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Uptake and transport of radioactive cesium and strontium into grapevines after leaf contamination
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Pergamon
0969-806X(94)00115-4
Radiat. Phys. Chem. Vol. 46, No. 1, pp. 61-69, 1995 Copyright © 1995 ElsevierScienceLtd Printed in Great Britain. All rights reserved 0969-806X/95 $9.50+ 0.00
U P T A K E A N D T R A N S P O R T OF R A D I O A C T I V E C E S I U M A N D S T R O N T I U M INTO G R A P E V I N E S A F T E R L E A F CONTAMINATION H. J. Z E H N D E R , 1 P. KOPP, 2 J. E I K E N B E R G , 2 U. F E L L E R 3 and J. J. OERTLI4¢ ~Swiss Federal Research Station for Fruit-Growing, Viticulture and Horticulture. CH-8820 W~denswil. 2Paul Scherrer Institute, CH-5232 Villigen-PSI. 3Institute of Plant Physiology, University of Bern. CH-3013 Bern and 41nstitute for Plant Science, Swiss Federal Institute of Technology, CH-8315 Lindau. Switzerland (Received 10 July 1994; accepted 31 August 1994)
Abstract--From1989 to 1993 the foliar uptake of radioactive strontium (Sr-85) and cesium (Cs-134) by
selected leaves of grapevine plants and the subsequent redistribution within the plants was examined under controlled conditions in a greenhouse. The radionuclides were applied as chlorides. These plants were grown in large pots containing a mixture of local soil and peat. Plant and soil samples were analyzed throughout the growing season and also during the following vegetation period. Only traces of the applied radiostrontium were taken up by the leaves. This element was essentially not redistributed within the plants. In contrast, radiocesium was easily taken up through the leaf surface, transported to other plant parts and to some extent released from the roots into the soil. Cesium reaching the soil may interact with clay particles causing a very reduced availability for plants. Therefore the soil may act as a long-term sink for radiocesinm. On the other hand, grape berries represent transient sinks. The cesium levels in the berries decreased again in a late phase of maturation, but the mechanisms causing this loss are not yet identified. During the second vegetation period, only a very minor proportion of the radiocesium taken up previously by the plants was present in the above ground parts.
solution, its uptake into plant roots and its transport to fruits, berries and nuts is rather low. These considerations motivated us to study the foliar uptake of radiocesium and radiostrontium, which is another interesting nuclide in this context. Both radioelements were present in the "Chernobyl fall-out'. Middleton (1959) reported that radiocesium was easily translocated from contaminated leaves to edible parts of crop plants, while radiostrontium was redistributed only to a very small extent. Strawberry plants were used in a first study (Zehnder et aL, 1993). However, strawberries are small plants and the risk of contaminating leaves and fruits in experiments with radioactive substances by contact is relatively high. Furthermore in most cultivated varieties of strawberries the fruit formation period is short. F o r further studies, we were therefore interested in using larger model plants, clearly separable into stem, leaves and fruits and having a long fruit formation period. Grapevine plants represent a suitable experimental system in this context. In a series o f studies carried out between 1989 and 1992 the foliar uptake of Cs-134 and Sr-85 into grapevine plants, their transport to other plant organs and finally also the release from the plants into the soil was investigated by repeated sampling and analysis of the plants and the soil. The accumulation of radioactivity in the berries was of special interest since this represents a pathway for these undesirable isotopes into the human food chain.
INTRODUCTION On 26 April 1986, one of the four reactors in the nuclear power station near the small Ukrainian town of Chernobyl exploded and started to burn In the following days and weeks winds drove air layers containing radioactive elements from the collapsed reactor over a large part of Europe. With the rain these substances were washed out and deposited on plants and on the soil surface. In the summer and autumn of 1986, the level of radioactivity in fruit, berries, nuts and some processed fruit products was slightly elevated in Switzerland (Zehnder, 1988). This increase in the radioactivity was mainly due to radioactive isotopes of cesium, Cs-137 and Cs-134. The joint occurrence of these two radionuclides in the appropriate ratio is typical for the nuclear accident mentioned above. F r o m the literature it is known that the interactions of cesium with soil particles are similar to those of potassium (Rich, 1968). Its availability for crop plants depends on soil properties, e.g. soil texture, clay mineralogy, contents of other cations, pH. Andersen (1967) stated that this element becomes less available for plants with increasing clay content. In Switzerland, most soils contain considerable amounts of clay. Therefore the availability of cesium in the soil tPresent address: Professor Dr J. J. Oertli, Schaienweg 25, CH-4107 Ettingen, Switzerland. 61
H.J. Zehnder et al.
62 MATERIALS AND METHODS
Plants and cultivation Grapevine plants, variety "Riesling x Sylvaner" (Mfiller-Thurgau), 2-3 years old were obtained from a nursery. They were planted in black 18.5 litre plastic pots in a 1 : 2 mixture of peat substrate and local soil (10-17kg total dry weight). To prevent contamination of the soil with radioactivity from the plant parts above ground, the top surface of the pots was covered with black plastic. Irrigation took place twice weekly from an underpot with periodic liquid fertilization using 0.25% Vegesan ~ (Hauert, Grossaffoltern, Switzerland). In spring the plants were pruned on two canes with five buds each. At a later date all emerged shoots of a cane were removed with the exception of one. On each of the remaining two shoots the first fully developed leaf reaching a size of between 50 and 80 cm 2 was contaminated with solutions of 134CSC1 or 85SRC12(see below). All leaves below those to be contaminated were previously removed. During the experiment plants were cultivated using normal procedures, and no further shoots and leaves were taken away. Pesticides were used only when necessary and only before starting the experiments. These experiments were carried out in the same greenhouse as that used in the strawberry study (Zehnder et al., 1993). The greenhouse floor was covered with plastic sheeting. The two short sides (front and back) of the greenhouse were made of fine plastic netting, the two long sides of polyester sheets. The plexiglass roof was fitted with a rainproof ventilation hole. These precautionary measures provided safety against loss of radioactivity and allowed air circulation.
Application of the radionuclides As in our previous experiments (Zehnder et al., 1993) we used the short-lived isotopes cesium-134 (half-life 2 years) and strontium-85 (half-life 65 days) instead of the long-lived isotopes (Cs-137, Sr-90) for safety reasons. Moreover, strontium-85 is a gamma emitter which can be measured more easily than strontium-90, which emits beta particles only. A suitable activity of carrier-free, aqueous solutions of 134CSC1 or 85SRC12(pH 6) from Amersham (UK) was used to contaminate the plants. The selected leaves were treated on the upper surface with 100#1 of carrier-free solution of 134CSC1 for one series of experiments and 85SRC12 for the other series. The solutions were applied with a micropipette as 20-25 small droplets which dried within 2-3 h.
Sampling In 1989 a first investigation with cesium and strontium was carried out. Three plants were available each for cesium and for strontium. They were harvested at three different dates. The first plant was removed when the grapes were semi-ripe (2 months),
the second plant when the grapes were fully ripe (2.5 months) and the third plant at the beginning of leaf drop (3.5 months). The results from this preliminary experiment were used to design the more detailed studies in the following seasons. In 1990 only strontium was applied. With 8 plants at our disposal, 2 were harvested per sampling date, one, two, three, and four months after contamination. In 1991 and 1992 similar investigations were carried out with cesium only as a contaminant, since in the preceding studies hardly any strontium was taken up by the plant leaves and even less was transported into other plant parts (see below). Two plants per sampling date were taken at fortnightly intervals, between 1 and 5 months after contamination. A further point of interest was to find out in which parts of the plants the activities resided during the dormant period in the winter. These experiments were carried out with surplus plants left over from the 1991 and 1992 investigations. The pruned plants were re-integrated into the experiment in the following year without further contamination. The plants were harvested 13.5 and 14.5 months after contamination as described above.
Preparation of samples For radioactivity measurements plants were harvested and separated into contaminated leaves, uncontaminated leaves, young twigs (leaves removed), branches and stems without bark, bark, grape berries, grape stalks and roots. The two contaminated leaves of each plant were removed first and washed with 50 ml of 0.1 N HC1 for five minutes with shaking. Then all harvested organs were cut into small pieces and weighed to obtain the fresh weights of the samples. After air-drying them under ventilation at 80°C the dry weights were measured. Samples were then put into standard 50 ml polyethylene bottles. Small samples (contaminated leaves, grape stalks) were placed in plastic dishes with a diameter of 5 cm. The roots were separated manually from the soil and treated similarly to the other plant parts. The soil was sieved, well mixed, dried and about one kilogram was put into a 1 litre plastic bottle.
Measurement of radioactivity Since only v-emitting samples had to be analysed, the concentrations of Cs-134 and Sr-85 could be determined by means of y-spectrometric methods. To obtain high photon energy resolution for separation of the Cs-134 and Sr-85 signals from other v-lines also registered by the detector (as for instance, photopeaks introduced by members of the natural uranium a n d thorium decay series in the soil sample material), all samples were measured in a P-type coaxial solid state intrinsic germanium detector linked to an automatically operating sample changer with a capability to analyse 10 samples consecutively. This detector has a relative efficiency of about 30% relative to a 3" x 3"
Foliar uptake of radioactivity by grapevines NaI(Tl) detector at the 1332keV photopeak of Cobalt-60 [Princeton Gamma-Tech (PGT), type IGC 30]. The most important parameters characterizing this Ge-detector are its high efficiency, energy resolution and peak to Compton ratio. A multichannel system was used to separate the photopeaks into 8000 individual channels. By setting the energy range from 0 to 2 MeV, 0.25 keV 'channel is obtained. The activity of the samples was calculated using the software package "inter-gamma" developed by the French company Intertechnique SA. By application of specific least square based algorithms, photopeaks are fitted and resolved from background and Compton scatter, and interferences of 7-1ines with similar energies are accounted for. Due to their highly variable activity, all samples were measured over different time periods in order to minimize the uncertainty resulting from counting statistics to variations not exceeding a few percent. Calibration of the detector with respect to photon energy and energy dependent efficiency was performed with mixed radionuclide standards. The uncertainty of the detector efficiency was found to be less than 3% for photoquants between 0.1 and 2 MeV. No correction was necessary for photon self absorption of 7-emitting Cs-134 and Sr-85 nuclides in the sample material, since the major ~-lines are above 0.5 MeV. For most geologica[ or biological materials with densities up to 4-5 g cm 3 the mass .attenuation coefficient (p/r) at a given energy remains almost independent of the sample material for energies above 0.2 MeV. The photon energies and emission probabilities for the radiotracers used were 604.7 keV (97.6%) and 795.8 keV (85.4%) for Cs-134; 513.9 (99.2%) for Sr-85. Because of the different ha/f-lives of the radioisotopes and the different times of analysis all measured activities were calculated back to the application date to provide a basis for comparison of the measured activities at different times. For safety reasons and improved counting efficiency the activities of the Cs-134 were steadily reduced. In 1992 less than a quarter of the activity used in 1989 was employed. We were also careful in our later experiments to reduce the number of different geometries of the samples for radioactivity measurements. In 1992 only two sample sizes were used, 50 ml for ail the plant materials and 1 litre bottles for the soil samples, both geometries were calibrated before. In 1992 we checked the geometry effect by comparing the results of the activity measurements as described above, with the results of activity measurements after chemical and physical digestion of the same plant material. We proceeded as follows: 5 g of the biological material of a sample was enclosed in a HPR-3000/1 rotor of a Microwave-laboratorysystem MLS-122 Mega (Milestone s.r.l., Sorisole/BG, Italy) together with 40 ml of nitric acid (65%) and 10ml of hydrogen peroxide (30%). Then a microRPC 46/I--E
63
wave treatment program was started: 250W for 10 min, 500 W for 6 min, 0 W for 2 min and 450 W for 6 min. After that, ventilation was performed for 5 rain. The rotor was then cooled to room temperature in a water bath and carefully opened in a fume cupboard. The clear solutions were transferred to 50 ml polyethylene bottles described above and activity measured. The procedure was repeated until all the material in a sample was digested and measured. The final results corresponded well with those from the direct measurements. Therefore it was not necessary to use this very time-consuming method for analyzing the large series of samples.
R E S U L T S AND D I S C U S S I O N
The activity of the radionuclides (cesium o r strontium) applied to the leaves is defined as the "initially applied activity". The sum of the radioactivity levels found in contaminated and uncontaminated plant parts and in the soil (means of 2 plants per sampling date in 1990, 1991 and 1992, only one plant in 1989) is the "tota] recovered activity", whereas the mean radioactivity detected in all untreated plant parts plus in the soil represents the "transported activity".
Strontium-85 experiments The 1989 experiments are not reported because of the small number of plants investigated. However the results did not differ essentially from those of the 1990 experiment. In 1990 the total recovered Sr-85 activity dropped from 95 to 72% with increasing experimental duration (Fig. 1). Most of the activity could be washed off the contaminated leaves (Fig. 2) and decreased from 97 to 88%. The part of activity retained in the washed leaves increased steadily from 3 to 11%, but 100
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Fig. 1. Total recovered Sr-85 activity in grapevine plants 1990. Mean values and standard deviation are shown.
64
H, J. Zehnder et al. 1
120
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the activity transported into other plant parts was less than 2.5%. F r o m these results it can be concluded that the strontium in the washed leaves was highly immobile in the plant. Strontium applied as chloride may be insolubilized as carbonate and sulfate. This finding is consistent with earlier reports concerning strawberries (Zehnder et al., 1993), grapevines (Hellmuth et al., 1989) and various other plants (Middleton, 1959; Koranda and Robison, 1978).
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Fig. 2. Distribution of the total recovered Sr-85 activity in grapevine plants 1990. Mean values and standard deviation are shown.
A continuous increase in recovery is noted in the cesium-134 experiments when comparing the activity balances for the years 1989, 1991 and 1992. In 1989 30% of the activity was lost. During the latter part of the 1991 experiment and during the entire 1992 experiment the recovered activity was close to 100% of the activity applied to the leaves. This improvement is probably due to better handling and measuring techniques (Fig. 3). As in the corresponding strontium experiments the 1989 results from the Cs-134 experiments are not reported, for the same reasons. As mentioned above, in the 1991/92 experiment, between 80 and 104% and in 1992 between 100 and 113% of the initially applied activity was recovered. The 1991 determinations (Fig. 4) show that radiocesium was taken up by the leaves only at the very beginning, immediately after application when the cesium was still in solution. When the droplets had dried completely no more cesium was
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Fig. 3. Cs-134 recovery 1991-1993 in grapevine plants. Mean values and standard deviation are shown.
Foliar uptake of radioactivity by grapevines [
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Fig. 4. Distribution of the total recovered Cs-134 activity in grapevine plants 1991. Mean values and standard deviation are shown,
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Fig. 5. Distribution of the total recovered Cs-134 activity in grapevine plants 1992, Mean values and standard deviation are shown.
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taken up during the whole experiment. Between 60 and 66% of the total recovered activity could be washed off the leaves in all samples with the exception of the plants which were harvested after 2 months.
Between 25 and 32% of the activity taken up by the leaves was transported to other plant parts. In the plants taken after 2 months 41% of the total recovered activity was translocated to other plant parts.
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Fig. 7. Distribution of transported Cs-134 activity in grapevine plants 1991/92. Mean values and standard deviation are shown.
Foliar uptake of radioactivity by grapevines This observation was in agreement with the finding that 10%o less activity could be washed from these leaves. Between 10 and 6% of the total recovered activity was retained in the contaminated leaves. The results in 1992 showed a different pattern (Fig. 5). The amounts of activity washed from contaminated leaves decreased steadily during the whole experiment from 66 to 39% of the total recovered activity. In contrast the amount of activity transported from these leaves to other plant parts increased steadily from 24 to 51%. The activities remaining in the contaminated leaves varied between 14 and 9%. This different pattern in the uptake of radiocesium by the contaminated leaves may have been caused by a lower temperature and a higher relative humidity in summer 1992. Figure 6 shows the monthly average of the air temperature and of the relative humidity in 1991 and 1992 from June to November. The temperatures in the greenhouse during summertime were high, especially when the sun was shining. Therefore, water consumption of the grapevines was high and although the plant pots were covered with plastic, the water supply of the plants was limited. It appears likely that humidity on the leaf surface and the behaviour of the stomata in 1991 was considerably different from 1992. From the literature, it is known that dry deposits have to be dissolved first by moisture (rain, mist, fog, condensation water, guttation liquid) or by making contact with water-filled pores prior to entering the leaf (Franke, 1984). The distribution of the transported radiocesium in the plants and in the soil (Figs 7 and 8) suggests that a large percentage was released from the plants to the soil (22-49%). From the distribution patterns we 100
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67
conclude that the grapes and the soil act as sinks for radiocesium. This radionuclide may be retranslocated from the fruits (e.g. to the stem, the roots or the soil). In the soil it may interact with particles and will no longer be available to the plants. From the literature it becomes evident that only a very minor fraction of the radiocesium is available for plants on soils with a high clay content (Andersen, 1967; Rocca et aL, 1989; Antonopoulos,Domis et al., 1991; Wagner and Diehl, 1991; Beckmann and Faas, 1992). In culture substrates with a high content of organic matter and a low pH, as it is found naturally in the northern regions o f the northern hemisphere or as are often used in horticulture, a considerably higher proportion may be taken up by the roots (Koranda and Robison, 1978). In our experiments, it remained open to what extent the Cs-134 activity found in the soil was released from living roots or lost by rotten or severed root parts. Generally the plants in 1991 were smaller than those i n 1992 because they were younger. Therefore the specific activities (activity/mass) in the 1992 plants were lower than in 1991. The accumulation of radioactivity in the grape berries was of special interest. Independent of the smaller plant size, the grape yield was about the same in both years. Initially, t h e specific activities in the berries increased rapidly in both years, decreased to low values and increased again towards the end of the experiments. This behaviour was more pronounced in 1991 than in 1992. These results indicate that relatively large amounts of radiocesium were first transported into the small fruits. During further development the radiocesium concentration was diluted by the growI
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Fig. 8. Distribution of transported Cs-134 activity in grapevine plants 1992/93. Mean values and standard deviation are shown.
H. J. Zehnder et a l .
68
ing biomass. Later the berries were losing water by aging and in this way the specific cesium activities increased again. As previously mentioned, grapes are only transient sinks f o r radiocesium. Apparently some cesium was released by the fruit back to the plant and partially also to the soil. In both years berries and stalks showed the highest specific activities of all plant organs. The highest activity in fruit was detected 2 months after contamination in 1991 and 3 months after contamination in 1992, when the grape berries contained 7 and 9% of the transported radiocesium, respectively. The fate of the radiocesium during winter and the subsequent vegetation period was subject to further investigation. From 4 plants ineach 1991 and 1992, the treated and non-treated leaves and the grapes were collected in the autumn. In the spring of the following year the plants were pruned. All plant parts removed and the sap issuing from the cut surfaces were collected and the activity, as well as that in the material harvested in the previous year, was measured. The pruned plants were reintegrated in the experiment without being contaminated again. The harvest of the wintered plants took place in August and September (13.5 and 14.5 months after contamination) as described above. The total activity lost by removing the dead leaves, the grapes, the pruning material and the sap was around 83% in 1991 and 68% in 1992. Thus all the activities measured in the winter plants and in their soil represent transported activities. As much as 72-83 % of the detected activity was found in the soil. Only 5-9% of the initially applied cesium activity could be detected in the plant and not more than 1.5% was accumulated in the grape berries. Considering the recoveries and the half-life of cesium- 134 (2.1 years) it can be concluded that only 10-20% of the originally applied activity was relevant during the second year. For the cesium isotope Cs-137, with a half-life of 30 years, a higher activity has to be expected in the second year. The radiocesium content of the soil increased during the second year of the experiments. This may be mainly caused by the fixation of cesium to soil particles, especially to certain clay fractions. Although plants and soils were exposed to rain and snow during winter time, activity was not leached during the dormant period. CONCLUSIONS In grapevines only a very minor part of the strontium deposited on the leaves was taken up and very little of this was translocated in the plants. These results are consistent with previous findings concerning strawberries (Zehnder et al., 1993). Therefore the foliar uptake of strontium constitutes no major risk to the consumer of fruit or other edible plant parts, provided that no direct contamination of these food items has taken place and that this radionuclide is not transported via the xylem. For cesium the situation is
very different. The behaviour of cesium is similar to that of potassium. It is readily taken up by leaves an d transported to other plant parts (e.g. to the grape berries) a n d may also be released into the soil. Fruits act as transient sinks. Apparently fruits release cesium activity back to the plant again and from there to the soil. No major percentage of the radiocesium excreted by the plant or released by rotting root parts was taken up by the roots and transported back into the plant. This study indicates that radiocesium, once bound to soil which contains clay minerals, is not easily available to plants. However it must be borne in mind that the retention of released cesium in the soil strongly depends on soil properties and cannot be generalized. Salts can only be taken up by leaves in a dissolved form. The 1991 experiment demonstrates that under dry conditions far less radiocesium is taken up by the leaves. Cesium nuclides may enter the food chain via the fruits. Approximately 25 % of the detected activity, or around 8% of the initially applied activity, was transported to the grape berries. Berries and stalks showed the highest specific activity of all examined plant parts. Far less radiocesium (not more than 1.5% of the initially applied activity) reached the fruits during the second season after foliar contamination.
REFERENCES
Andersen A. J. (1967) Investigations on the plant uptake of fission products from contaminated soils: 1. Influence of plant species and soil types on the uptake of radioactive strontium and cesium. Ris6 Rep. No. 170, Agric. Res. Dept., Danish Atomic Energy Comm. Res. Establ. Ris6, Denmark. Antonopoulos-Domis M., Clouvas A. and Gagianas A. (1991) Radiocesium dynamics in fruit trees following the Chernobyl accident. Health Phys. 61, 837. Beckmann C. and Faas C. (1992) Radioactive contamination of soils in lower Saxony, Germany, after the Chernobyl accident. Analyst 117, 525. Franke W. (1984) The basis of foliar absorption of fertilizers with special regard to the mechanism. In Foliar Fertilization (Edited by Alexander A.), p. 17. Martinus Nijhoff, Dordrech. Hellmuth K.-H., Wagner A. and Fischer E. (1989) Zur Radiorkologie der Rebe: Teil 1. Transfer von Kernwaffenfallout vom Boden in den Wein. Z. Lebensm. Unters. Forsch. 188, 317. Koranda J. J. and Robison W. L. (1978) Accumulation of radionuclides by plants as a monitor system, Environ. Health Perspective 27, 165. Middteton L. J. (1959) Radioactive strontium and caesium in the edible parts of crop plants after foliar contamination~ Int. J. Radiat. Biol. 4, 387. Rich C. I. (1968) Mineralogy of soil potassium. In The Role o f Potassium in Agriculture (Edited by Kilmer V. J., Younts S. E. and Brady N. C.), p. 79. American Society of Agronomy, Madison. Rocca V., Napolitano M., Speranza P. R. and Gialanella G. (1989) Analysis of radioactivity levels in soils and crops
Foliar uptake of radioactivity by grapevines from the Campania region (South Italy) after the Chernobyl accident. J. Environ. Radioactivity 9, 117. Wagner A. and Diehl J. F. (1991) Zur Radio6kologie der Weinrebe: Teil 2. Auswirkungen des Reaktorunfalls yon Tschernobyl auf Radioaktivit/it in Boden, B1/ittern, Trauben, Wein. Z. Lebensm. Unters. Forsch. 192, 339.
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Zehnder H. J. (1988) Radioaktivit/it in Frfichten, Nfissen und verarbeiteten Produkten 1986/87. Schweiz. Zeitschr. Obst- u. Weinbau 124, 101. Zehnder H. J., Kopp P., Oertli J. J. and Feller U. (1993) Uptake and transport of radioactive cesium and strontium into strawberries after leaf contamination. Gartenbauwissenschaft 58, 209.
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Radiat. Phys. Chem. Vol. 46, No. 1, pp. 61-69, 1995 Copyright © 1995 ElsevierScienceLtd Printed in Great Britain. All rights reserved 0969-806X/95 $9.50+ 0.00
U P T A K E A N D T R A N S P O R T OF R A D I O A C T I V E C E S I U M A N D S T R O N T I U M INTO G R A P E V I N E S A F T E R L E A F CONTAMINATION H. J. Z E H N D E R , 1 P. KOPP, 2 J. E I K E N B E R G , 2 U. F E L L E R 3 and J. J. OERTLI4¢ ~Swiss Federal Research Station for Fruit-Growing, Viticulture and Horticulture. CH-8820 W~denswil. 2Paul Scherrer Institute, CH-5232 Villigen-PSI. 3Institute of Plant Physiology, University of Bern. CH-3013 Bern and 41nstitute for Plant Science, Swiss Federal Institute of Technology, CH-8315 Lindau. Switzerland (Received 10 July 1994; accepted 31 August 1994)
Abstract--From1989 to 1993 the foliar uptake of radioactive strontium (Sr-85) and cesium (Cs-134) by
selected leaves of grapevine plants and the subsequent redistribution within the plants was examined under controlled conditions in a greenhouse. The radionuclides were applied as chlorides. These plants were grown in large pots containing a mixture of local soil and peat. Plant and soil samples were analyzed throughout the growing season and also during the following vegetation period. Only traces of the applied radiostrontium were taken up by the leaves. This element was essentially not redistributed within the plants. In contrast, radiocesium was easily taken up through the leaf surface, transported to other plant parts and to some extent released from the roots into the soil. Cesium reaching the soil may interact with clay particles causing a very reduced availability for plants. Therefore the soil may act as a long-term sink for radiocesinm. On the other hand, grape berries represent transient sinks. The cesium levels in the berries decreased again in a late phase of maturation, but the mechanisms causing this loss are not yet identified. During the second vegetation period, only a very minor proportion of the radiocesium taken up previously by the plants was present in the above ground parts.
solution, its uptake into plant roots and its transport to fruits, berries and nuts is rather low. These considerations motivated us to study the foliar uptake of radiocesium and radiostrontium, which is another interesting nuclide in this context. Both radioelements were present in the "Chernobyl fall-out'. Middleton (1959) reported that radiocesium was easily translocated from contaminated leaves to edible parts of crop plants, while radiostrontium was redistributed only to a very small extent. Strawberry plants were used in a first study (Zehnder et aL, 1993). However, strawberries are small plants and the risk of contaminating leaves and fruits in experiments with radioactive substances by contact is relatively high. Furthermore in most cultivated varieties of strawberries the fruit formation period is short. F o r further studies, we were therefore interested in using larger model plants, clearly separable into stem, leaves and fruits and having a long fruit formation period. Grapevine plants represent a suitable experimental system in this context. In a series o f studies carried out between 1989 and 1992 the foliar uptake of Cs-134 and Sr-85 into grapevine plants, their transport to other plant organs and finally also the release from the plants into the soil was investigated by repeated sampling and analysis of the plants and the soil. The accumulation of radioactivity in the berries was of special interest since this represents a pathway for these undesirable isotopes into the human food chain.
INTRODUCTION On 26 April 1986, one of the four reactors in the nuclear power station near the small Ukrainian town of Chernobyl exploded and started to burn In the following days and weeks winds drove air layers containing radioactive elements from the collapsed reactor over a large part of Europe. With the rain these substances were washed out and deposited on plants and on the soil surface. In the summer and autumn of 1986, the level of radioactivity in fruit, berries, nuts and some processed fruit products was slightly elevated in Switzerland (Zehnder, 1988). This increase in the radioactivity was mainly due to radioactive isotopes of cesium, Cs-137 and Cs-134. The joint occurrence of these two radionuclides in the appropriate ratio is typical for the nuclear accident mentioned above. F r o m the literature it is known that the interactions of cesium with soil particles are similar to those of potassium (Rich, 1968). Its availability for crop plants depends on soil properties, e.g. soil texture, clay mineralogy, contents of other cations, pH. Andersen (1967) stated that this element becomes less available for plants with increasing clay content. In Switzerland, most soils contain considerable amounts of clay. Therefore the availability of cesium in the soil tPresent address: Professor Dr J. J. Oertli, Schaienweg 25, CH-4107 Ettingen, Switzerland. 61
H.J. Zehnder et al.
62 MATERIALS AND METHODS
Plants and cultivation Grapevine plants, variety "Riesling x Sylvaner" (Mfiller-Thurgau), 2-3 years old were obtained from a nursery. They were planted in black 18.5 litre plastic pots in a 1 : 2 mixture of peat substrate and local soil (10-17kg total dry weight). To prevent contamination of the soil with radioactivity from the plant parts above ground, the top surface of the pots was covered with black plastic. Irrigation took place twice weekly from an underpot with periodic liquid fertilization using 0.25% Vegesan ~ (Hauert, Grossaffoltern, Switzerland). In spring the plants were pruned on two canes with five buds each. At a later date all emerged shoots of a cane were removed with the exception of one. On each of the remaining two shoots the first fully developed leaf reaching a size of between 50 and 80 cm 2 was contaminated with solutions of 134CSC1 or 85SRC12(see below). All leaves below those to be contaminated were previously removed. During the experiment plants were cultivated using normal procedures, and no further shoots and leaves were taken away. Pesticides were used only when necessary and only before starting the experiments. These experiments were carried out in the same greenhouse as that used in the strawberry study (Zehnder et al., 1993). The greenhouse floor was covered with plastic sheeting. The two short sides (front and back) of the greenhouse were made of fine plastic netting, the two long sides of polyester sheets. The plexiglass roof was fitted with a rainproof ventilation hole. These precautionary measures provided safety against loss of radioactivity and allowed air circulation.
Application of the radionuclides As in our previous experiments (Zehnder et al., 1993) we used the short-lived isotopes cesium-134 (half-life 2 years) and strontium-85 (half-life 65 days) instead of the long-lived isotopes (Cs-137, Sr-90) for safety reasons. Moreover, strontium-85 is a gamma emitter which can be measured more easily than strontium-90, which emits beta particles only. A suitable activity of carrier-free, aqueous solutions of 134CSC1 or 85SRC12(pH 6) from Amersham (UK) was used to contaminate the plants. The selected leaves were treated on the upper surface with 100#1 of carrier-free solution of 134CSC1 for one series of experiments and 85SRC12 for the other series. The solutions were applied with a micropipette as 20-25 small droplets which dried within 2-3 h.
Sampling In 1989 a first investigation with cesium and strontium was carried out. Three plants were available each for cesium and for strontium. They were harvested at three different dates. The first plant was removed when the grapes were semi-ripe (2 months),
the second plant when the grapes were fully ripe (2.5 months) and the third plant at the beginning of leaf drop (3.5 months). The results from this preliminary experiment were used to design the more detailed studies in the following seasons. In 1990 only strontium was applied. With 8 plants at our disposal, 2 were harvested per sampling date, one, two, three, and four months after contamination. In 1991 and 1992 similar investigations were carried out with cesium only as a contaminant, since in the preceding studies hardly any strontium was taken up by the plant leaves and even less was transported into other plant parts (see below). Two plants per sampling date were taken at fortnightly intervals, between 1 and 5 months after contamination. A further point of interest was to find out in which parts of the plants the activities resided during the dormant period in the winter. These experiments were carried out with surplus plants left over from the 1991 and 1992 investigations. The pruned plants were re-integrated into the experiment in the following year without further contamination. The plants were harvested 13.5 and 14.5 months after contamination as described above.
Preparation of samples For radioactivity measurements plants were harvested and separated into contaminated leaves, uncontaminated leaves, young twigs (leaves removed), branches and stems without bark, bark, grape berries, grape stalks and roots. The two contaminated leaves of each plant were removed first and washed with 50 ml of 0.1 N HC1 for five minutes with shaking. Then all harvested organs were cut into small pieces and weighed to obtain the fresh weights of the samples. After air-drying them under ventilation at 80°C the dry weights were measured. Samples were then put into standard 50 ml polyethylene bottles. Small samples (contaminated leaves, grape stalks) were placed in plastic dishes with a diameter of 5 cm. The roots were separated manually from the soil and treated similarly to the other plant parts. The soil was sieved, well mixed, dried and about one kilogram was put into a 1 litre plastic bottle.
Measurement of radioactivity Since only v-emitting samples had to be analysed, the concentrations of Cs-134 and Sr-85 could be determined by means of y-spectrometric methods. To obtain high photon energy resolution for separation of the Cs-134 and Sr-85 signals from other v-lines also registered by the detector (as for instance, photopeaks introduced by members of the natural uranium a n d thorium decay series in the soil sample material), all samples were measured in a P-type coaxial solid state intrinsic germanium detector linked to an automatically operating sample changer with a capability to analyse 10 samples consecutively. This detector has a relative efficiency of about 30% relative to a 3" x 3"
Foliar uptake of radioactivity by grapevines NaI(Tl) detector at the 1332keV photopeak of Cobalt-60 [Princeton Gamma-Tech (PGT), type IGC 30]. The most important parameters characterizing this Ge-detector are its high efficiency, energy resolution and peak to Compton ratio. A multichannel system was used to separate the photopeaks into 8000 individual channels. By setting the energy range from 0 to 2 MeV, 0.25 keV 'channel is obtained. The activity of the samples was calculated using the software package "inter-gamma" developed by the French company Intertechnique SA. By application of specific least square based algorithms, photopeaks are fitted and resolved from background and Compton scatter, and interferences of 7-1ines with similar energies are accounted for. Due to their highly variable activity, all samples were measured over different time periods in order to minimize the uncertainty resulting from counting statistics to variations not exceeding a few percent. Calibration of the detector with respect to photon energy and energy dependent efficiency was performed with mixed radionuclide standards. The uncertainty of the detector efficiency was found to be less than 3% for photoquants between 0.1 and 2 MeV. No correction was necessary for photon self absorption of 7-emitting Cs-134 and Sr-85 nuclides in the sample material, since the major ~-lines are above 0.5 MeV. For most geologica[ or biological materials with densities up to 4-5 g cm 3 the mass .attenuation coefficient (p/r) at a given energy remains almost independent of the sample material for energies above 0.2 MeV. The photon energies and emission probabilities for the radiotracers used were 604.7 keV (97.6%) and 795.8 keV (85.4%) for Cs-134; 513.9 (99.2%) for Sr-85. Because of the different ha/f-lives of the radioisotopes and the different times of analysis all measured activities were calculated back to the application date to provide a basis for comparison of the measured activities at different times. For safety reasons and improved counting efficiency the activities of the Cs-134 were steadily reduced. In 1992 less than a quarter of the activity used in 1989 was employed. We were also careful in our later experiments to reduce the number of different geometries of the samples for radioactivity measurements. In 1992 only two sample sizes were used, 50 ml for ail the plant materials and 1 litre bottles for the soil samples, both geometries were calibrated before. In 1992 we checked the geometry effect by comparing the results of the activity measurements as described above, with the results of activity measurements after chemical and physical digestion of the same plant material. We proceeded as follows: 5 g of the biological material of a sample was enclosed in a HPR-3000/1 rotor of a Microwave-laboratorysystem MLS-122 Mega (Milestone s.r.l., Sorisole/BG, Italy) together with 40 ml of nitric acid (65%) and 10ml of hydrogen peroxide (30%). Then a microRPC 46/I--E
63
wave treatment program was started: 250W for 10 min, 500 W for 6 min, 0 W for 2 min and 450 W for 6 min. After that, ventilation was performed for 5 rain. The rotor was then cooled to room temperature in a water bath and carefully opened in a fume cupboard. The clear solutions were transferred to 50 ml polyethylene bottles described above and activity measured. The procedure was repeated until all the material in a sample was digested and measured. The final results corresponded well with those from the direct measurements. Therefore it was not necessary to use this very time-consuming method for analyzing the large series of samples.
R E S U L T S AND D I S C U S S I O N
The activity of the radionuclides (cesium o r strontium) applied to the leaves is defined as the "initially applied activity". The sum of the radioactivity levels found in contaminated and uncontaminated plant parts and in the soil (means of 2 plants per sampling date in 1990, 1991 and 1992, only one plant in 1989) is the "tota] recovered activity", whereas the mean radioactivity detected in all untreated plant parts plus in the soil represents the "transported activity".
Strontium-85 experiments The 1989 experiments are not reported because of the small number of plants investigated. However the results did not differ essentially from those of the 1990 experiment. In 1990 the total recovered Sr-85 activity dropped from 95 to 72% with increasing experimental duration (Fig. 1). Most of the activity could be washed off the contaminated leaves (Fig. 2) and decreased from 97 to 88%. The part of activity retained in the washed leaves increased steadily from 3 to 11%, but 100
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Fig. 1. Total recovered Sr-85 activity in grapevine plants 1990. Mean values and standard deviation are shown.
64
H, J. Zehnder et al. 1
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the activity transported into other plant parts was less than 2.5%. F r o m these results it can be concluded that the strontium in the washed leaves was highly immobile in the plant. Strontium applied as chloride may be insolubilized as carbonate and sulfate. This finding is consistent with earlier reports concerning strawberries (Zehnder et al., 1993), grapevines (Hellmuth et al., 1989) and various other plants (Middleton, 1959; Koranda and Robison, 1978).
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A continuous increase in recovery is noted in the cesium-134 experiments when comparing the activity balances for the years 1989, 1991 and 1992. In 1989 30% of the activity was lost. During the latter part of the 1991 experiment and during the entire 1992 experiment the recovered activity was close to 100% of the activity applied to the leaves. This improvement is probably due to better handling and measuring techniques (Fig. 3). As in the corresponding strontium experiments the 1989 results from the Cs-134 experiments are not reported, for the same reasons. As mentioned above, in the 1991/92 experiment, between 80 and 104% and in 1992 between 100 and 113% of the initially applied activity was recovered. The 1991 determinations (Fig. 4) show that radiocesium was taken up by the leaves only at the very beginning, immediately after application when the cesium was still in solution. When the droplets had dried completely no more cesium was
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taken up during the whole experiment. Between 60 and 66% of the total recovered activity could be washed off the leaves in all samples with the exception of the plants which were harvested after 2 months.
Between 25 and 32% of the activity taken up by the leaves was transported to other plant parts. In the plants taken after 2 months 41% of the total recovered activity was translocated to other plant parts.
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Fig. 7. Distribution of transported Cs-134 activity in grapevine plants 1991/92. Mean values and standard deviation are shown.
Foliar uptake of radioactivity by grapevines This observation was in agreement with the finding that 10%o less activity could be washed from these leaves. Between 10 and 6% of the total recovered activity was retained in the contaminated leaves. The results in 1992 showed a different pattern (Fig. 5). The amounts of activity washed from contaminated leaves decreased steadily during the whole experiment from 66 to 39% of the total recovered activity. In contrast the amount of activity transported from these leaves to other plant parts increased steadily from 24 to 51%. The activities remaining in the contaminated leaves varied between 14 and 9%. This different pattern in the uptake of radiocesium by the contaminated leaves may have been caused by a lower temperature and a higher relative humidity in summer 1992. Figure 6 shows the monthly average of the air temperature and of the relative humidity in 1991 and 1992 from June to November. The temperatures in the greenhouse during summertime were high, especially when the sun was shining. Therefore, water consumption of the grapevines was high and although the plant pots were covered with plastic, the water supply of the plants was limited. It appears likely that humidity on the leaf surface and the behaviour of the stomata in 1991 was considerably different from 1992. From the literature, it is known that dry deposits have to be dissolved first by moisture (rain, mist, fog, condensation water, guttation liquid) or by making contact with water-filled pores prior to entering the leaf (Franke, 1984). The distribution of the transported radiocesium in the plants and in the soil (Figs 7 and 8) suggests that a large percentage was released from the plants to the soil (22-49%). From the distribution patterns we 100
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67
conclude that the grapes and the soil act as sinks for radiocesium. This radionuclide may be retranslocated from the fruits (e.g. to the stem, the roots or the soil). In the soil it may interact with particles and will no longer be available to the plants. From the literature it becomes evident that only a very minor fraction of the radiocesium is available for plants on soils with a high clay content (Andersen, 1967; Rocca et aL, 1989; Antonopoulos,Domis et al., 1991; Wagner and Diehl, 1991; Beckmann and Faas, 1992). In culture substrates with a high content of organic matter and a low pH, as it is found naturally in the northern regions o f the northern hemisphere or as are often used in horticulture, a considerably higher proportion may be taken up by the roots (Koranda and Robison, 1978). In our experiments, it remained open to what extent the Cs-134 activity found in the soil was released from living roots or lost by rotten or severed root parts. Generally the plants in 1991 were smaller than those i n 1992 because they were younger. Therefore the specific activities (activity/mass) in the 1992 plants were lower than in 1991. The accumulation of radioactivity in the grape berries was of special interest. Independent of the smaller plant size, the grape yield was about the same in both years. Initially, t h e specific activities in the berries increased rapidly in both years, decreased to low values and increased again towards the end of the experiments. This behaviour was more pronounced in 1991 than in 1992. These results indicate that relatively large amounts of radiocesium were first transported into the small fruits. During further development the radiocesium concentration was diluted by the growI
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Fig. 8. Distribution of transported Cs-134 activity in grapevine plants 1992/93. Mean values and standard deviation are shown.
H. J. Zehnder et a l .
68
ing biomass. Later the berries were losing water by aging and in this way the specific cesium activities increased again. As previously mentioned, grapes are only transient sinks f o r radiocesium. Apparently some cesium was released by the fruit back to the plant and partially also to the soil. In both years berries and stalks showed the highest specific activities of all plant organs. The highest activity in fruit was detected 2 months after contamination in 1991 and 3 months after contamination in 1992, when the grape berries contained 7 and 9% of the transported radiocesium, respectively. The fate of the radiocesium during winter and the subsequent vegetation period was subject to further investigation. From 4 plants ineach 1991 and 1992, the treated and non-treated leaves and the grapes were collected in the autumn. In the spring of the following year the plants were pruned. All plant parts removed and the sap issuing from the cut surfaces were collected and the activity, as well as that in the material harvested in the previous year, was measured. The pruned plants were reintegrated in the experiment without being contaminated again. The harvest of the wintered plants took place in August and September (13.5 and 14.5 months after contamination) as described above. The total activity lost by removing the dead leaves, the grapes, the pruning material and the sap was around 83% in 1991 and 68% in 1992. Thus all the activities measured in the winter plants and in their soil represent transported activities. As much as 72-83 % of the detected activity was found in the soil. Only 5-9% of the initially applied cesium activity could be detected in the plant and not more than 1.5% was accumulated in the grape berries. Considering the recoveries and the half-life of cesium- 134 (2.1 years) it can be concluded that only 10-20% of the originally applied activity was relevant during the second year. For the cesium isotope Cs-137, with a half-life of 30 years, a higher activity has to be expected in the second year. The radiocesium content of the soil increased during the second year of the experiments. This may be mainly caused by the fixation of cesium to soil particles, especially to certain clay fractions. Although plants and soils were exposed to rain and snow during winter time, activity was not leached during the dormant period. CONCLUSIONS In grapevines only a very minor part of the strontium deposited on the leaves was taken up and very little of this was translocated in the plants. These results are consistent with previous findings concerning strawberries (Zehnder et al., 1993). Therefore the foliar uptake of strontium constitutes no major risk to the consumer of fruit or other edible plant parts, provided that no direct contamination of these food items has taken place and that this radionuclide is not transported via the xylem. For cesium the situation is
very different. The behaviour of cesium is similar to that of potassium. It is readily taken up by leaves an d transported to other plant parts (e.g. to the grape berries) a n d may also be released into the soil. Fruits act as transient sinks. Apparently fruits release cesium activity back to the plant again and from there to the soil. No major percentage of the radiocesium excreted by the plant or released by rotting root parts was taken up by the roots and transported back into the plant. This study indicates that radiocesium, once bound to soil which contains clay minerals, is not easily available to plants. However it must be borne in mind that the retention of released cesium in the soil strongly depends on soil properties and cannot be generalized. Salts can only be taken up by leaves in a dissolved form. The 1991 experiment demonstrates that under dry conditions far less radiocesium is taken up by the leaves. Cesium nuclides may enter the food chain via the fruits. Approximately 25 % of the detected activity, or around 8% of the initially applied activity, was transported to the grape berries. Berries and stalks showed the highest specific activity of all examined plant parts. Far less radiocesium (not more than 1.5% of the initially applied activity) reached the fruits during the second season after foliar contamination.
REFERENCES
Andersen A. J. (1967) Investigations on the plant uptake of fission products from contaminated soils: 1. Influence of plant species and soil types on the uptake of radioactive strontium and cesium. Ris6 Rep. No. 170, Agric. Res. Dept., Danish Atomic Energy Comm. Res. Establ. Ris6, Denmark. Antonopoulos-Domis M., Clouvas A. and Gagianas A. (1991) Radiocesium dynamics in fruit trees following the Chernobyl accident. Health Phys. 61, 837. Beckmann C. and Faas C. (1992) Radioactive contamination of soils in lower Saxony, Germany, after the Chernobyl accident. Analyst 117, 525. Franke W. (1984) The basis of foliar absorption of fertilizers with special regard to the mechanism. In Foliar Fertilization (Edited by Alexander A.), p. 17. Martinus Nijhoff, Dordrech. Hellmuth K.-H., Wagner A. and Fischer E. (1989) Zur Radiorkologie der Rebe: Teil 1. Transfer von Kernwaffenfallout vom Boden in den Wein. Z. Lebensm. Unters. Forsch. 188, 317. Koranda J. J. and Robison W. L. (1978) Accumulation of radionuclides by plants as a monitor system, Environ. Health Perspective 27, 165. Middteton L. J. (1959) Radioactive strontium and caesium in the edible parts of crop plants after foliar contamination~ Int. J. Radiat. Biol. 4, 387. Rich C. I. (1968) Mineralogy of soil potassium. In The Role o f Potassium in Agriculture (Edited by Kilmer V. J., Younts S. E. and Brady N. C.), p. 79. American Society of Agronomy, Madison. Rocca V., Napolitano M., Speranza P. R. and Gialanella G. (1989) Analysis of radioactivity levels in soils and crops
Foliar uptake of radioactivity by grapevines from the Campania region (South Italy) after the Chernobyl accident. J. Environ. Radioactivity 9, 117. Wagner A. and Diehl J. F. (1991) Zur Radio6kologie der Weinrebe: Teil 2. Auswirkungen des Reaktorunfalls yon Tschernobyl auf Radioaktivit/it in Boden, B1/ittern, Trauben, Wein. Z. Lebensm. Unters. Forsch. 192, 339.
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Zehnder H. J. (1988) Radioaktivit/it in Frfichten, Nfissen und verarbeiteten Produkten 1986/87. Schweiz. Zeitschr. Obst- u. Weinbau 124, 101. Zehnder H. J., Kopp P., Oertli J. J. and Feller U. (1993) Uptake and transport of radioactive cesium and strontium into strawberries after leaf contamination. Gartenbauwissenschaft 58, 209.