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Published in J. Environ. Qual. 32:2254-2264 (2003).
© ASA, CSSA, SSSA
677 S. Segoe Rd., Madison, WI 53711 USA

TECHNICAL REPORTS

Plant and Environment Interactions

Cesium-134 and Strontium-85 in Strawberry Plants following Wet Aerial Deposition

F. Carini*,a, M. Brambillaa, N. Mitchellb and Z. Ould-Dadac

a Università Cattolica del Sacro Cuore, Institute of Agricultural and Environmental Chemistry, Faculty of Agricultural Sciences, Via Emilia Parmense 84, I-29100 Piacenza, Italy
b Mouchel Consulting Ltd., West Hall, Parvis Road, West Byfleet, Surrey KT14 6EZ, United Kingdom
c Food Standards Agency, Radiological Protection and Research Management Division, Aviation House, 125 Kingsway, Room 715B, London WC2B 6NH, United Kingdom

* Corresponding author (franca.carini{at}unicatt.it).

Received for publication December 31, 2002.

    ABSTRACT
 TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
The understanding of the processes that control the behavior of radionuclides in crops can support policymakers to take actions to protect the environment and safeguard human health. Data concerning the behavior of radionuclides in fruits are limited. Strawberry (Fragaria x ananassa Duchesne) plants were contaminated on the aboveground part by sprinkling an aqueous solution of 134Cs and 85Sr at three growing stages: predormancy, anthesis, and beginning of ripening. Intercepted activity was more affected by the posture and physical orientation of leaves rather than by leaf area or biomass. Fruit interception ranges from 0.2 to 1.2% of the sprinkled activity. Translocation coefficients from leaf to fruit are on the order of 10-4 for 134Cs and 10-5 for 85Sr. Translocation reaches its highest intensity between anthesis and ripening. If deposition occurs when plants are bearing fruits, the fruit activity will be affected by the activity initially deposited on the fruit surfaces. This is important for 85Sr as it is not translocated in the phloem. The loss of the dead leaves at the resumption of growth causes high plant decontamination, but a fraction of both radionuclides remains in the storage organs, roots, and shoots, which is retranslocated to fruits in the following spring. The values of the environmental half-time, tw, after deposition at predormancy are 114 d for 134Cs and 109 d for 85Sr. Cesium-134 tends to be allocated to fruits, while 85Sr remains in leaves and crowns. Translocation of radionuclides to roots results in soil contamination.

Abbreviations: RF, residual fraction • TC, translocation coefficient


    INTRODUCTION
 TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
STRAWBERRY is an herbaceous fruit-bearing plant, widely grown in temperate, subtropical, and tropical highland climates. Its production has increased dramatically during the past decades. As a consequence, strawberries have become a popular dessert fruit available fresh all year. Europe produces about 50% and North America 25% of the total world production. The USA, Poland, Spain, Japan, and Italy are the greatest strawberry-producing countries, together totaling 70% of the world production (Rosati, 1993). Strawberries have to be considered one of the leading crops, particularly in new countries, where the industry is expanding, since they rapidly raise the income of rural communities (Rosati, 1993).

In the case of an acute release of radionuclides to the atmosphere, the aboveground part of the plant can become a receptor of pollutants, posing a hazard to the environment and humans. The experience after the Chernobyl accident in 1986 demonstrated that the process of foliar uptake is the dominant one in the year of deposition, making soil uptake negligible in the estimate of the plant contamination. The understanding of the processes that affect the behavior of radionuclides in crops can both improve the assessment of the risk to man from ingestion of contaminated food and support policymakers to take actions to protect environmental quality and to safeguard human health.

Considerable interest has been raised in recent years on the behavior of radionuclides in fruit systems. A Fruits Working Group, established in the framework of the International Atomic Energy Agency BIOMASS (BIOsphere Modelling and ASSessment) project, discussed modeling and experimental studies to improve assessment of the transfer of radionuclides to fruit (International Atomic Energy Agency, 2003). Results from the group activities demonstrate that this field is still affected by large uncertainty due to the lack of knowledge and poor understanding of processes.

In the case of strawberry, the process of time-dependent foliar uptake of 134Cs and 85Sr and the kinetics of their distribution in the plant components have been investigated after deposition of small radioactive droplets onto their leaves (Zehnder et al., 1993, 1996; Kopp et al., 1990). No study has been performed on either direct contamination of fruit, or seasonality, a term proposed by Aarkrog as the dependence of plant contamination on the time of the year when the deposition occurs (Aarkrog, 1992).

This research was designed to evaluate the fate of 134Cs and 85Sr in strawberry crops in the short term following wet deposition to the aboveground part of the plant. Data were provided for the validation of SPADE models, used for radiological assessment by the UK Food Standards Agency. Cesium and strontium were chosen because of their persistence in the environment and their mobility in the biological systems. The processes of interception, loss, and leaf-to-fruit translocation of 134Cs and 85Sr in strawberry plants have been assessed.


    MATERIALS AND METHODS
 TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Choice of the Plant and Agricultural Practices
Strawberry, Fragaria x ananassa Duchesne (Otterbacher and Skirvin, 1978; cited by Branzanti, 1985), is a herbaceous, perennial member of the rose family (Rosaceae). The present research was undertaken with June bearer plants, which are the most representative of commercial production in Italy. These plants are transplanted at the end of July, develop flower buds in the autumn, lose all old leaves at the resumption of growth (in March), flower in the spring, and produce a single crop from early May to June. After harvest the plants are removed and replaced by new plants.

Strawberries can be grown outdoors or in ventilated polythene tunnels (protected culture) to speed up fruit ripening and to protect fruit from excess rain. Tunnel growing conditions are widely used, mainly in Europe and Japan. However, tunnels only exert a partial protective function against fallout deposition, as demonstrated by Baldini et al. (1986) after the Chernobyl accident.

One-hundred twenty cold-stored plants, cultivar MISS, were received from the farm Martorano 5 (Cesena, Italy). At end of July they were transplanted in 18- x 18-cm (volume = 3.6 L) pots filled with a horticultural substrate (fair peat) mixed with agriperlite at 15%. Peat substrate was chosen to reproduce the growing conditions of commercial plants. Pots were placed under a tunnel (2.5 x 12.0 x 2.0 m) covered with polythene from the top down, leaving a margin of 1 m from the ground. This minimized loss of radioactivity by rain while allowing natural ventilation. This brought near-natural conditions of temperature and humidity and favored pollination.

Plants were arranged in two double rows of 30 plants each, reproducing open field planting. Distances between plants on the row and inside the double rows were 35 cm. Distances between the two double rows were 110 cm. The plant density was 5.2 plants m-2. Irrigation was provided, as required, by an automatic drip system. Plants were also regularly fertilized and treated with pesticides for disease control.

Characteristics of Growth Medium
The main physicochemical characteristics of peat were determined: density, moisture (at 105°C), ash (at 550°C), pH in H2O and in CaCl2, cation exchange capacity (CEC), organic matter, exchangeable potassium and calcium (extraction with 0.5 M HCl and determination by inductively coupled plasma [ICP]) (Cunniff, 1995), organic carbon (Springer and Klee), total nitrogen (Kjeldahl) (Ministero delle Politiche Agricole e Forestali, 2000), total potassium, and total calcium (microwave digestion by concentrated HNO3 and determination by ICP spectrometry) (Papp and Fischer, 1987). Data are reported in Table 1.


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Table 1. Main physicochemical characteristics of the growth medium.

 
Experimental Design and Plant Contamination
The study was performed for three consecutive years. New plants were transplanted into fresh growing medium each year at the end of July. The experimental design considered the contamination of the aboveground part of different sets of plants at three stages of development: predormancy, anthesis, and beginning of ripening (Table 2). At the predormancy stage (beginning of November) plants had well-developed leaves, but no flowers, fruits, or runners. At the anthesis stage (April) plants had well-developed leaves, flowers, and few small green berries. At the stage of the beginning of ripening (May) plants were bearing a few flowers together with green and ripe berries (Fig. 1) . While contamination at anthesis and at ripening was performed each year, that at predormancy was conducted in only one year. The second-year treatments were performed earlier than in the other two years: at preanthesis (plants with few flowers) and before ripening (plants bearing mainly green berries and some flowers). The number of replicates for those plants to be harvested at maturity was nine.


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Table 2. Experimental design.

 


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Fig. 1. Vegetative cycle of June bearer strawberry. Modified from Branzanti (1985)(p. 32–33).

 
Two radionuclides were used, 134Cs and 85Sr, supplied by Amersham (Buckinghamshire, UK). They were in the form of chloride salts in aqueous solution. Aliquots of 134Cs and 85Sr mother solutions were mixed and diluted with double-distilled water to obtain a final solution containing the desired concentration of the radionuclides. A delay in delivery of 85Sr made it impossible to contaminate plants with 85Sr in the third year at anthesis.

Each plant was introduced into a plexiglass box measuring 50 x 50 x 60 cm to prevent the contamination of the surrounding environment during sprinkling. A sprinkler was introduced into the box 20 cm over the foliar apparatus, and about 1 mL of the radioactive solution was sprinkled onto the plant. Before treatment, the soil was covered with a plastic sheet to avoid direct contamination. The plastic sheet was removed after treatment and the soil surface was covered with a layer of expanded clay to avoid contact between leaves and soil. The activities administered to the aboveground part of the plant for each year of the study, expressed as kBq plant-1, are reported in Table 3.


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Table 3. Activities administered to the aboveground part of the plant.

 
Harvests

The samples were weighed as collected, oven-dried at 60°C to constant weight, and reweighed. Yields, expressed as grams of fresh or wet weight per plant and percent dry matter content, are reported in Table 4 (fruits) and Table 5 (leaves, crowns, and roots). Each dried sample was ground and homogenized before analysis by {gamma} spectrometry. A different protocol was followed for fruits. These were weighed as collected and frozen plant by plant during the whole harvest. The samples were then defrosted, crushed, homogenized, and analyzed by {gamma} spectrometry. Finally, they were dried following the same procedure as for the other samples, to determine their dry matter content.


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Table 4. Average yields of fruits and corresponding dry matter content.

 

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Table 5. Average yields of leaves, crowns, roots, and dead leaves and corresponding dry matter content.

 
Gamma Analyses
The concentration of 134Cs and 85Sr was measured by direct {gamma} spectrometry of the samples. A HpGe detector was used, with an efficiency of 38% and a FWHM resolution of 1.76 keV at 1.33 MeV of the 60Co. The {gamma} spectrum analysis was performed using the program SAMPO 90 (Logion Oy, Helsinki, Finland). Each sample was analyzed for a time sufficient to collect at least 4000 net counts in the peaks of interest to reach a maximum error of 3 to 4% at 95% confidence.

Fruits were analyzed while fresh, whereas leaves, crowns, roots, and soil samples were analyzed after drying. Samples from each plant were analyzed separately. In the case of crowns, samples from three plants were pooled, to produce a minimum volume suitable for {gamma} analysis. Different counting geometries were employed, depending on the size of the analytical sample. All results were decay-corrected to the same reference time, arbitrarily chosen as the average date of fruit harvest. Various parameters have been calculated, whose expression is reported below.


    RESULTS
 TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Intercepted Activity and Leaf Area
Interception is the fraction of activity deposited on the aboveground part of the plant as opposed to total applied activity. The interception of the ith sample (Ii) is expressed by the ratio:

where i = 1, 2, ... n and n = number of replicates.

The activity intercepted by plants was obtained by sprinkling four plants, harvesting the whole aboveground part immediately after the spray had dried, and measuring the 134Cs and 85Sr activity on the whole fresh mass, called "leaves" for brevity. When plants were bearing fruits, these were analyzed separately. The means and standard errors of interception for four replicates are summarized in Table 6 for the three years of study and the three growing stages considered.


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Table 6. Cesium-134 and 85Sr fraction intercepted by the aboveground part of strawberry, expressed as percentage of the sprinkled radioactivity; leaf area; and leaf and fruit biomass.

 
The same four plants were also used to determine leaf area. After harvesting, each fresh leaf blade was cut from the stalk, laid out on a sheet, and photocopied onto a transparency. Detection of the area of the leaves was performed by passing photocopied transparencies through a Model LI 3000 surface integrator leaf area meter (LI-COR, Lincoln, NE). Mean and standard error of the leaf areas of the four replicates, expressed in cm2 plant-1, as well as foliar biomass, expressed as g of dry weight plant-1, are reported in Table 6.

Interception of 85Sr was found to be generally higher than that of 134Cs. This is mainly due to the adsorption of radionuclides onto the surfaces of glassware. Such adsorption, being higher for 134Cs than for 85Sr, reduces 134Cs concentration in the solution, apparently reducing 134Cs interception by the plant. Trials performed at our laboratory where the glassware was treated with silicone (dimethildichlorosilane) confirm such adsorption.

The interception of wet-deposited radionuclides is also dependent on the interactions between the negatively charged plant surfaces and the physicochemical properties of the element. Bivalent cations seem to be retained more strongly on the plant surface than do monovalent cations, as shown by Pröhl et al. (1995) for 140Ba and 137Cs. The higher interception of 85Sr as compared with 134Cs could be the result of such a process.

Interception depends on the growing stage of the plant at the time of deposition. It ranges from 17.4 ± 1.3 to 39.0 ± 2.5% of the sprayed 134Cs and from 30.3 ± 1.5 to 45.7 ± 3.1% of the sprayed 85Sr (Table 6). In various experimental situations the interception of wet deposited activity was found to be positively correlated with the leaf area and/or with the dry biomass of the crop: interception increases as leaf area per unit of soil or biomass increases (Pröhl and Hoffman, 1996). In this study comparisons between anthesis and beginning of ripening for the first and the third year show that there is no positive correlation between interception and leaf area or leaf dry biomass. Although leaf area and, in general, biomass increases from anthesis to ripening, interception decreases. Photographs taken from the top of plants during contamination show that, while at anthesis almost all the leaves were horizontally exposed to intercept the maximum amount of light, at ripening the more external and aged leaves were bent down, with a reduced intercepting efficiency. It seems therefore that interception at the stages considered in the present study is more affected by variables such as the posture and physical orientation of leaves, rather than by parameters such as leaf area or biomass.

Deposition can affect also fruits. Fruit interception capability, however, is lower than that of leaves due to their ovoidal shape and their orientation toward the base of the plant. The interception values range from 0.2 to 1.2% of the sprayed activity for both radionuclides, depending on the plant stage at time of deposition (Table 6). Even though only four points are available for 134Cs and three points for 85Sr, it has been considered useful to draw some conclusions on the trend of the process. The values for the fruit interception of 134Cs and 85Sr in the three years have been correlated with their dry biomass (Table 6). As shown in Fig. 2 , results present a good positive linear correlation, with the determination coefficient r2 values of 0.89 and 0.80 for 134Cs and 85Sr, respectively.



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Fig. 2. Interception of radionuclides by fruits depending on biomass.

 
Leaf-to-Fruit Translocation
Leaf-to-fruit translocation coefficients (TCs) were calculated to represent the share of 134Cs or 85Sr activity found in fruits at ripening. The TC of the ith sample (TCi) is expressed by the ratio:

Translocation coefficients can be converted into dry weight by the dry matter content (Table 4).

The average values of the TCs following deposition at different growing stages are shown in Table 7. It is evident that 134Cs is translocated from leaf to fruit to a greater extent than 85Sr. The difference between the TCs for the two radionuclides is of one order of magnitude: 10-4 for 134Cs and 10-5 for 85Sr.


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Table 7. Leaf to fruit translocation coefficients following deposition at different growing stages.

 
When comparing the growing stages it appears that the highest TCs are obtained in plants contaminated at anthesis and before ripening. At these stages the translocation of both radionuclides from leaf to fruit reaches its highest intensity.

When deposition occurs at predormancy, in autumn, plants expose well-developed leaves to fallout, even if some are aged. They do not bear any flowers, fruits, or runners, but have developed flower buds for the next spring. At the resumption of growth, plants have lost all the old leaves and produce new ones that are initially nourished by the nutrients translocated to the storage organs, roots, and crowns the previous autumn. In the present study, the removal for dead and senescent leaves in spring, four months after contamination, removed the largest fraction of intercepted radioactivity, approximately (65.6 ± 5.1)% for 134Cs and (86.7 ± 6.8)% for 85Sr. A minor percentage of the intercepted radioactivity had been translocated to the storage organs before dormancy, or lost to the surrounding environment.

Following deposition at predormancy, the TCs for fruits at harvest are on average one order of magnitude higher for 134Cs than for 85Sr (Table 7). Fruits at the time of harvesting were divided into two groups: a first harvest, performed around 191 d after contamination, and a second harvest, performed 204 d after. The TCs calculated per each harvest (Table 7) show decreasing concentrations from the first to the second harvest: four times for 134Cs and two orders of magnitude for 85Sr. This occurs notwithstanding the decrease of fruit biomass, from 274.3 ± 10.5 to 222.6 ± 25.4 g plant-1 and the increase in dry matter content, from 6.2 ± 0.2 to 7.4 ± 0.5%, in the consecutive harvests, that, in conditions of constant uptake, would support an increase in radionuclide concentration per unit weight. The processes of radionuclide translocation to storage organs before dormancy, followed by their retranslocation to various plant components at the resumption of growth, probably favor a higher concentration in those fruits developed from the first buds in spring, fed by remobilized nutrients, than in fruits developed later in the season.

If deposition occurs when plants are bearing fruits, the fruit activity at harvest will be affected by the activity initially deposited on the fruit surfaces (Table 6). This is the case of plants contaminated at the stage of beginning of ripening (Table 7). It should be noted, however, that the contamination of fruits, harvested during the 30-d period after contamination, is the result of the processes of direct deposition, loss from fruit surfaces, leaf to fruit translocation, and growth dilution. These processes will affect the final activity of fruit depending on whether fruits are harvested just after the deposition or at various times later. The TC values reported in Table 7 represent the average activity of the whole harvest per plant.

By analyzing the TCs reported for 134Cs and for 85Sr in Fig. 3 , it is possible to study in more detail the trend of the radioactivity during the time of harvest. Fruits harvested during the first experimental year after deposition at the beginning of ripening were kept separate for each consecutive harvest, for a total of five harvests, during one month. The five harvests were performed 0, 5, 9, 15, and 26 d after deposition. The TCs ascertained in fruits at the first harvest (Day 0) can be ascribed to direct deposition on the exposed fruit surfaces. Their values are in fact quite similar for 134Cs and 85Sr: (1.7 ± 0.1) x 10-4 and (1.6 ± 0.1) x 10-4, respectively. In the following 26 d 134Cs TCs increase up to (5.0 ± 0.9) x 10-4 while those of 85Sr, after an initial decrease to (3.0 ± 0.5) x 10-5, remain fluctuating around an average value of (6.7 ± 1.8) x 10-5. The decrease of 85Sr TCs from the first to the second harvest (Day 5) is probably the result of the loss process from the fruit surfaces. Radionuclides deposited on fruits are only partially absorbed into the internal part of the fruit. A considerable fraction can therefore be lost in the environment. While this fraction is measurable for 85Sr, and corresponds to an average of 59 ± 2% of the intercepted activity, it is not the same for 134Cs, where the process of leaf-to-fruit translocation, greater than for 85Sr as reported above, probably overlaps and conceals that of loss.



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Fig. 3. Leaf to fruit translocation coefficients (TCs) in consecutive harvests following deposition at the beginning of ripening.

 
Residual Fraction in Time
The fraction of the intercepted 134Cs and 85Sr present in the aboveground part of the plant at various times after deposition was defined as residual fraction (RF). It represents the sum of the activity retained on the plant surfaces, of that absorbed but not translocated far from the point of application, and of that translocated to the new growth of the aboveground part, such as fruits. The residual fraction of the ith sample (RFi) is expressed by the ratio:

The RFs of 134Cs and 85Sr in the aboveground part of the plant have been reported, along with the activity intercepted at time 0, for plants contaminated at anthesis (Table 8) and for plants contaminated at predormancy (Table 9).


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Table 8. Activity in the aboveground part of the plant after deposition at anthesis.{dagger}

 

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Table 9. Activity in the aboveground part of the plant after deposition at predormancy.{dagger}

 
At the time of the fruit harvests, which occurred between the penultimate and final sampling, the whole of the aboveground part of the plant was not sampled. The RFs are therefore available for fruits, but not for the remainder of the shoot system. It is believed however that the plant activity at the time of fruit sampling is an interesting point, especially for plants contaminated at the predormancy stage. The theoretical RFs of the aboveground part of the plant (mainly leaves) at the dates of fruit harvests have been derived from the lines drawn between Days 33 and 80 for the second year and 26 to 70 for the third year (data in Table 8), and 163 to 234 (data in Table 9). The theoretical RFs of the aboveground part of the plant, calculated as reported above, have been summed up to the RFs of fruits. The sum is reported in Tables 8 and 9.

The RFs after deposition at anthesis for 134Cs in the second and third year and 85Sr in the second year are shown in Table 8. The residual fraction is radionuclide dependent. The RFs are higher for 85Sr than for 134Cs: 79.4 ± 11.5 and 45.4 ± 5.4 against 67.7 ± 8.9 and 32.1 ± 4.1 at 33 and 80 d, respectively, after deposition. The residual fraction is also year dependent: 134Cs values obtained in the third year, 61.1 ± 4.9 and 29.0 ± 2.0 at 26 and 70 d after deposition, respectively, are lower than those obtained in the second year.

The linear regressions of the residual fraction on the days from deposition have been calculated. The values of the determination coefficient, r2, are 1.0 for 85Sr second year, 0.99 for 134Cs second year, and 0.86 for 134Cs third year. The points corresponding to the Days 28, 39, 41, 46, 71, where the fruit activities have been included in the RFs of the aboveground part of the plant, fit well with the linear trend of the regression.

From the mathematical equations of the linear lines the parameters of the environmental half-time, tw, have been calculated. The environmental half-time is the time necessary for one-half of the radioactivity to be removed by environmental processes. The tw values, when deposition occurs at anthesis, are 74 d for 85Sr second year, 59 d for 134Cs second year, and 46 d for 134Cs third year. If the data for 134Cs are considered together, irrespectively of the year, a tw value of 58 d is obtained.

The RFs after deposition at predormancy are shown in Table 9. The trend of radioactivity in leaves during the period of almost eight months is shaped by the loss of the directly contaminated leaves at the resumption of growth where a complete renewal of the aboveground part of the plant takes place. In the first four months (128 d) the RFs show a decrease from 100 to 86.7 ± 6.6 for 85Sr and to 65.6 ± 4.9 for 134Cs. Also as shown in Table 8, the slower decrease of 85Sr as opposed to 134Cs is clearly evident. The values of tw calculated for this period are 481 d for 85Sr and 186 d for 134Cs.

The removal of contaminated leaves causes a sharp drop in the RF values to 5.4 ± 2.4 for 134Cs and 2.3 ± 1.1 for 85Sr at the sampling time of 163 d after deposition (Table 9). It is evident at this stage that the previous trend has been reversed: the 134Cs values are higher than those of 85Sr. This remains effective until the last sampling, 234 d after deposition, when the RFs are 5.1 ± 0.3 for 134Cs and 0.8 ± 0.2 for 85Sr.

At fruit harvest dates of 191 and 204 d, the fruit activities have been included in the RFs of the aboveground part of the plant, giving values of 15.4 ± 1.1 and 7.5 ± 0.4 for 134Cs and 3.3 ± 0.2 and 1.4 ± 0.2 for 85Sr (Table 9). The RFs at this time show an increase, more pronounced for 134Cs than for 85Sr, ascribable to the fruit component of the plant.

The linear regressions of the residual fraction of 134Cs and 85Sr on the days from deposition after deposition at predormancy have been calculated. The derived r2 values are 0.87 for 134Cs and 0.76 for 85Sr. The tw values, derived from the total trend, are 114 d for 134Cs and 109 d for 85Sr.

Radioactivity in Plant and Soil at Harvest
The 134Cs and 85Sr activity in the various plant components at harvest has been defined as activity fraction (AF). The activity fraction of the ith sample (AFi) is expressed by the ratio:

The AFs of 134Cs and 85Sr in leaves, fruits, crowns, and roots following deposition at the three growing stages of predormancy, anthesis, and ripening are shown in Table 10. Average values have been reported when the AFs were available for more than one year. The AFs give a picture of the share of radioactivity expected in the different plant components at the time of harvest.


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Table 10. Activity of the plant components at harvest following deposition at different growing stages.

 
After deposition at predormancy the activity in the whole plant is the lowest, about 20% for 134Cs and 3% for 85Sr of the total intercepted, as a consequence of the removal of the largest part of directly contaminated biomass at the resumption of growth. Of all the plant components, fruit concentrates the largest percentage of radioactivity, with 61.6 and 53.3% of the total for both 134Cs and for 85Sr, respectively. Foliage contains 25.3% of 134Cs and 24.8% of 85Sr, crowns 9.5% of 134Cs and 18.9% of 85Sr, and roots 3.6% of 134Cs and 3.0% of 85Sr of the total plant activity.

When deposition occurs at anthesis the activity in the whole plant is 50% for 134Cs and 54% for 85Sr of the total intercepted. The largest percentage of radioactivity is found in leaves, the major receptors of radioactivity: 75.0% of the total for 134Cs and 95.4% for 85Sr. Among the other components, 134Cs is mainly allocated to fruits (18.6%), followed by crowns (5.9%) and roots (0.5%), while a small percentage of 85Sr is allocated to crowns (2.7%), fruits (1.8%), and roots (0.1%).

The trend of radioactivity in plants contaminated at ripening is similar to that at anthesis. The total radioactivity in the plant, however, is higher than at anthesis, 82% for 134Cs and 71% for 85Sr, given the shorter time between deposition and harvest. The distribution of 85Sr in the plant is quite similar to that at the stage of anthesis with 95.5% in leaves, 2.1% in fruits, 2.2% in crowns, and 0.2% in roots. For 134Cs, however, the percentage of radioactivity is higher in leaves (89.3%) and lower in fruits (6.5%) than that at anthesis. The remaining 3.7% is in crowns and 0.5% in roots.

The activity of the soil samples has been expressed as (Bq g-1 dry wt. soil)/(Bq intercepted). The average values of soil activity after deposition at predormancy, anthesis, and ripening are given in Fig. 4 . The days from deposition to harvest, 232, 65, and 39, have been reported in the graph instead of the growing stages.



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Fig. 4. Soil activity following deposition at different growing stages.

 
In general, the longer the time between deposition and harvest, the higher the activity in soil. This applies mainly to 134Cs, whose activity is also higher than that of 85Sr.

The data on the distribution of radioactivity in the two layers of soil have not been reported. However, they show that the largest fraction of activity, from 80 to 90%, is concentrated in the upper 4 cm for both 134Cs and 85Sr.


    DISCUSSION
 TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Interception
During the temperate-climate growing season the shoot system of strawberry rapidly changes its physical architecture (the proportion of crowns, leaves, and fruits) in a short period of time (Fig. 1). At anthesis, petioles are shorter and leaves are smaller and horizontally oriented, with a thinner cuticle on the upper leaf surface than at ripening, when older leaves are partially inclined to the bottom. The physical structure and spatial arrangement of the plant components affect the interception capacity of the shoot system, one of the factors contributing to seasonality, defined by Aarkrog (1992) as the varying response to radioactive contamination of environmental samples according to the time of the year when the contamination occurs.

Few studies have considered interception by fruit. Those results obtained in real-world conditions, such as in the aftermath of the Chernobyl accident, do not differentiate between direct and indirect contamination. There are no data on strawberries and the other few data available are not suitable for comparison, being obtained in different experimental conditions and/or expressed with different units of measure. Direct contamination of apples (Malus domestica Borkh.) was 5% of the applied activity for 134Cs and 85Sr (Bengtsson, 1992). The interception of 238Pu-bearing particles by orange [Citrus sinensis (L.) Osbeck] fruit was approximately 0.11% of the deposition (Pinder et al., 1987) and the authors calculated that approximately 0.8% of the deposited 238Pu would be intercepted by fruits in mature orchards. The order of magnitude of interception is similar to that obtained in this work for strawberries, ranging from 0.2 to 1.2% of the applied activity.

Leaf-to-Fruit Translocation
Fruit can also receive radionuclides via translocation from contaminated foliage. After leaf interception, which is higher for 85Sr than for 134Cs (see above), radionuclides are absorbed into the leaf. The rate of penetration of cations through the cuticle is inversely related to the size of the hydrated ion, so that Cs is absorbed more readily than Sr (Swietlik and Faust, 1984). After leaf absorption, the radionuclides can be translocated to fruit through the phloem. The efficiency of translocation is radionuclide dependent. Cesium, chemically analogous to potassium, is mobile in the phloem transport system, while strontium, a calcium analog, is virtually immobile (Marschner, 1986).

The contamination of fruit arises from leaf-to-fruit translocation when deposition occurs at anthesis. The fruit activity has been expressed as the percentage of the applied activity for comparison with literature values. Values of 15% for 134Cs and 1.6% for 85Sr confirm the higher mobility of Cs compared with Sr. Following contamination of strawberries via application of droplets to leaves, Kopp et al. (1990) found that 20% of the applied Cs and 0.3% of the applied Sr was translocated from leaf to fruit. In similar experiments, Zehnder et al. (1993)(1996) ascertained that while 28 to 36% of applied 134Cs was translocated from leaf to fruit, no 85Sr was found in the fruit.

Results on fruit contamination obtained after deposition at the beginning of ripening, 7% for 134Cs and 2% for 85Sr, are not comparable with those reported in the literature on leaf-to-fruit translocation, being mainly the result of direct deposition on fruit. In contrast to data on leaf-to-fruit translocation, the order of magnitude of fruit contamination is the same for 134Cs and 85Sr. Cesium-134 activity is lower than that derived from the leaf to fruit translocation, while 85Sr activity is higher.

Fruit contamination after deposition at predormancy deserves a different comment. A proportion of the radionuclides intercepted by, and absorbed into, the leaves is remobilized and translocated to the storage organs before leaf drop. Remobilization is the decrease in the net content of elements in leaves (Marschner, 1986). It is highly selective for mineral elements and depends on the concentration of mineral elements in the fully expanded leaves (Loneragan et al., 1976; cited by Marschner, 1986). Given that Cs, as reported above, is better absorbed than Sr and more mobile in the phloem, its remobilization and translocation to roots and crowns is presumably higher than that of Sr. The lower activity of 134Cs than 85Sr in dead leaves denotes its higher remobilization. A few months later, the activity in ripe fruits, being one order of magnitude higher for 134Cs than for 85Sr, is an indication of the higher translocation of 134Cs than 85Sr from roots and crowns to fruits. Strawberry fruits have been shown to act as sink for cesium (Zehnder et al., 1993).

Following deposition at the various growing stages, activity in fruit is not only the result of a different interception capacity by the shoot system, as indicated in the mathematical expression of the TCs, but also of different absorption and remobilization capacities. Absorption is not only radionuclide specific as reported above, but also depends on leaf senescence. Leaf age is a parameter that seems to reduce the absorption of radioactivity (Aarkrog, 1969). On this basis it can be assumed that leaf absorption is higher at anthesis than at ripening or even more at predormancy. On the other hand, the extent of remobilization depends on the plant growing stage. For example, during the reproductive stage the degree of remobilization of micronutrients and of calcium is often astonishingly high compared with that during vegetative growth (Marschner, 1986). It follows that the process of leaf-to-fruit translocation is highest at anthesis. This is particularly evident for 134Cs. All the factors discussed above contribute to seasonality.

Residual Fraction in Time
The residual fraction in the aboveground part of the plant at various times after deposition is the result of processes of external loss (Lext), from the aboveground part to the environment, and of internal loss (Lint), from the aboveground part to other plant components (Carini and Bengtsson, 2001). External loss is due to the action of wind, abrasion between leaves, and shedding of cuticular wax. The action of rain is excluded in this case since plants were placed in a tunnel, while fog, dew, and air humidity can all contribute to Lext. Radionuclides, mainly cesium, also undergo Lint: absorption, remobilization from leaves, and translocation from the point of application. Different climatic conditions in different years (e.g., wind, humidity, temperature) can produce different residual fractions in the plant.

The results summarized here show that the residual fraction of 134Cs after deposition at anthesis is lower than that of 85Sr. These results confirm the study of Kopp et al. (1990) on the kinetics of foliar uptake for 134Cs and 85Sr into strawberry plants, showing that the loss from the directly contaminated leaves after 62 d is higher for 134Cs than for 85Sr. However, a more detailed analysis of the results does not provide conclusive evidence for a higher loss of 134Cs than 85Sr from the plant (see below). This trend is only evident after deposition at anthesis, when the metabolic activity of the plant and the process of leaf to fruit translocation reach their highest intensity and 134Cs is translocated to other plant components and fruits to the largest extent.

The environmental half-time, tw, reported in literature, is determined per unit area of ground, which excludes the effect of growth dilution, or per unit mass of vegetation (Pröhl and Hoffman, 1996). In the present work tw was determined per plant and is the same as per unit area. It should be noted that the tw values, not being a specific object of this work, have been calculated even where only few points were available. They are probably associated with a considerable uncertainty and can only be considered as indicative of a trend. The tw values calculated after deposition at anthesis, 59 and 46 d for 134Cs and 74 d for 85Sr, are considerably higher than the mean value of 11 d (geometric mean, with a range of 4.5 to 34 d) reported in the literature for herbaceous vegetation per unit ground area (Miller and Hoffman, 1983; cited by Pröhl and Hoffman, 1996). The tw data reported in the literature have been obtained in field conditions, where precipitation increases the process of loss through wash off from the surface and leaching of radionuclides from the leaf tissues. In experiments in which the environmental half-time was determined simultaneously on experimental plots protected against rain, significantly longer values for tw were observed (Ertel et al., 1989; Krieger and Burmann, 1969; cited by Pröhl and Hoffman, 1996). Ertel et al. (1989) found a tw of >60 d for grass grown in pots protected from rain, and a tw reduced by a factor of 2 (30 d) for plots not protected from rain. Data for fruit plants, produced in greenhouses or in precipitation-free conditions (Kopp et al., 1990; Bengtsson, 1992; Zehnder et al., 1995) show lower loss of radionuclides than data obtained under field conditions (Carini et al., 1999; Carini and Lombi, 1997).

As discussed by Pröhl and Hoffman (1996), the stage of plant growth plays an important role in determining the removal rate of radionuclides from the plant. Some studies indicate that processes of radionuclide removal from the surfaces of herbaceous vegetation (mostly grasses) may be substantially reduced after the plant dies or becomes dormant (various authors, cited by Pröhl and Hoffman, 1996). In contrast, shedding of waxes was demonstrated to be greatest when plants are growing quickly (Juniper, 1960). After deposition on strawberries at the stage of predormancy the tw values calculated for the first slope of the curve, a lapse of four months, are considerably higher than those calculated after deposition at anthesis: 186 d for 134Cs and 481 d for 85Sr. These, however, only give an indication of the trend, because they are derived from two points. The longest environmental half-lives reported in the literature were obtained for dormant vegetation, with a geometric mean value of 25 d and a range from 5 to 49 d, although these values were obtained for plants not protected from rain (Pröhl and Hoffman, 1996).

Senescence of leaves is a mechanism for radionuclide removal. After removal of dead contaminated leaves from strawberry plants, the residual fraction is considerably reduced. At this stage the RF is the result of the process of translocation of radionuclides from roots and crowns, where they had been stored before dormancy, to the new emerging leaves. Before dormancy 134Cs is probably translocated through the phloem toward the storage organs more than 85Sr. For this reason the RFs in new leaves are higher for 134Cs than for 85Sr.

The tw values derived from the whole period after deposition at predormancy cover an initial period of four months during which the vegetation was dormant (see above), and a second period of four months during which the plants were growing quickly and fruiting. The tw values are similar for 134Cs and 85Sr, 114 and 109 d respectively, and their extent reflects the rain-protected location of plants.

Radioactivity in Plant and Soil at Harvest
Following deposition at predormancy the largest percentage of radioactivity for both radionuclides is allocated to fruit. This means that 134Cs and 85Sr, translocated to the storage organs before dormancy and retranslocated at the resumption of growth to new shoots and leaves, are highly remobilized during fruit development (see above). To give an example of high remobilization during the reproductive stage, in lupine (Lupinus albus L.) up to 50% of the micronutrients and 18% of the calcium that originally accumulated in the leaves were retranslocated to the fruits (Hocking and Pate, 1978; cited by Marschner, 1986).

The distribution of each radionuclide in the plant components is similar after deposition at anthesis or at ripening. In general 134Cs shows a tendency to be allocated to fruits, which act as a sink for potassium for strawberry plants, while 85Sr tends to remain in leaves and crowns. Similar results were found in experimental work on grape vines (Vitis vinifera L.) contaminated via leaves, where at ripening 48% of 134Cs was concentrated in berries while 57% of 85Sr remained in leaves (Carini and Lombi, 1997).

A fraction of the radioactivity intercepted by the plant is found in the soil at the end of the growing cycle. This is ascribable to the process of translocation of radionuclides from leaves to roots, followed by root exudation and root loss (Hale et al., 1978). Translocation mainly depends on radionuclide mobility in the phloem and on the plant. In greenhouse studies on grape vines Zehnder et al. (1995) reported that a large percentage of radiocesium, but not of radiostrontium, can be released from the plants to the soil. However, other studies performed on grape vines in open field conditions found similar concentrations of 134Cs and 85Sr in soil (Carini and Lombi, 1997). This is ascribable to the action of wind and rain on the loss of radionuclides from the system and subsequent deposition to the soil.

In the present work the activity of 134Cs in the soil is higher than that of 85Sr, and confirms its higher remobilization from the leaves and translocation to other plant components, such as roots. The activity translocated to soil increases with time, with a trend opposite to that in the whole plant, which goes through a process of decontamination. At the end of the longest period considered in this work (i.e., eight months after deposition), plant activity is similar to that of soil for 134Cs and even lower for 85Sr.

The sum of the activities in plant and soil for each stage is always higher for 134Cs than for 85Sr, and reveals a higher loss of 85Sr from the soil–plant system. Even if 134Cs, as reported above, undergoes a higher loss from the leaves than 85Sr at anthesis, its activity in the whole plant is generally higher than that of 85Sr. Incorporation into internal tissues reduces its external loss and allows translocation to the other plant components, and eventually to the soil, to take place.


    CONCLUSIONS
 TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
From the experimental work performed on strawberries to evaluate the behavior of 134Cs and 85Sr at short term after deposition, the following conclusions can be drawn:


    ACKNOWLEDGMENTS
 
The authors are grateful to the Food Standards Agency (United Kingdom) for their financial support for the experimental work. Financial support for the publication of this paper was provided by the Università Cattolica under their programs of promotion and dissemination of the scientific research for the year 2003. The authors are also indebted to Dr. Walther Faedi (Experimental Institute for Fruit-Growing of Rome, Manager of the Department of Forlì, Italy) who gave his invaluable assistance with advice on strawberry growth and management, and to the staff of the Institute of Pathology of the Università Cattolica (Piacenza) that placed the LAM (leaf area meter) at their disposal.


    NOTES
 TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Sponsoring organization: Food Standards Agency, United Kingdom.


    REFERENCES
 TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 


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