Published online 12 October 2005
Published in J Environ Qual 34:1972-1979 (2005)
DOI: 10.2134/jeq2004.0412
© 2005 American Society of Agronomy, Crop Science Society of America, and Soil Science Society of America
677 S. Segoe Rd., Madison, WI 53711 USA
TECHNICAL REPORTS
Plant and Environment Interactions
Is the Transfer Factor a Relevant Tool to Assess the Soil-to-Plant Transfer of Radionuclides under Field Conditions?
T. Centofantia,*,
R. Penfieldb,
A. Albrechta,c,
S. Pellerind,
H. Flühlerb and
E. Frossarda
a Plant Nutrition, Institute of Plant Sciences, ETH Zurich, Eschikon 33, CH-8315 Lindau (ZH), Switzerland
b Soil Physics, Institute of Terrestrial Ecology, ETH Zurich, Grabenstrasse 11a, CH-8952 Schlieren, Switzerland
c ANDRA Direction Scientifique, Service Transferts, Parc de la Croix Blanche 1/7, rue Jean-Monnet, F-92298 Chatenay-Malabry Cedex, France
d Institut National de la Recherche Agronomique, UMR Transfert sol-plante et cycle des éléments minéraux dans les écosystèmes cultivés, BP 81, F-33883 Villenave-d'Ornon Cedex, France
* Corresponding author (tiziana.centofanti{at}googlemail.com)
Received for publication November 5, 2004.
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ABSTRACT
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The radiological impact of radionuclides released to the terrestrial environment is usually predicted with mathematical models in which the transfer of radionuclides from soil to the plant is described with the transfer factor (TF). This paper questions the validity of the protocols proposed by the International Atomic Energy Agency to measure TF in the field and in greenhouses conditions. We grew maize (Zea mays L.) both in the field after a surface application of radionuclides (54Mn, 57Co, 65Zn, and 134Cs) and in a greenhouse with the same soil that has received the same fertilization and that had been previously sieved and homogeneously labeled with the same radionuclides before being repacked in pots. The analysis of the displacement of radionuclides in the field soil profile showed a higher concentration of the surface-applied radionuclides in the preferential flow path (PFP) in comparison to the soil matrix indicating that they infiltrated heterogeneously in the soil profile due to the structure-induced non-uniform water flow. A significantly higher recovery of 57Co and 134Cs was observed in the plants grown in the field soil, whereas no differences in the recovery of 54Mn and 65Zn between the two experiments were detected. These results suggest that (i) under field conditions the soil-to-plant transfer of radionuclides that co-exist as stable elements present at low concentrations in the soil and in the plant is higher than that measured under greenhouse conditions and (ii) the implicit assumption made when calculating the TF (that radionuclides are homogeneously distributed in the soil profile) is not valid, thereby preventing the calculation of an average concentration to obtain the TF parameter.
Abbreviations: PFP, preferential flow path TF, transfer factor
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INTRODUCTION
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THE RADIOLOGICAL IMPACT of radionuclides released to the terrestrial environment is usually predicted with mathematical models in which the transfer of radionuclides from the soil to the plant is described with the transfer factor (TF) defined as the ratio of the radionuclide concentrations in vegetation and soil (International Atomic Energy Agency, 1994). Transfer factors are determined either in greenhouses or field studies, meaning implicitly that results obtained under both conditions are comparable. The greenhouse experiments are performed with plants grown in pots filled with a sieved soil that has been homogeneously labeled with radionuclides. The field experiments are mostly making use of the fallout products naturally incorporated in the field soil by infiltration, bioturbation, and other mixing processes. The fallout products are the radionuclides deposited after the nuclear weapon tests in the 1950s and 1960s, after the Chernobyl accident in 1986, and after controlled release from nuclear installations (International Atomic Energy Agency, 1994). In the International Atomic Energy Agency (1994) handbook of parameter values for the prediction of radionuclide transfer, TF values are standardized for a homogenously contaminated soil layer of 20 cm for crops and of 10 cm for pasture.
Ehlken and Kirchner (2002) have recently criticized the use of the TF to study the transfer of radionuclides from the soil to the plant. These authors point out that the TF integrates various soil and plant properties and processes, each of which showing its own variability and being influenced by external factors. Soil structure, for instance, might affect the soil-to-plant transfer of surface-applied radionuclides as it controls (i) the distribution of water and solutes in the soil (Flury et al., 1994; Stamm et al., 1998; Bundt et al., 2000; Albrecht et al., 2002), (ii) the rate of exchange of ions between the solution and solid phase of the soil and therefore their availability to plants (Sinaj et al., 1997, 1999; Bühler et al., 2003), and (iii) the rooting pattern of plants (Bundt et al., 2000; Stewart et al., 1999; Pierret et al., 1999).
This paper questions the validity of the protocols proposed by the International Atomic Energy Agency (1994) to measure TF in the field and in greenhouses conditions. The hypotheses of this paper are the following. First, surface-applied radionuclides become heterogeneously distributed in the profile of soils that exhibit active preferential flow paths (PFPs, zones in which a rapid transport of water and solutes is observed). The presence of PFPs and the fact that these soil regions are preferred locations for root development prevents the calculation of a relevant average radionuclide concentration in the upper soil horizon and therefore the calculation of TF. Second, radionuclide uptake by maize measured in the greenhouse differs from the uptake of radionuclide observed in the field also when both experiments are performed with the same cultivar, soil, and fertilization. This systematic deviation of the system response makes the test system (greenhouse experiment) unrepresentative for the system under investigation (field soil).
To test these hypotheses we grew maize (cv. Corso) both in the field after a surface application of radionuclides (54Mn, 57Co, 65Zn, and 134Cs) and in a greenhouse with the same soil that had received the same fertilization and had been previously sieved and homogeneously labeled with the same radionuclides. Plant growth, radionuclides, total Mn, Co, Zn, Cs, and macronutrient (N, P, and K) uptake, and root weight density were analyzed both in the field and in a pot experiment. In the field experiment radionuclides displacement in the soil profile and the interrelation between roots and PFP distribution patterns were analyzed.
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MATERIALS AND METHODS
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Field Experiment
Soil Characteristics
The study was performed on a field site located at Eschikon (47°27' N, 8°41' E; 550 m elevation), 20 km east of Zurich, Switzerland, on a Gleyic Cambisol (Food and Agriculture Organization of the United Nations, 1974). Selected soil chemical and physical properties are given in Table 1. The field has a slope of around 1%. The experimental plot has been under grassland and has not been plowed for the last 30 yr.
Experimental Design of the Field Study
The three plots were separated 0.15 m from each other. The plots were 5.6 x 1.05 m. The plant density was 8.3 plants m2, with 0.80 m between rows and 0.15 m between plants in the row. The radionuclide solution was applied on the central area (2.4 x 0.45 m) of each plot encompassing the central three rows and three plants per row. Plants were sampled in these central plots only. The area outside the central plots was used to minimize edge effects (Fig. 1)
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Fig. 1. Plot design. (A) Overview of the layout in the field experiment. The symbol "x" = plants; gray areas = traced with radionuclides; white areas = buffer to minimize edge effects. (B) Sampling scheme in traced area. Black horizontal lines = position of the vertical profiles; dashed area = location of the horizontal planes; white circles = auger sampling.
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Radiotracer Application
On 23 July 2001, a solution containing 54Mn, 65Zn, 57Co, and 134Cs, all in chloride form diluted in an acidic solution, was applied onto the soil surface of the three central plots (Table 2). Radionuclides were purchased from Amersham (Little Chalfont, UK). The solution was applied manually, using a watering can with a sprinkling bar fixed at the end of the spout. To avoid surface ponding the solution was applied in 12 slops of equal amounts of 10 L in a period of 6 h. The 120 L of solution contained 71, 33, 9.5, and 37 kBq mL1 of 54Mn, 57Co, 65Zn, and 134Cs, respectively, dissolved in Osmosis I water of an electrical conductivity of 17 µS cm1 at 25°C. To avoid lateral infiltration toward the rows, a similar volume of Osmosis I water was applied at the same rate on the buffer area outside the central plots.
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Table 2. Characteristics and quantities of 54Mn, 65Zn, 57Co, and 134Cs applied to (i) the soil surface of an untilled agricultural soil (field experiment) and (ii) the same homogenized soil (pot experiment).
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Plants
On 20 May 2001, the grass was burnt and a solution of 1% of glyphosate (RoundUp; Monsanto, St. Louis, MO) was applied at the rate of 0.42 mL m2. Furrows were manually prepared and maize was sown on 22 July 2001. After sowing, the soil was fertilized with 110 kg N ha1 as NH4NO3, 41 kg P ha1 as KH2PO4, and 125 kg K ha1 as KCl as recommended for maize production in Switzerland (Ryser et al., 2001). Fertilizers were manually applied in a solid form. The plants were not irrigated to reduce radiotracer mobility during the experiment. During the growing period plant height was measured regularly. A weather station placed 60 m from the site recorded air and soil temperatures, rainfall, and solar radiation (Table 3). On 17 Sept. 2001, after two months of growth when plants had reached pollen shed, the shoots were harvested by cutting the stem 1 cm above the soil level, and then washed with tap water, chopped, and oven-dried at 105°C for 24 h. The whole shoot was used for plant analyses. The dry weight was determined and the dry material milled to powder. A portion of the sample was used to measure Mn, Zn, Co, Cs, K, N, and P while the remaining part was weighted and transferred into calibrated
-spectrometry containers to measure the activities of the radionuclides. Nitrogen was extracted by using the Kjeldahl method, whereas the other elements, after ignition of the sample at 500°C for 1 h, were extracted with 2 mL of 0.1 M HCl solution, filtered through a Whatman (Maidstone, UK) no. 40 ashless cellulose filter, and diluted to 50 mL with deionized water. The concentration of P in the diluted solution was measured by colorimetry using the method of Murphy and Riley (1962) while the concentration of cations was measured by atomic absorption spectroscopy.
Dye Tracer Application and Analysis of Radionuclide Distribution on Soil Vertical Profiles
On 17 Sept. 2001, the dye tracer Brilliant Blue FCF was applied immediately after harvest onto the soil surface to visualize the PFP (stained areas) from the soil matrix (unstained areas). To avoid surface ponding the solution was applied in 12 slops of equal amounts of 10 L in a period of 6 h. The 120 L of solution contained 5 g L1 of Brilliant Blue FCF dissolved in Osmosis I water of an electrical conductivity of 17 µS cm1 at 25°C. To avoid lateral infiltration toward the rows, a similar volume of Osmosis I water was applied at the same rate on the buffer area outside the central plots.
On 18 Sept. 2001, in delineated depths of 0 to 5, 5 to 15, and 15 to 35 cm, samples were taken with a small spatula from the stained regions, representing preferential flow paths, and from the unstained soil matrix. The results on the correlation between the dye tracer and the radionuclide activities are described by Penfield et al. (unpublished data, 2002).
Mapping Root and Flow Path Distribution
On each plot two horizontal planes were prepared above each other at depths of 0.2 and 0.4 m, respectively. They had an area of 0.45 m parallel to the row and 0.8 m perpendicular to the row (Fig. 1). On the two horizontal planes the occurrence of roots intersecting the plane of observation was mapped with a felt-tip pen onto polythene sheets with a grid of 0.05 x 0.05 m to systematically locate and document root occurrence (Tardieu and Manichon, 1986). A second sheet was used to trace the PFP by drawing the contours of the stained areas. Root maps were scanned and digitized using Scion Image (Version ß 4.02; Scion Corp., Frederick, MD) for recording the x,y coordinates of the individual roots. Maps of the PFP areas were scanned and digitized using IDL (Version 4.01 of Interactive Data Language; Research Systems Inc., Boulder, CO) to determine the dye coverage (fraction of stained area in relation to the exposed plane). The corners of the grid borders were used as reference points to superimpose the flow path and root map. The number of roots occurring within the PFP was determined for the three plots. All three plots displayed similar root and stained area patterns and thus only the maps obtained from the middle plot are shown as an example (Fig. 2)
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Fig. 2. Superimposed maps of root occurrence (open circles) and stained preferential flow paths (black areas) observed on the two horizontal planes at 20- and 40-cm depths.
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Root Weight Density
In each plot six cylindrical cores (0.20 m long and 0.05 m in diameter) were sampled at two depths (00.20 and 0.200.40 m) using a hand-held auger. To obtain a realistic representation of the root distribution in relation to the plant position, four samples were taken at 0.05 m from the plant row and at 0.40 m from the plant row, where root density tends to decrease (Fig. 1). Soil was rinsed off from the root samples using the hydro pneumatic elutriation system (Gilson, Middleton, WI) developed by Smucker et al. (1982). Roots were freeze-dried for 48 h. Root dry weight was determined and the root weight density (g cm3) calculated. Measurements of the radionuclide activities in root samples obtained from the field experiment were discarded as they were unreliable due to the fine soil particles adhering on the root epidermis.
Pot Experiment
Untreated soil was collected from the area surrounding the field experiment. The quantity of soil taken from the field site corresponded to an area of 0.72 m2 (1.6 x 0.45 m) and a depth of 20 cm. The soil was air-dried at 24°C for 1 wk. Stones and plant debris were separated and the soil was sieved at 6 mm. On 12 Dec. 2001 the sieved soil was divided into two portions of 90 kg and each portion was spiked with a solution containing the four radionuclides used in the field experiment (activities are shown in Table 2) and 35 L of Osmosis I water. This amount of water was chosen to bring the soil water content to a value of 0.28 m3 m3 which corresponds to the water content of the field soil measured after plant harvest in samples taken from 0 to 0.20 m depth (average value). To obtain a homogeneous activity, each soil portion was mixed with the solution for 3 h in a rotating concrete mixer. The labeled soil was divided in six equal parts of 30 kg (dry weight) and repacked in plastic pots (0.26 x 0.36 m and 0.25 m deep). To test the homogeneity of the radioactivity a sample was taken from each pot and the activity measured by
-spectroscopy. The coefficient of variation of these activities was 0.28 to 0.31. On 13 Dec. 2001 one seed of maize was placed in the middle of each plot at a depth of 3 to 4 cm corresponding to a sowing density of 10 plants m2. On the same day, the equivalent of 110 kg N ha1 as NH4NO3, 41 kg P ha1 as KH2PO4, and 125 kg K ha1 as KCl were manually applied in solid form onto the soil surface of each pot. Plants in the greenhouse grew under the following conditions: 16-h photoperiod, day and night temperatures of 25 and 20°C, respectively, 40 to 50% relative humidity of ambient air, and 300 µmol photons m2 s1 minimum light intensity (provided as artificial light by 400-W DL/BH lamps; EYE, Tokyo, Japan). Plants were watered with Osmosis I water by a time-controlled automatic watering device. The total amount of water given to the plants for two months was about 300 mm, approximately equivalent to the amount of rainfall monitored during the field experiment (Table 3). No leaching occurred in the pot experiment. During the growing period plant height was measured regularly.
On 13 Feb. 2001, after two months of growth when plants reached pollen shed, the stem was cut 1 cm above the soil level. Two core samples (20 cm long and 5 cm in diameter) were taken from each pot at 5 and 13 cm from the stem, using a hand-driven auger. Identical procedures as described in the field experiments were used for plant and root analysis.
-Spectrometry
All samples were analyzed for 65Zn (half-life, t1/2 = 243.9 d, 1115.55 keV), 57Co (t1/2 = 271.7 d, 122.06 keV), 54Mn (t1/2 = 312.2 d, 834.84 keV), and 134Cs (t1/2 = 2.07 yr, 475.34 keV) at the
-spectrometry laboratory of EAWAG (Swiss Federal Institute for Environmental Science and Technology, Dübendorf, Switzerland) using high purity Ge detectors. Plant, root, and soil samples were measured with flat crystals. Radionuclide activities were determined in Bq g1 (dry weight); decay was corrected to the common date of 18 July 2001, 1200 h. The measurement errors were 5 to 10%. Geometry correction and calibration are based on standard solutions. The recovery of radionuclide in the aerial parts of the plant was calculated as the ratio of total activity measured in the shoot (Bq) to the total activity applied to a single plant (Bq) and expressed in
. The specific activity of radionuclide in the aerial parts of the plant was calculated as the ratio of radionuclide recovery in a plant to the total amount of element present expressed in mg.
Statistical Analysis
Significant differences between the mean values, calculated for plant dry matter production, plant uptake, root weight density, and concentration of radionuclides measured in the soil matrix and PFP, were tested by analyzing the variance (ANOVA) and Duncan's multiple range test. All tests were conducted at the 5% significance level. The analyses were performed with Statgraphics software Version 3.1 (Manugistics, 1997).
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RESULTS
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Plant Growth and Radionuclide Uptake in the Field and Greenhouse
After two months of growth, the overall shoot production had reached 54.6 g plant1 in the field experiment and 36.0 g plant1 in the greenhouse which was equivalent to a production of 4.7 Mg dry matter ha1 in the field and 3.8 Mg dry matter ha1 in the greenhouse. The height and shoot dry matter production did not differ significantly between maize grown in the field and in the greenhouse (Table 4). The higher shoot biomass observed in the field can be explained by the higher total light radiation received by the plant in the field. Values of root weight density (Table 5) obtained in the upper 0 to 20 cm of the soil profile in the field experiment did not differ from those obtained in the pot experiment. In the field experiment root weight density values showed an abrupt decrease between 20 and 40 cm of soil depth which might be explained by the high bulk density of the B horizon (Table 1).
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Table 4. Plant height and dry matter measured after two months of maize grown in the field and under greenhouse conditions.
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Table 5. Root weight density values obtained from the field experiment (at two different depths: 020 and 2040 cm) and from the pot experiment.
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The concentrations of P and N measured in the shoots were higher in the plants grown in the field than in the greenhouse (Table 6). Since 2.5 to 3.5 mg P g1 dry matter is needed in the aerial parts of maize for optimum growth (Bergmann, 1992) the two groups of plants had sufficient levels of P. The use of the model proposed by Plénet and Lemaire (1999) to assess the critical concentration of N in maize shoot showed that plants from both sites were N deficient although they had received the rate of N fertilization recommended by the Swiss Federal Stations for Agricultural Research (Ryser et al., 2001). The critical N concentration of plants grown in the field was 1.9% whereas they contained only 1.6% N and the critical N concentration of plants grown in the greenhouse was 2.0% whereas their actual N content was 1.1%. The concentration of K measured in the shoots of the field-grown maize was within the range required for a normal growth (1723 mg K g1 dry matter; Bergmann, 1992) (Table 6). The shoot of greenhouse-grown maize presented significantly higher K concentration than the field-grown plant (Table 6). The recovery of 54Mn and 65Zn and the total Mn and Zn concentrations in the aerial parts of maize were similar in the field and in the greenhouse experiment (Tables 6 and 7). The recovery of 57Co was two times higher in the shoots of maize grown in the field (Table 7), while the total Co concentration was identical in the two groups of plants (Table 6). Ten times more 134Cs was recovered in the shoots of maize grown in the field than in the shoots of maize grown in the greenhouse. The total Cs concentration was higher, although not significantly, in the shoots of the field-grown plants. The Zn and Mn specific activity of the shoots of maize grown under field or greenhouse conditions was similar whereas Cs and Co specific activity was two times higher in the shoots of the field-grown maize (Table 8).
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Table 6. Concentration of Mn, Zn, Co, Cs, P, N, and K in the shoots of maize after two months of growth under field conditions (field experiment) and in the greenhouse (pot experiment).
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Table 7. Recovery of applied radionuclides in the aerial parts of maize grown under field conditions (field experiment) and in a greenhouse (pot experiment). In the field radionuclides were applied onto the soil surface while in the greenhouse the soil had been sieved and homogeneously labeled with the radionuclides before being repacked in pots.
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Table 8. Specific activity of Mn, Zn, Co, and Cs calculated for the aerial parts of maize after two months of growth either under field conditions (field experiment) or in a greenhouse (pot experiment).
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Displacement of Surface-Applied Radionuclides and Relation between Roots and Preferential Flow Path Distribution Patterns
Surface-applied radionuclides were distributed heterogeneously in the soil profile. All four radionuclides showed significantly higher concentrations in the PFP compared to the soil matrix. They were more concentrated in the upper 0 to 15 cm of soil depth and displayed much lower concentration with depth (Fig. 3) .

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Fig. 3. Concentration of 54Mn, 65Zn, 57Co, and 134Cs measured in the soil matrix (unstained) and in preferential flow paths (stained). Mean and standard error are given. The symbols *, **, and *** indicate significance at the 0.05, 0.01, and 0.001 probability levels, respectively; while n.s. is not significant and n.d. is not detectable.
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The analysis of the overlaid root and PFP maps (Fig. 2) showed that at 0.20 m depth PFP covered 11% of the analyzed area and that 15% of the roots were in the PFP. At 0.40 m depth, PFP covered 6% of the analyzed area and 9% of roots were in these areas.
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DISCUSSION
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The first hypothesis of our paper stating that surface-applied radionuclides distribute heterogeneously in the profile of soils presenting active PFP is confirmed. The higher concentration of the surface-applied radionuclides observed in the PFP in comparison to the soil matrix indicates that they infiltrated heterogeneously in the soil profile due to the structure-induced non-uniform water flow, and consequently a fraction of each radioactive element remained sorbed on the soil particles in the vicinity of the PFP. This result supports those of Bundt et al. (2001) and Sinaj et al. (2002) who observed a high radionuclide activity and P concentration sorbed on soil particles within and around the PFP. In our experiment the concentration of radionuclides in the PFP was significantly higher than that in the soil matrix at all soil depths analyzed except at 25 to 35 cm for 54Mn and 57Co. This result indicates that in structured field soils the implicit assumption made in the calculation of the TF that radionuclides are homogeneously distributed in the soil profile is not valid, thereby preventing the calculation of an average concentration to obtain the TF parameter.
The second hypothesis of our paper stating that radionuclide uptake by maize observed in the greenhouse is different (also not representative) from the uptake of radionuclide observed in the field was validated for 134Cs and 57Co but not for 54Mn and 65Zn. In the following we present arguments that could help explain these results.
As Cs uptake depends on the K concentration in the solution and on K uptake by the plant (Zhu and Smolders, 2000) we hypothesize that the lower uptake of 134Cs in the greenhouse was related either to the higher soil K availability in the sieved soil and/or to the lower plant demand for K in the greenhouse. The concentration of water-extractable K measured after 14 d in a batch experiment conducted with the soil sample used for the greenhouse experiment (i.e., sieved at 6 mm) and with the nonsieved soil with a 1:3 soil to water ratio, reached 504.3 µg L1 (±76.1) in the sieved soil against 267.7 µg L1 in the nonsieved soil (±50.3) suggesting that soil K availability was higher in the sieved soil. This higher K concentration in the soil solution might have decreased Cs uptake as, at high K concentration, plants take up this cation through a K+ channel that shows a high discrimination against Cs (Zhu and Smolders, 2000). The low plant demand for K in the greenhouse is shown by its low N to K ratio of 0.3 whereas maize growing under nonlimiting conditions has a N to K ratio of 1.5 (International Fertilizer Industry Association, 1992). The N to K ratio of shoots of field-grown maize plants reached 0.8. The low plant demand for K in the greenhouse is most probably related to the overall limited plant growth itself due to insufficient light and strong N deficiency. Since K and Cs are taken up by similar mechanisms, the less K is taken up, the less Cs the plant will contain. As Cs is not or very little transported by the hyphae of arbuscular mycorrhizal fungi (Joner et al., 2004), which usually colonize the roots of maize, the higher Cs specific activity observed in the shoots of field-grown maize might be related to the activity of roots exploring soil zones enriched with 134Cs, that is, either the first 0 to 5 cm of the profile or the PFP located between 5 and 25 cm. However, as fine roots of corn are the major sites of water and nutrient uptake into a mature root system and only became active at about 10 to 20 cm from the main axis tips (McCully, 1999), we suggest that this higher 134Cs uptake was mainly due to the exploration of PFP located between 5 and 25 cm.
The lower uptake of 57Co is more difficult to explain. The total Co concentration in the shoot of maize grown in the greenhouse or under field conditions is in the same order of magnitude as the Co concentration reported for the shoot of rye grass (Loué, 1988). As for Cs the higher Co specific activity observed in the shoots of the field-grown plants could probably be explained by the activity of roots exploring soil zones enriched with 57Co (i.e., the PFP located between 5 and 25 cm) as this element is also very little or not transported by the hyphae of arbuscular mycorrhizal fungi (Marschner and Dell, 1994; Suzuki et al., 2001).
Although higher concentrations of 54Mn are observed in the PFP compared to the matrix in the field experiment and Mn is not transported by arbuscular mycorrhizal fungi (Marschner and Dell, 1994; Suzuki et al., 2001), we do not observe any difference in 54Mn uptake in both groups of plants. This lack of difference can be related to the facts that the added radionuclide has been diluted in a very large amount of stable Mn present in the soil, and that Mn, being a micronutrient, is taken up in large quantities by the entire root system (i.e., both from the 54Mn enriched and from the non-enriched matrix zones). We assume that much larger radionuclide applications would have been needed to detect a difference between both groups of plants.
The similar uptake of 65Zn and the similar specific activity of Zn between plants grown in field and greenhouse conditions are not surprising although higher concentrations of 65Zn were observed in the PFP in the field. As in the case of Mn, the entire root system of maize (whether located in the 65Zn enriched or in the non-enriched zones) takes up large quantities of Zn from the soil, resulting in a similar Zn and 65Zn uptake in both groups of plants. Furthermore, arbuscular mycorrhizal fungi are able to take up and transport significant amounts of Zn to the roots (Bürkert and Robson, 1994). Since the fungal hyphae can transport 65Zn from distances of up to 10 cm from the roots (Jansa et al., 2003) and, since hyphae having a diameter of a few µm can penetrate and explore very fine pores, it is possible that they explored the entire surface horizon in the field and the entire soil volume in the pot, hence contributing to the 65Zn uptake by maize.
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CONCLUSIONS
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These results show that the TF concept is inadequate to describe the soil-to-plant transfer of surface-applied radionuclide in field soil presenting active preferential flow paths. In this context "inadequate" means that it leads to a systematic underestimation of the uptake of some radionuclides. The uptake of 54Mn and 65Zn by plants grown in the greenhouse was representative of that measured under field conditions because they are strongly diluted in the large pool of stable element in the soil and being micronutrients are taken up by the whole root system both from the radionuclide enriched zone (PFP) and non-enriched zones (soil matrix). Contrarily, the uptake of 134Cs or 57Co was twofold higher in plants grown in the field experiment. This is due to a more efficient uptake of 134Cs and 57Co from soil zones enriched in these nuclides. In the case of Cs this could be related to different K nutrition patterns in the field and in the greenhouse. Finally, as plants accumulate Cs and Co at very low concentrations and as these elements are present at very low concentrations in the soil, the accumulation of 134Cs and 57Co in specific zones of the soil causes a relatively strong increase in the specific activity of these elements in these areas and their exploration by roots results in large variations in shoot specific activity. On the opposite, a much higher rate of radionuclide addition would be necessary to modify the shoot specific activity of an element (as Mn or Zn) taken up in high quantities by the plant and present at high concentrations in the soil.
However, our results are the product of a short-term field experiment performed in one soil type and with one crop, thus additional experiments on reproducibility of data for a range of soil types and plant species are needed. Furthermore, it is clear that macroporous flow is not an ever-occurring phenomenon but certain soil physical (saturated hydraulic conductivity, water content, and surface contributing area) and meteorological conditions (intensity and amount of rainfall) are necessary to have it happen (Weiler and Naef, 2003).
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ACKNOWLEDGMENTS
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We thank A. Mollier (INRA Bordeaux) and B. Kulli (ITOe, ETH Zurich) for their help in image processing, E. Grieder and J. Beer (EAWAG, Dübendorf) for the
-spectrometry measurements, K. Bartmettler (ITOe, ETH Zurich) for the inductively coupled plasmamass spectrometry (ICPMS) analysis, and J. Leuenberger (ITOe, ETH Zurich) for the aggregate stability tests and help in the field. We also thank A. Fehlmann for the soil chemical and physical analyses. T. Centofanti and R. Penfield acknowledge the financial support of the Swiss National Foundation for Scientific Research (Project no. 3152-064135.00) and the Swiss Federal Nuclear Safety Inspectorate (HSK, Villigen-HSK, Switzerland).
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