result shows that a single component function fits the data slightly better than a double exponential. Similar results are obtained when the data of Fig. 2a are fitted. For this reason, the behavior of 137Cs distribution in DCP and DPG could be described by a single exponential function and the constant lT deduced for pomegranate and red and green chili peppers. A second component, representing root uptake, might be more important at longer time period past contamination. From lT were obtained the following biological half-life values due to 137Cs translocation from the tree reservoir (BHLT): 0.30, 0.12 and 0.07 years for pomegranate and red and green peppers, respectively. Although there are no values available in literature for the same species of pomegranate, we can announce that our result is of the same order of magnitude of BHLT values found for similar fruit trees. Antonopoulos-Domis et al.
C. Carvalho et al. / J. Environ. Radioactivity 86 (2006) 241e250
249
(1996) obtained BHLT values of 0.60 G 0.6 years for apple, peach and sweet cherries trees, whereas biological half-life values due to root uptake (BHLU) for these fruit trees ranged from 1.4 to 3.2 years. At this point it is interesting to note that the BHLT of pomegranate is about 10 times lower than BHLU and about 100 times lower than the physical decay constant of 137Cs (T1/2 Z 30.2 years). In the case of chili peppers these ratios are 25 and 250 times lower, respectively. Knowing the rate at which such contaminant decline within various ecosystems components can be important for evaluating the length and severity of potential risks to resident species. The soil where the chili pepper trees were initially planted was poor in nutrients, and this could have facilitated a high uptake of radiocesium by the plants. DPG was transplanted to the same kind of soil, whereas DCP was transplanted to manured soil, which would explain the increase of K concentration after transplantation. Considering this behavior, the K enhancement can also be estimated by a model that takes into account the radionuclide transfer between the soil and one biological compartment that has reached a steady-state (Fievet and Plet, 2003). This model can be expressed by the equation: CðtÞZA½1 expð ktÞ
ð2Þ
When t Z t1/2 Z ln 2/k, C(t1/2) is equal to half the steady-state value and can be referred to as the biological half-life (BHLK). So, BHLK for 40K in green and red peppers are 0.22 and 0.12 years, respectively. 4. Conclusions Our results have shown that 137Cs and 40K have similar distributions among some tree compartments. We have also shown the occurrence of a direct competition between Cs and K ions during the process of accumulation throughout the plant, suggesting that the two elements could have a common accumulation mechanism. The study of biological half-life values due to 137Cs translocation from the tree reservoir indicate that its values are of the order of months. Such information is important for the reclaiming of agricultural ecosystems after a nuclear fallout. Knowing how tropical trees decontaminate after a period of growth in a 137Cs contaminated area could be of interest in terms of risk assessment, and in terms of understanding the process involved in translocation of small ions in tropical or subtropical species. Acknowledgments The authors would like to thank the Brazilian financial agencies: CNPq and CAPES. We are grateful to Mr. Fabiano Veiga for precious help with the plants cultivation, Dr. A.E. Oliveira (IRDeCNEN) for donating the 137Cs standard and researchers of LAGEMAR and Instituto de Geoquı´mica of UFF by soil analysis. Constructive comments from the anonymous referee were highly appreciated. References Antonopoulos-Domis, M., Clouvas, A., Gagianas, A., 1990. Compartment model for long-term contamination prediction in deciduous fruit trees after a nuclear accident. Health Physics 58, 737e741.
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Antonopoulos-Domis, M., Clouvas, A., Gagianas, A., 1991. Radiocesium dynamics in fruit trees following the Chernobyl accident. Health Physics 61, 837e842. Antonopoulos-Domis, M., Clouvas, A., Gagianas, A., 1996. Long term radiocesium contamination of fruit trees following the Chernobyl accident. Health Physics 71, 910e914. Carini, F., 2001. Radionuclide transfer from soil to fruit. Journal of Environmental Radioactivity 52, 237e279. Fievet, B., Plet, D., 2003. Estimating biological half-lives of radionuclides in marine compartments from environmental time-series measurements. Journal of Environmental Radioactivity 65, 91e107. Health Physics, 1991. The Goiaˆnia radiation accident. Health Physics 60 (special issue). IAEA, 1988. The Radiological Accident in Goiaˆnia. International Atomic Energy Agency, Vienna. IAEA, 1994. Handbook of Parameters Values for the Prediction of Radionuclide Transfer in Temperate Environments. Technical Report Series No. 364. International Atomic Energy Agency, Vienna. Mosquera, B., Carvalho, C., Veiga, R., Mangia, L., Anjos, R.M. 137Cs distribution in tropical fruit trees after soil contamination. Environmental and Experimental Botany, in press. Myttenaere, C., Shell, W.R., Thiry, Y., Sombre, L., Ronneau, C., van der Stegen de Schrieck, J., 1993. Modelling of Cs137 cycling in forests: recent developments and research needed. The Science of the Total Environment 136, 77e91. Schell, W.R., Linkov, I., Myttenaere, C., Morel, B., 1996. A dynamic model for evaluating radionuclide distribution in forest from nuclear accidents. Health Physics 70, 1e18. Shaw, G., Bell, J.N.B., 1989. The kinetics of caesium absorption by roots of winter wheat and the possible consequences for the derivation of soil-to-pant transfer factors for radiocaesium. Journal of Environmental Radioactivity 10, 213e 231. Shaw, G., Bell, J.N.B., 1991. Competitive effects of potassium and ammonium on caesium uptake kinetics in wheat. Journal of Environmental Radioactivity 13, 283e296. Simon, S.L., Graham, J.C., Terp, S.D., 2002. Uptake of 40K and 137Cs in native plants of the Marshall Islands. Journal of Environmental Radioactivity 59, 223e243. Zhu, Y.G., Shaw, G., Nisbet, A.F., Wilkins, B.T., 2002. Effect of external potassium supply and plant age on the uptake of radiocaesium (137Cs) by broad bean (Vicia faba): interpretation of results from a large-scale hydroponic study. Environmental and Experimental Botany 47, 173e187.
Radiocesium contamination behavior and its effect on potassium absorption in tropical or subtropical plants C. Carvalho, R.M. Anjos*, B. Mosquera, K. Macario, R. Veiga Instituto de Fı´sica, Universidade Federal Fluminense, Av. Litoraˆnea s/n, Gragoata´, Nitero´i, Rio de Janeiro, Cep 24210-340, Brazil Received 19 May 2005; received in revised form 7 September 2005; accepted 7 September 2005 Available online 25 October 2005
Abstract The accumulation and long-term decline of radiocesium contamination in tropical plant species was studied through measurements of gamma-ray spectra from pomegranate (Punica granatum) and chili pepper (Capsicum fructescens) trees. The plants were originally grown at a 137Cs contaminated site (where a radiological accident occurred in the city of Goiaˆnia, Brazil, in 1987), and transplanted to uncontaminated soil, so that the main source of contamination of the new leaves and fruits would be the fraction of the available radiocesium in the body of the plants. Measurements of 137Cs and 40K concentrations along the roots, main trunk, twigs, leaves and fruits before and after the transplant process of both plant species indicated a direct competition between Cs and K ions, suggesting that these elements could have a common accumulation mechanism. Cesium transfer factors from soil to pomegranate, green and red chili pepper fruits were evaluated as 0.4 G 0.1, 0.06 G 0.01 and 0.05 G 0.01, respectively. Biological halflife values due to 137Cs translocation from the tree reservoir (BHLT) were calculated as 0.30 years for pomegranate, 0.12 years and 0.07 years for red and green peppers, respectively. Ó 2005 Elsevier Ltd. All rights reserved. Keywords: Long-term decline;
137
Cs and
40
K distributions; Pomegranate and chili pepper trees
* Corresponding author. Tel.: C55 21 2629 5770; fax: C55 21 2629 5887. E-mail address: [email protected] (R.M. Anjos). 0265-931X/$ - see front matter Ó 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.jenvrad.2005.09.003
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1. Introduction In recent years, there has been a growing interest in the evaluation of nutrient fluxes and radioactive contaminants in forest and agricultural ecosystems (Shaw and Bell, 1989, 1991; Myttenaere et al., 1993; Schell et al., 1996; Simon et al., 2002; Zhu et al., 2002; Mosquera et al., in press). In order to contribute to the understanding of the relative behavior of KC and CsC ions, the purpose of this work was to examine the concentration levels of 40K and 137Cs in pomegranate (Punica granatum) and chili pepper (Capsicum fructescens) trees in two different situations in the context of a nuclear accident: first, investigating the 137Cs contamination by root uptake from contaminated soil, and then, when the plant is transferred to ‘‘uncontaminated’’ soil (i.e. soil free from the specific 137Cs contamination caused by the radiological accident) so that the main source of the contamination of new leaves and fruits is the fraction of the available radiocesium in the body of the plant. Biological half-lives (BHL) of 137Cs for this second special situation, and analysis of how these radionuclides are distributed throughout these tropical plants are shown in this paper. Additionally, as there are no measurements available in the literature for pepper or pomegranate species, cesium transfer factors from soil to fruits are presented.
2. Material and methods Four chili pepper trees, around 80 cm high, and a pomegranate tree around 2 m high, which had been cultivated in the garden of one of the sites where the Goiaˆnia radiological accident occurred (IAEA, 1988; Health Physics, 1991) were collected. The ground where the chili pepper trees had been planted (except from the fourth one) was composed of a red soil containing construction remains with sandyeclayeloam texture. Features of the 137Cs contaminated soils are given in Table 1. Total potassium was low, 0.5 G 0.1 g kg1. In contrast, the ground where the pomegranate tree and the fourth chili pepper tree had been planted was composed of a black soil, also a sandyeclayeloam texture, but with a higher total potassium concentration, 2.9 G 0.3 g kg1. In order to obtain a soil sampling that would be representative of the cesium available to each plant, about 10 samples of about 200 g of soil were collected within the rooting zone for each plant. Samples were taken from root, trunk, twigs, leaves and fruits of two chili pepper trees (referred to as CCP1 and CCP2), from the leaves and fruits of a third chili pepper tree (CCP3), and from a pomegranate tree (referred to as CPG). A fourth chili pepper tree (CCP4) was planted on the same kind of soil where CPG had been planted and had only its fruits sampled. Table 1 Overview of the main features of
pH (KCl) Sand (%) Clay (%) Silt (%) C (%) CEC (cmolc kg1) K (g kg1)
137
Cs in accidentally contaminated and uncontaminated soils
Contaminated soil (CCP1, CCP2 and CCP3 trees)
Contaminated soil (CCP4 and CPG trees)
Uncontaminated soil (DCP and DPG trees)
6.300 G 0.005 70.4 G 2.6 6.6 G 0.4 20.0 G 0.7 1.5 G 0.1 5.4 G 0.2 0.5 G 0.1
5.761 G 0.005 80.8 G 2.3 5.9 G 0.2 13.3 G 0.4 1.7 G 0.1 5.3 G 0.2 2.9 G 0.3
5.808 G 0.005 55.2 G 1.4 10.0 G 0.3 34.8 G 0.9 2.1 G 0.1 10.8 G 0.4 3.3 G 0.3
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Each sampling of roots, main trunks, twigs and leaves, was taken from five replicates for CCP1 and CCP2. Since chili peppers produce simultaneously both green and red fruits (red pepper is a green fruit ripened), about 150 units of each were collected, such that three replicates of green and three of red fruits were produced for each plant CCP1, CCP2, CCP3 and CCP4. Each sampling of soil, twigs and leaves, was taken from five replicates for CPG. For each fruit sample of the pomegranate tree five fruits were used, producing five replicates. The chili pepper tree CCP3 and the pomegranate tree CPG were transplanted to another site with uncontaminated soil. This soil was black, with a sandyeclayeloam texture, and a total potassium concentration of 3.3 G 0.3 g kg1. Soil characteristics are also given in Table 1. The transplanted CCP3 and CPG trees are referred to as DCP and DPG, respectively. Samples of green and red peppers from DCP were simultaneously collected during one year. About 100 units of green and red chili peppers were collected in each sampling, resulting in three replicates from each of them. Samples of pomegranate from DPG were collected during three years. About five fruits were collected in each sampling. At the end of this period, samples of root, trunk, twig, leaves and fruit of these plants were also analyzed. Sample preparation and analysis were carried out at the Laboratory of Radioecology (LARA) of the Physics Institute of the Universidade Federal Fluminense. The root, main trunk, twig, leaf and fruit samples were first washed with distilled water, while the soil samples were sieved through a 1-mm screen. Then they were submitted to a drying process, at 110 C. Additionally, the vegetable samples were ground to powder. Afterwards, all samples were packed into cylindrical plastic containers, dryweighed and sealed. The dry weights of each vegetable and soil samples were about 10 and 200 g, respectively. The amount of 137Cs and 40K in the samples was determined by standard gamma-ray spectroscopy using a well-type, 3 ! 3 inch NaI(Tl) detector. Placing samples inside appropriate shielding for low-level counting, the measurement time for each sample was about 1.5 ! 104 s. Radionuclide concentrations in soil and plants were determined as described by Mosquera et al. (in press). The uncertainties of the specific 137Cs activity of soil samples were below 5% and between 5e10% for plant samples. The uncertainties of the specific 40K activity of plant samples were between 10e15%. The detection limit was estimated to be 7.0 Bq kg1 for 137Cs and 75 Bq kg1 for 40K.
3. Results The soil to plant transfer factor (TF) is a parameter that gives the transfer rate of radionuclides from soil to plants. TF is expressed as the ratio between the radionuclide concentration in the dried edible part of the plant and that in the oven dried soil and is calculated as follows (IAEA, 1994): TF Z (Bq kg1 dry fruit weight)/(Bq kg1 dry soil weight). According to Carini (2001), TF values for soil to fruit transfer of cesium (converted to Bq kg1 dry weight fruit to Bq kg1 dry weight soil) show a wide range of values covering five orders of magnitude, from 103 to 101, and are higher in tropical rather than in temperate fruits. Woody trees and herbaceous plants from tropical and subtropical regions show a range of values from 9.0 ! 103 to 1.9 ! 101. The small number of plants studied in this work could be considered a drawback, as well as the limited number of soil systems with variable mineral composition, pH, K concentration, organic matter, etc. Despite this, there is such a lack of information considering radiocesium transfer factors for tropical and subtropical plants, that this work does add important data, providing TF values for the plants. Using the mean 137Cs concentration in the contaminated ground where the pomegranate was planted (73 G 10 kBq kg1) and the measured 137Cs concentration in pomegranate fruits presented in Table 2, cesium TF value from soil to pomegranate was calculated as 0.36 G 0.09.
C. Carvalho et al. / J. Environ. Radioactivity 86 (2006) 241e250
244 Table 2 Mean values of
137
Sample
Cs and
40
K concentrations in the younger and older parts of a pomegranate tree (Punica granatum)
Contaminated plant (CPG)
Roots Main trunk Twigs Leaves Fruit
Decontaminated plant (DPG)
137
Cs (Bq kg1)
40
K (Bq kg1)
137
Cs/40K
e e 23 332 G 3054 64 987 G 9421 26 650 G 3238
e e 242 G 30 654 G 72 414 G 68
e e 96.4 99.4 64.4
137
Cs (Bq kg1)
40
K (Bq kg1)
137
Cs/40K
1252 G 100 800 G 66 190 G 40 338 G 60 226 G 22
134 G 13 91 G 10 187 G 20 543 G 60 471 G 65
9.3 8.8 1.0 0.6 0.5
CPG samples were analyzed when this tree was planted in 137Cs contaminated site and DPG samples were analyzed three years after this pomegranate tree had been transplanted to a site with uncontaminated soil. The sampling of roots, tree trunks, twigs, leaves and fruits was taken from five replicates from each plant. The uncertainties represent the standard deviation from the mean.
Similarly, using the mean 137Cs concentration in the soil from CCP1 (17 G 1 kBq kg1), CCP2 (42 G 2 kBq kg1), and CCP3 (32 G 2 kBq kg1), along with 137Cs concentrations in chili pepper fruits CCP1 and CCP2 (Table 3), green pepper fruits (1.8 G 0.2 kBq kg1) and red peppers (1.7 G 0.3 kBq kg1) from CCP3, the mean cesium TF values from soil to green and red chili peppers were calculated as 0.063 G 0.006 and 0.053 G 0.006, respectively. As potassium content in different soils could be interfering in the accuracy of 137Cs TFs obtained, in order to verify its variability we determined for plant CCP4 the TFs from soil to green and red chili peppers finding as 0.060 G 0.009 and 0.050 G 0.008, respectively. Since 21 G 0.2 kBq kg1 of 137Cs was observed in the ground from CCP4, and 1.2 G 0.1 kBq kg1 in green and 1.0 G 0.1 kBq kg1 in red chili pepper fruits, there are no tangible indications that the soil would be influencing the TF directly, and so these TF results suggest that higher transfer in pomegranate is an intrinsic feature of this kind of plant and not due to the higher concentration and availability of potassium and cesium in the soil. Table 3 Mean values of fructescens) Sample
137
Cs and
40
K concentrations in the younger and older parts of two chili pepper trees (Capsicum
Contaminated plant
Decontaminated plant
CCP1 137
Cs (Bq kg1) Roots Main trunk Twigs Leaves Green pepper Red pepper
961 G 78 442 G 38
CCP2 40
K (Bq kg1)
137
40
Cs/ K
137
Cs (Bq kg1)
DCP 40
K (Bq kg1)
137
40
Cs/ K
137 40 Cs K (Bq kg1) (Bq kg1)
137
127 G 11 275 G 20
0.30 0.54
245 G 14 3.9 236 G 20 1.9
2096 G 167 241 G 38 8.7 1108 G 89 214 G 32 5.2
1042 G 86 473 G 43 2.2 3073 G 518 1060 G 99 2.9 1225 G 102 370 G 36 3.3
2489 G 195 472 G 53 5.3 6149 G 474 935 G 10 6.6 2548 G 239 342 G 48 7.4
82 G 7 1232 G 243 0.07 40 G 10 2200 G 421 0.02 8 G 1 1328 G 197 0.006
1021 G 84
1933 G 198 612 G 92 3.2
16 G 2
814 G 80 1.2
450 G 50 505 G 60
Cs/40K
1001 G 184 0.016
CCP1 and CCP2 were analyzed immediately after being collected from a 137Cs contaminated site and DCP was analyzed one year after being transplanted to a site with uncontaminated soil. The sampling of roots, tree trunks, twigs and leaves was taken from five replicates from each plant. The uncertainties represent the standard deviation from the mean.
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Additionally, these TF values are in agreement with the range of soil to fruit transfer factors for tropical and subtropical fruits observed by Carini (2001), showing a higher transfer of cesium to pomegranate when compared to chili peppers. Furthermore, the results for chili peppers revealed an interesting behavior. Although both green and red peppers were produced simultaneously by the same plant, the observed TFs seem to be slightly different. This observation compelled us to study the distribution of salts in the different parts of the plant. Therefore, 137Cs and 40K concentrations along the roots, main trunk, twigs, leaves and fruit of these two plants were evaluated. Table 2 shows the mean values of specific activities of these radionuclides for the younger (twigs, leaves and fruit) and older parts (main trunk) of a pomegranate tree, where CPG samples were analyzed while the pomegranate tree was still planted on 137 Cs contaminated site and DPG samples were analyzed three years after the pomegranate tree had been transplanted to a site with uncontaminated soil. Similarly, Table 3 shows 137Cs and 40 K concentrations in the different parts of the three chili pepper trees. CCP1 and CCP2 were analyzed immediately after being collected from a 137Cs contaminated site and DCP was analyzed one year after being transplanted to a site with uncontaminated soil. Even though there are no roots and main trunk sampling from pomegranate in the contaminated soil, it is possible to observe a similar distribution of Cs and K in the other components of CPG and CCP1 and CCP2 (Tables 2 and 3): the younger parts present higher 137Cs and 40K concentrations than the older parts. The concentration of these radionuclides in the different organs of the plant decreases on the whole according to foliage O fruits O twigs O wood or main trunk. This behavior has also been observed for other tropical and temperate trees (Myttenaere et al., 1993; Mosquera et al., in press). Furthermore, results shown in Table 3 for the fruit samples suggest that for CCP1 and CCP2, the green fruits have higher 137Cs concentration than the red ones, corroborating that 137Cs concentrations in plant organs are greater in younger tissues. Potassium levels also seem to depend on the age of the plant organ, but unlike Cs its concentration increases as the pepper fruits aged (turn red). These differences between 137Cs and 40 K distribution suggest that the elements could be competing within plant tissues as a function of tissue age. Competition phenomenon appears even clearer when the distribution of these radionuclides is investigated from tissues of DCP and DPG. These plants were transplanted to uncontaminated soil so that the 137Cs contamination of leaves and fruits would only occur from the radiocesium available in the body of the plant. Fig. 1 shows the 137Cs and 40K distributions in pomegranate fruits with time. The empty squares represent the fruits sampled when the pomegranate tree was still planted on contaminated soil, whereas the filled squares represent the fruits sampled after it was transplanted to uncontaminated soil. The analysis of Table 2 together with Fig. 1 discloses a new situation where there is an inversion of 137Cs levels in the different organs of the plant, as the available radionuclide was being redistributed to the younger parts of the plant. In the end, the youngest parts of DPG present lower specific 137Cs activity than other older parts, whereas the mean distribution of 40K has not changed. This last result is expected, since potassium is still available in the uncontaminated soil. On the other hand, cesium behavior suggests that there is an amount of radiocesium in the body of the plant that will remain retained in the main trunk and will just end up by the physical decay of 137Cs. This same behavior can also be observed in Fig. 2 and Table 3 for 137Cs and 40K distributions in chili pepper tree DCP. Furthermore, relative 137Cs and 40K levels in green and red peppers show a new configuration: the 137Cs concentration is now higher in the red
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Fig. 1. Time dependence of radionuclides concentrations in pomegranate fruits: (a) 137Cs, where the solid line represents a single exponential function fit which provides lT value of 0.19 G 0.01 months1 (R2 Z 0.99); (b) 40K, empty squares represent the fruit sampled when the pomegranate tree was planted on contaminated soil, whereas the filled squares represent the fruit sampled after this tree was transplanted to uncontaminated soil. This tree was transplanted to uncontaminated soil during fruit sampling of third point. The samplings of fruits were taken from five replicates of one fruit each. The error bars represent the standard deviation of the mean.
than in the green peppers, while the 40K concentration is higher in the green than in the red peppers. Slower cesium loss in red chili pepper fruits is likely because the chili is not growing to the extent the green chili is and therefore the cesium is not being moved as fast to other parts of the
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Fig. 2. Time dependence of radionuclides concentrations in green and red chili peppers: (a) 137Cs, where solid and dotted lines represent single exponential function fits which provide lT values of 0.89 G 0.06 months1 (R2 Z 0.91) and 0.47 G 0.02 months1 (R2 Z 0.92) for green and red chili peppers, respectively; (b) 40K, where solid and dotted lines represent fits of Eq. (2) which provides k values of 0.26 G 0.05 months1 (R2 Z 0.97) and 0.49 G 0.02 months1 (R2 Z 0.95) for green and red chili peppers, respectively. About 100 units of green and red chili peppers were collected from each sampling, resulting in three replicates from each of them. The error bars represent the standard deviation of the mean.
plant and the mass of the red chili is not changing. The green chili is still growing, the mass increases, the potassium is still being picked up and placed in the chili and the cesium concentration decreases. The potassium increases in the green chili because it is placed in a higher potassium soil and it is still growing. The red chili is not growing as quickly and therefore you do not see the increase in potassium that was seen in the green chili pepper.
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These results suggest that with the decrease in 137Cs levels in the body of the plant, the potassium tends to return and be redistributed by the different organs of the plant, which had formerly been occupied by cesium. Such behavior confirms the occurrence of a direct competition between Cs and K ions during the accumulation process throughout the plant indicating that the two elements have a common accumulation mechanism and this competition could be described by means of the number of sites available to the ion. If the percentage of sites occupied by cesium is the same as the percentage of cesium in the total amount of cesium C potassium, then it is likely that site availability would be determining cesium levels. It is important to notice that if on the one hand the isotope 137Cs represents all the cesium in the plant, being product of contamination, on the other hand the isotope 40K represents just a fraction of the total amount of potassium in the plant. The natural abundance of such isotope is 1.17 ! 104. Also, the half-life of 40K is much greater than that of 137Cs. These two factors together make the relation between the numbers of Cs atoms in a sample with same activity of both radioisotopes 2.7 ! 1012 of the total K atoms. Even though the number of atoms of cesium and potassium is of such a different order of magnitude the competition still seems to occur as potassium concentration grows during decontamination process. The biological half-life of 137Cs after a nuclear fallout can be evaluated, for the soil system investigated, from Fig. 1 for pomegranate and Fig. 2 for both red and green chili peppers, because the main source of the contamination of new leaves and fruits is the fraction of the available radiocesium in the body of the plant. It is expected for 137Cs concentrations to decrease faster than its physical half-life because of the loss of 137Cs by leaves or fruits, plant growth, transfer back to the soil, etc. This loss estimate can be estimated using a compartment model for long-term radiocesium contamination of fruit trees proposed by Antonopoulos-Domis et al. (1990, 1991, 1996). According to this model, the loss of 137Cs concentration in fruits or leaves can be described by the sum of two exponentials: CCs ðtÞZA expð lT tÞCB expð lU tÞ
ð1Þ
where, A, B, lT O 0 and lU O 0 are constants. The first term of Eq. (1) corresponds to the translocation of cesium from the tree reservoir, and the second is due to root uptake. Given that this experiment was performed with the aim of investigating how a fraction of the available radiocesium in the body of the plant can be redistributed to other permanent organs, the second term can be neglected. This assumption can be confirmed analyzing the data fit showed in Fig. 1, for instance. The solid line represents a single exponential function fit which provides the equation Y Z 57 356 exp(0.19t) with a correlation coefficient R2 Z 0.99. If a double exponential function fit is performed the equation becomes Y Z 67 468 exp(0.21t) C 196 exp(0.02t); with R2 Z 0.96. This result shows that a single component function fits the data slightly better than a double exponential. Similar results are obtained when the data of Fig. 2a are fitted. For this reason, the behavior of 137Cs distribution in DCP and DPG could be described by a single exponential function and the constant lT deduced for pomegranate and red and green chili peppers. A second component, representing root uptake, might be more important at longer time period past contamination. From lT were obtained the following biological half-life values due to 137Cs translocation from the tree reservoir (BHLT): 0.30, 0.12 and 0.07 years for pomegranate and red and green peppers, respectively. Although there are no values available in literature for the same species of pomegranate, we can announce that our result is of the same order of magnitude of BHLT values found for similar fruit trees. Antonopoulos-Domis et al.
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(1996) obtained BHLT values of 0.60 G 0.6 years for apple, peach and sweet cherries trees, whereas biological half-life values due to root uptake (BHLU) for these fruit trees ranged from 1.4 to 3.2 years. At this point it is interesting to note that the BHLT of pomegranate is about 10 times lower than BHLU and about 100 times lower than the physical decay constant of 137Cs (T1/2 Z 30.2 years). In the case of chili peppers these ratios are 25 and 250 times lower, respectively. Knowing the rate at which such contaminant decline within various ecosystems components can be important for evaluating the length and severity of potential risks to resident species. The soil where the chili pepper trees were initially planted was poor in nutrients, and this could have facilitated a high uptake of radiocesium by the plants. DPG was transplanted to the same kind of soil, whereas DCP was transplanted to manured soil, which would explain the increase of K concentration after transplantation. Considering this behavior, the K enhancement can also be estimated by a model that takes into account the radionuclide transfer between the soil and one biological compartment that has reached a steady-state (Fievet and Plet, 2003). This model can be expressed by the equation: CðtÞZA½1 expð ktÞ
ð2Þ
When t Z t1/2 Z ln 2/k, C(t1/2) is equal to half the steady-state value and can be referred to as the biological half-life (BHLK). So, BHLK for 40K in green and red peppers are 0.22 and 0.12 years, respectively. 4. Conclusions Our results have shown that 137Cs and 40K have similar distributions among some tree compartments. We have also shown the occurrence of a direct competition between Cs and K ions during the process of accumulation throughout the plant, suggesting that the two elements could have a common accumulation mechanism. The study of biological half-life values due to 137Cs translocation from the tree reservoir indicate that its values are of the order of months. Such information is important for the reclaiming of agricultural ecosystems after a nuclear fallout. Knowing how tropical trees decontaminate after a period of growth in a 137Cs contaminated area could be of interest in terms of risk assessment, and in terms of understanding the process involved in translocation of small ions in tropical or subtropical species. Acknowledgments The authors would like to thank the Brazilian financial agencies: CNPq and CAPES. We are grateful to Mr. Fabiano Veiga for precious help with the plants cultivation, Dr. A.E. Oliveira (IRDeCNEN) for donating the 137Cs standard and researchers of LAGEMAR and Instituto de Geoquı´mica of UFF by soil analysis. Constructive comments from the anonymous referee were highly appreciated. References Antonopoulos-Domis, M., Clouvas, A., Gagianas, A., 1990. Compartment model for long-term contamination prediction in deciduous fruit trees after a nuclear accident. Health Physics 58, 737e741.
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