Environ. Sci. Technol. 1999, 33, 2752-2757
High Plant Uptake of Radiocesium from Organic Soils Due to Cs Mobility and Low Soil K Content A . L . S A N C H E Z , * ,† S . M . W R I G H T , † E. SMOLDERS,‡ C. NAYLOR,† P. A. STEVENS,§ V. H. KENNEDY,† B. A. DODD,† D. L. SINGLETON,† AND C. L. BARNETT† Institute of Terrestrial Ecology, Merlewood Research Station, Grange-over-Sands, Cumbria LA11 6JU, U.K., Laboratory of Soil Fertility and Soil Biology, Department of Land Management, K. U. Leuven, K. Mercierlaan 92, B-3001 Heverlee, Belgium, and Institute of Terrestrial Ecology, Bangor Research Unit, University of Wales, Bangor, Gwynedd LL57 2UP, U.K.
Post-Chernobyl experience has demonstrated that persistently high plant transfer of 137Cs occurs from organic soils in upland and seminatural ecosystems. The soil properties influencing this transfer have been known for some time but have not been quantified. A pot experiment was conducted using 23 soils collected from selected areas of Great Britain, which were spiked with 134Cs, and Agrostis capillaris grown for 19-45 days. The plant-tosoil 134Cs concentration ratio (CR) varied from 0.06 to 44; log CR positively correlated to soil organic matter content (R 2 ) 0.84), and CR values were highest for soils with low distribution coefficients (Kd) of 134Cs. Soils with high organic matter contents and high concentrations of NH4+ in solution showed high 134Cs mobility (low Kd). The plantto-soil solution 134Cs ratio decreased sharply with increasing soil solution K+. A two parameter linear model, used to predict log CR from soil solution K+ and Kd, explained 94% of the variability in CR values. In conclusion, the high transfer of 134Cs in organic soils is related to both the high 134Cs mobility (low clay content and high NH + concentra4 tions) and low K availability.
Introduction Pre- and post-Chernobyl studies have shown that soil-toplant concentration ratios (CR) for radiocesium (hereafter referred to as Cs) are consistently higher for plant species growing on peaty (highly organic) soils compared to mineral soils. In field sites established within 50 km of the Chernobyl nuclear power plant following the 1986 accident, the 137Cs transfer factors for grass species growing on peaty swamp soils were around 4-7 times higher than for those growing on other soil types (1, 2). Various crop species grown on peat soils show up to an order of magnitude higher CR values than for loam and sand (3). The persistently high uptake of Cs into vegetation growing on upland pastures of Great Britain have resulted in high Cs activity concentrations in sheep grazing these areas (4, 5). * Corresponding author phone: +44 15395 32264; fax: +44 15395 34705; e-mail:
[email protected]. † Institute of Terrestrial Ecology, Merlewood Research Station. ‡ Laboratory of Soil Fertility and Soil Biology. § Institute of Terrestrial Ecology, Bangor Research Unit. 2752
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It is important to understand the mechanisms controlling Cs behavior in upland and other natural and seminatural ecosystems, as soils in these areas have been found to have longer ecological half-lives for Cs than improved agricultural soils, and human food products are obtained from these areas (6). Soil organic matter is known to have a strong influence, particularly where the organic matter content exceeds 50% (7-9). The Cs adsorbed on the organic fraction is readily exchangeable and is highly available for plant uptake (8, 10-12). Most of the data reported for organic soils are based on site observations with limited quantitative information on the variations of CR with soil properties. This paper presents the results of a greenhouse pot experiment conducted to identify and quantify the soil factors that may explain the high uptake of Cs by Agrostis capillaris (bent-grass) from organic soils. This species is commonly found in unimproved acidic grasslands and grazed by sheep (13, 14) and was expected to grow adequately on organic soils. The experimental approach followed that used by Smolders et al. (15) investigating the availability of 137Cs for ryegrass (Lolium perenne) uptake from various mineral soil types in Belgium.
Materials and Methods Soil Samples and Soil Characteristics. Twenty-three soils were collected from selected areas of north and mid-Wales, northwest England, and Scotland during 1996-1997 (Table 1). The soils were taken from the top 10 cm to avoid the mineral materials which occur in the deeper layers. Vegetation was removed, and the soil was then mixed thoroughly for air-drying (5-fold) reductions in K+ and NH4+ concentrations. Increasing concentrations of NH4+ in soil solution reduced the Kd of 134Cs (R 2 ) 0.37 for the log Kd - log mNH4 relationship, n ) 23, Table 3). This is consistent with previous results (e.g., refs 21 and 29), which have shown that NH4+ ions, having higher selectivity than K+ on Cs sorption sites, had the effect of mobilizing Cs+ into solution. The mean CR values varied between 0.06 (S19) to 44 (S4) (Table 2), with good reproducibility; maximum SD was 35% of the mean for S8. In general, the low CR values (CR < 1) were obtained for soils with relatively low organic matter contents; conversely, the high CR values were for those soils with relatively high (>70%) organic matter contents. The histosols (peat soils) had higher CR values (median CR 21.43) than the dystric gleysols (median CR 1.20) (Table 2). The CR
TABLE 2. Grass Yields, Soil-to-Plant Concentration Ratio (CR), and Soil-to-Soil Solution Distribution Coefficient (Kd) for Concentrations in Soil Solutiona for K+ and NH4+ b soil code
and
K+ (mM)
NH4+ (mM)
Histosols (Peats) 36.2 (1.8) 120 (30) 44 (4) 110 (20) 6.4 (0.8) 290 (50) 9.9 (1.4) 100 (10) 27.9 (1.8) 220 (20) 41(3) 67 (10) 28.5 (1.4) 59 (5) 3.4 (0.5) 6900 (5900) 21.4 (2.3) 43 (4) 0.09 (0.01) 109000 (57000) 0.42 (0.05) 26000 (20000) 3.2 (0.2) 290 (40) 22.9 (1.5) 58 (16) 21.4
0.07 (0.02) 0.05 (0.01) 0.10 (0.02) 0.22 (0.02) 0.04 (0.03) 0.07 (0.02) 0.051 (0.003) 0.06 (0.01) 0.16 (0.01) 0.03 (0.01) 0.08 (0.02) 0.39 (0.14) 0.10 (0.02)
0.30 (0.18) 0.35 (0.04) 0.78 (0.13) 0.49 (0.10) 0.23 (0.13) 0.55 (0.15) 1.24 (0.18) 1.05 (0.59) 2.02 (0.32) 0.005 (0.002) 0.21 (0.16) 3.79 (0.62) 1.40 (0.34)
0.31 (0.09) 0.25 (0.03) 0.27 (0.10) 0.34 (0.05) 0.67 (0.05) 0.39 (0.03) 0.43 (0.06) 0.57 (0.06) Median CR
Dystric Gleysols 0.95 (0.34) 16000 (6000) 1.44 (0.05) 1350 (150) 0.06 (0.01) 2800 (700) 0.49 (0.03) 1570 (20) 4.6 (0.4) 260 (30) 0.74 (0.11) 14000 (9000) 7.6 (1.3) 81 (2) 3.0 (0.4) 220 (30) 1.44
0.11 (0.05) 0.24 (0.01) 1.65 (0.23) 0.48 (0.06) 0.28 (0.00) 0.09 (0.04) 0.38 (0.01) 0.41 (0.04)
0.02 (0.01) 3.71 (0.38) 0.01 (0.01) 4.69 (049) 2.07 (0.00) 0.06 (0.05) 2.57 (0.07) 1.00 (0.07)
1.74 (0.10) 0.43 (0.13)
Brown Soils 0.21 (0.02) 53000 (5000) 0.16 (0.03) 22000 (2800)
0.14 (0.04) 0.17 (0.01)
0.78 (0.20) 0.007 (0.003)
0.13 1.74 0.32
0.06 44.08 3.41
0.03 1.65 0.11
0.01 4.69 0.78
n
grass yield (g pot-1)
S1 S4 S6 S7 S9 S10 S11 S14 S18 S24 S25 S28 S30
5 5 3 5 4 5 3 5 3 3 3 3 5
0.31 (0.15) 0.26 (0.06) 0.28 (0.05) 0.13 (0.09) 0.49 (0.02) 0.35 (0.16) 0.20 (0.08) 0.52 (0.05) 0.17 (0.07) 0.23 (0.06) 0.27 (0.01) 0.47 (0.06) 0.32 (0.05) Median CR
S8 S17 S19 S20 S22 S23 S26 S27
3 3 3 3 3 3 3 3
S21 S29
3 3
min. max. median
134Cs
Kd
CR
All 23 Soils 43 109033 292
a Soil solution data based on observations after plant growth. b The data are grouped into the major FAO soil types used in the study. All data are means and standard deviations (in brackets) for n replicates.
TABLE 3. Pearson Correlation Coefficients (R) Showing the Variation (and Their Significance) in 134Cs Plant-to-Soil Concentration Ratio (CR) and Soil-to-Solution Distribution Coefficient (Kd) after Plant Growth, with Selected Parameters % organic matter pH % clay Kd (before) log Kd (before) mM K (before) log mM K (before) mM NH4 (before) log mM NH4 (before) Kd (after) log Kd (after) mM K (after) log mM K (after) mM NH4 (after) log mM NH4 (after) a
log CR
log Kd (after)
0.919c -0.773c -0.600b -0.544b -0.897c -0.477a -0.426a 0.058 0.495a -0.604b -0.870c -0.437a -0.367 0.078 0.551b
-0.831c 0.651c 0.462a 0.633b -0.958c 0.066 0.034 -0.237 -0.55b
0.025 -0.081 -0.284 -0.61b
p < 0.05. b p < 0.01. c p < 0.001.
values found here were much higher (overall median value 3.4) than those found for ryegrass (15) in a similar pot trial using fertilized mineral soils (median value 0.06). For evaluation of the experimental results, we used the soil solution data after plant growth to unravel the source of variability of 134Cs availability. This approach is similar to that of Smolders et al. (15), which is based on the hypothesis that Cs+ is taken up from soil solution. Plant uptake is
described as a series of two reactions: 134
Kd
CF
Cssoil 798 134Cssoil solution 798 134Csplant
(1)
The first reaction (sorption-desorption of 134Cs) is assumed to be an instantaneous equilibrium reaction and quantified in terms of the Kd. The reaction further assumes that all 134Cs is reversibly sorbed and ignores changes of Kd with time during plant growth. In organic soils, the fraction of Cs adsorbed on organic sites constitute a labile, exchangeable pool (e.g., refs 11, 12, and 20); thus, we assume that although decreases in 134Cs activities in soil solution occurred in the time span of the experiment (Figure 1c), this would have been replenished readily from the organic pool. Furthermore, the presence of NH4+ would have the effect of maintaining Cs+ in soil solution (29). The second reaction describes plant radiocesium uptake from soil solution and is quantified using the concentration factor, CF (ratio of 134Cs activity concentration in plant biomass (shoot only) to that in soil solution). From the serial reaction (eq 1), the concentration ratio, CR (ratio of 134Cs activity concentration in plant to that in the soil), can be written as
CR ) (134Csplant )/(134Cssoil) ) CF/Kd
(2)
A logarithmic transformation yields
log CR ) log CF - log Kd
(3)
Equation 3 shows that if the CF is independent of soil type, VOL. 33, NO. 16, 1999 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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FIGURE 2. Log-log plot of the plant-to-soil concentration ratio CR versus the distribution coefficient Kd for 134Cs.
FIGURE 4. Model fit showing predicted versus observed concentration ratio CR for 134Cs. Model predictions for log CR based on soil solution K concentration and distribution coefficient Kd (see text for discussion). net effect is that it mobilizes 134Cs+ into soil solution, rendering Cs+ more available for root uptake. The CF values found here are generally much higher (median: 1900) than those for ryegrass (15) grown in mineral soils from intensive grasslands (median: 150). This difference is mainly due to higher soil solution K+ in intensive grassland soils than in unimproved organic soils (median solution K+ 1.0 and 0.1 mM, respectively). Thus, the high availability of radiocesium in unimproved organic soils is due to high Cs mobility (i.e., low Kd values of the soil and substantial NH4+ concentrations) combined with low K+ concentrations, favoring the uptake of radiocesium from solution. The significant correlation shown in Figure 3a effectively means that K availability is an additional factor controlling 134Cs uptake from soil. Therefore, eq 3 was converted to the model
log CR ) (a - b*log mK) - log Kd
FIGURE 3. Log-log plot of the plant-to-soil solution concentration factor CF for 134Cs versus the K+ and NH4+ concentrations in soil solution after plant growth. log CR should be negatively correlated with log Kd with a slope of -1 (15). The regression line for our experimental data (Figure 2) showed a negative correlation between log CR and log Kd (slope ) -0.72 ( 0.05, R 2 ) 0.76, n ) 23). The CF values, however, were not independent of soil type (from Table 2, CF ) CR*Kd), varying from 167 (S19) to 23 200 (S14) and decreasing with increasing soil solution K+ (Figure 3a). A similar trend was found for the 137Cs CF of ryegrass grown in different mineral soils (15). This effect is most likely related to K+ competing for radiocesium uptake as has been found in several solution culture experiments (30, 31). Recently, 137Cs uptake by A. capillaris was measured in solution culture at varying K supply (32). The shoot to solution CF decreased from 4700 mL g-1 at 0.025 mM K+ to 220 mL g-1 at 1.0 mM K+. Both this trend and the absolute values of CF agree with those found here (Figure 3a). The CF values were largely unaffected by the solution NH4+ concentration (R 2 ) 0.10, Figure 3b), suggesting that NH4+ ions did not compete with 134Cs plant uptake. Similar conclusions have been drawn from root uptake studies (29, 30), where NH4+ competes far more weakly than K+ with the Cs+ uptake process of wheat. Thus, NH4+ in solution competes more effectively for mineral sorption sites than it does for plant uptake relative to Cs+; as mentioned previously, the 2756
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(4)
In the above equation, log CF in eq 3 is substituted by the term (a - b*log mK), which can be derived from the plot shown in Figure 3a. The terms a and b are the linear regression coefficients of the line in Figure 3a, and mK is the soil solution K+ concentration in mM. The coefficients were a ) 2.54 ( 0.16 and b ) -0.99 ( 0.17. The model based on eq 4 explains 94% of the variation of log CR values (Figure 4). Predicting 134Cs availability from soil solution composition is useful to test mechanistic models but is not practical for field predictions. Soil solution sampling is time-consuming, and the solution Cs activities are often far below detection limits. The data from the pot experiment provided empirical correlations between CR values and readily measurable soil parameters (Table 3) which are being used in a semimechanistic model to predict the behavior of Cs in European soils (33). The log CR values showed a significant positive correlation with the organic matter content of the soils (R 2 ) 0.84, n ) 23). In conclusion, this study demonstrated that the high CR values of 134Cs in organic soils is related to both the high 134Cs mobility (related to low clay content and high NH4+ concentrations) and low K availability and that it is possible to quantify these relationships to obtain parameters that can be used to predict Cs plant uptake.
Acknowledgments We thank ITE colleagues B. Howard, N. Beresford, R. Creamer, M. Hornung, and A. Scott for their help with this study. This work was jointly funded by the European Commission through the SAVE project (Contract F14P-CT-950015), the Natural Environment Research Council, and the U.K. Ministry of Agriculture, Fisheries and Food (Contract RP0244).
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Received for review January 20, 1999. Revised manuscript received May 19, 1999. Accepted June 1, 1999. ES990058H
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