Journal of Environmental Quality 31:904-909 (2002)
© 2002 American Society of Agronomy, Crop Science Society of America, and Soil Science Society of America
TECHNICAL REPORTS
Plant and Environment Interactions
Uptake of Cesium-137 and Strontium-90 from Contaminated Soil by Three Plant Species; Application to Phytoremediation
Mark Fuhrmann*,a,
Mitch M. Lasatb,
Stephen D. Ebbsb,
Leon V. Kochianb and
Jay Cornishc
a Environmental and Waste Technology Group, Brookhaven National Lab., Building 830, Upton, NY 11973-5000
b U.S. Plant, Soil and Nutrition Lab., USDA-ARS, Cornell Univ., Ithaca, NY 14853
c MSE Technology Applications, P.O. Box 4078, Butte, MT 59702
* Corresponding author (fuhrmann{at}bnl.gov)
Received for publication September 30, 1999.
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ABSTRACT
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A field test was conducted to determine the ability of three plant species to extract 137Cs and 90Sr from contaminated soil. Redroot pigweed (Amaranthus retroflexus L.), Indian mustard [Brassica juncea (L.) Czern.], and tepary bean (Phaseolus acutifolius A. Gray) were planted in a series of spatially randomized cells in soil that was contaminated in the 1950s and 1960s. We examined the potential for phytoextraction of 90Sr and 137Cs by these three species. Concentration ratios (CR) for 137Cs for redroot pigweed, Indian mustard, and tepary bean were 2.58, 0.46, and 0.17, respectively. For 90Sr they were substantially higher: 6.5, 8.2, and 15.2, respectively. The greatest accumulation of both radionuclides was obtained with redroot pigweed, even though its CR for 90Sr was the lowest, because of its relatively large biomass. There was a linear relationship between the 137Cs concentration in plants and its concentration in soil only for redroot pigweed. Uptake of 90Sr exhibits no relationship to 90Sr concentrations in the soil. Estimates of time required for removal of 50% of the two contaminants, assuming two crops of redroot pigweed per year, are 7 yr for 90Sr and 18 yr for 137Cs.
Abbreviations: CR, concentration ratio
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INTRODUCTION
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PHYTOEXTRACTION, THE USE OF plants to remove contaminants from soil by accumulation of contaminants in plant tissue, is a promising cleanup technology for a variety of metal-containing soils (Kumar et al., 1995; Cunningham et al., 1997). However, phytoextraction of high specific activity radionuclides such as 137Cs or 90Sr is a challenge because of the very low molar concentrations of the radionuclide in soil (typically in the order of 10-12 mol/kg) compared with much higher concentrations of stable elements naturally present in soil. In addition, plant uptake of 137Cs and 90Sr can be inhibited by competition with K (Shaw and Bell, 1991) and Ca (Menzel, 1965), respectively. Further, the prospect of phytoextraction of 137Cs from contaminated soil is minimized because sorption of Cs into interlayer spaces on mica–illite minerals appears to be highly specific and poorly reversible (Tamura and Jacobs, 1960; Comans et al., 1991).
A field experiment was conducted in 1996 at Brookhaven National Laboratory to assess the ability of selected plant species to extract 137Cs and 90Sr from contaminated soil. Although immobilization within micaceous minerals can significantly reduce bioavailablity of 137Cs for plant uptake, the relatively simple mineralogy (mostly quartz with only a trace of micaceous minerals) of soil on Long Island (New York) suggested that phytoextraction of 137Cs might be effective. In an earlier paper, we reported on the uptake of 137Cs by three plant species (redroot pigweed, Indian mustard, and tepary bean), and the effect of ammonium nitrate solutions on desorbing 137Cs from the soil to enhance uptake in the plants (Lasat et al., 1998). Tepary bean is a high-biomass-producing legume that can grow in a number of different environments and climate regimes. It tends to concentrate Ca to higher concentrations than many other crop plants (Christenson, 1982), implying that it may be exceptional in its ability to accumulate 90Sr. Indian mustard was tested because it has been used extensively in phytoremediation of metals, especially lead and uranium (Salt et al., 1995; Blaylock et al., 1997), but had not been tested with radionuclides. Redroot pigweed was tested because of its high biomass and because earlier, unpublished work had suggested that it might be useful for uptake of metals. In this paper, we investigate the potential for phytoextraction of 90Sr and 137Cs by plants grown in field cells of radionuclide-contaminated soil.
A considerable body of information exists on the uptake of 137Cs and 90Sr radionuclides into plants. Much of it originates in the health physics literature, which reports the transfer of radionuclides from nuclear weapons tests, through the food chain, to humans. The effectiveness of contaminant transfer from soil into plants is quantified by the concentration ratio (CR), which is the concentration of the element of interest in the dried plant material divided by its concentration in the dried soil. Typical CR values for many elements have been compiled by Wang et al. (1993). For example, for root vegetables, grains, and fruit, values for 137Cs are 0.019 (Ng et al., 1992), 0.017 (Napier et al., 1988), 0.03 (Baes et al., 1984), and 0.098 (Kennedy and Strange, 1992). Slightly greater values of CR are observed for 90Sr, being 1.4 (Ng et al., 1992), 0.37 (Napier et al., 1988), 0.25 (Baes et al., 1984), and 0.4 (Kennedy and Strange, 1992). For leafy vegetables, these values remain about the same for 137Cs and are slightly higher for 90Sr, ranging between 1.3 and 2.5 (Baes et al., 1984). These low values mean that there is generally little uptake of 137Cs into plant tissues and slightly greater uptake of 90Sr, especially by leafy vegetables.
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MATERIALS AND METHODS
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Soil at the Hazardous Waste Management Facility site at Brookhaven National Laboratory is contaminated with 137Cs ranging from background (less than 0.02 kBq/kg) to about 110 kBq/kg, mostly in the upper layer. The soil contains 90Sr with activities ranging from 0.02 to 1.4 kBq/kg and extending to a depth of several meters. The average activity of 90Sr in the upper 20 cm of the Hazardous Waste Management Facility phytoremediation test area was 0.06 kBq/kg compared with 11.8 kBq/kg for 137Cs. Contamination occurred in the 1950s and 1960s during waste processing and equipment cleaning. At that time the concentrations of the two fission products (137Cs and 90Sr) at the soil surface were about equal. The values of the partition coefficients (Kd, the concentration of a species of interest on the solid phase divided by the concentration of that species in the liquid phase, at steady state) are 7 L/kg for 90Sr in local soil, compared with 190 L/kg for 137Cs (Fuhrmann, unpublished data, 1999). The lower the Kd, the less sorption takes place. Thus, much of the 137Cs has remained at the surface, while the 90Sr has migrated into the soil column, carried by rainwater.
The soil in the test area is coarse-loamy, mixed, mesic typic Dystrochrept. It is generally well drained and formed as a mantle of sandy loam over thick deposits of sand and gravel. Mineralogy is dominated by quartz, with percentages typically around 90%. Rock fragments range from 2 to 23% with higher percentages in gravel fractions; micaceous minerals represent no more than a few percent (Faust, 1963). The mass of soil in a square meter was calculated for a depth of 15 cm, and the bulk density was taken to be 1.6 kg/m3.
In the summer of 1996 the soil was sprayed with an herbicide (Roundup; Monsanto, San Ramon, CA), rototilled, limed (0.3 kg/m2), and fertilized (N–P–K 16–16–16, 0.068 kg/m2), and 36 randomized cells were set up, measuring 0.5 m on a side. Twelve cells were directly seeded with Indian mustard while each of the remaining cells received 15 transplants (14 d old) of either redroot pigweed or tepary bean. The plot was irrigated as necessary. Once a week for three weeks just prior to harvest, each cell received 4 L of either water or a 0.1 or 0.2 M solution of ammonium nitrate. The intent was to determine if the ammonium ion would displace enough 137Cs from the soil to solution to stimulate uptake of 137Cs in the plants, as had been observed in greenhouse studies (Lasat et al., 1997). Plants were harvested 15 wk after planting, dried, and analyzed for 137Cs and 90Sr. In addition, native plants in the experimental area were sampled and analyzed.
Individual plant and soil samples were weighed, dried, reweighed, and then crushed. These samples were analyzed by gamma spectroscopy for 137Cs at the 661 keV line using a high-purity Ge gamma-ray detector. A river sediment standard (National Institute of Standards and Technology Standard Reference Material [SRM] 4350B) and a secondary vegetation standard (DOE-EML-QAP44 9603 from the Environmental Measurements Laboratory in New York) were used. Samples to be analyzed for 90Sr were dried, ground to a powder, and then sent to the Institute for Power Engineering Problems in Minsk, Belarus. Because of insufficient sample weights not all samples were sent for 90Sr analysis. Analysis for 90Sr was based on a standard radiochemical method (Chieco et al., 1992). Soil samples were ashed with 6 M HCl and washed in ammonium solution at pH = 8, and the Sr was extracted as the carbonate. Plant samples were also ashed with HCl, oxalates were converted to oxides, and any other radionuclides were removed. Yttrium was extracted as the oxalate and counted after 14 d ingrowth. The chemical yield of Sr was determined by atomic absorption spectrometry and the yield of Y determined gravimetrically. Samples were counted with a Canberra (Meriden, CT) 2400 beta spectrometer with an efficiency of 0.108 and a background of 7.3 counts per minute. The summed error of measurements is estimated to be less than 15%.
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RESULTS AND DISCUSSION
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Cesium-137 and Strontium-90 Uptake in Plants
Accumulation of 137Cs in shoots is shown in Fig. 1
. We have plotted the concentration of the radionuclide in the dried plant against its concentration in soil. The CR value is then estimated by the slope of the regression line. For 137Cs, redroot pigweed provided the greatest uptake with an average CR of 3.03 and a relatively good linear relationship between concentrations of 137Cs in the soil and the plant (R2 = 0.86) (n = 12). For tepary bean the CR was 0.22 with a linear correlation of R2 = 0.72 (n = 11). For Indian mustard the concentration in the shoots was apparently unchanged as 137Cs in the soil increased. Consequently, the CR was determined by averaging 11 measurements, giving a CR value of 0.46. The CR values obtained by linear regression are similar to those obtained in Table 1 by averaging the bulk estimates of 137Cs concentrations in the soil and plants.
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Fig. 1. Cesium-137 concentrations in plants relative to its concentrations in soil at the phytoremediation test plot at the Hazardous Waste Management Facility. The slope of the regression line is an estimation of concentration ratio (CR).
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Lasat et al. (1997), in earlier greenhouse work with the same soil, reported enhanced uptake of 137Cs by plants grown in an ammonium nitrate–treated soil. To examine this effect in the field, some of the cells were treated with ammonium nitrate solutions as described earlier. As shown in Fig. 2
, and as we have discussed elsewhere (Lasat et al., 1998), there was no increase in uptake of 137Cs in shoots of plants grown in field cells as a result of ammonium addition. The difference between the greenhouse result and that of the field work is suspected to be related to the short residence time of the solution in the open system of the field experiment.
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Fig. 2. Effect of addition of ammonium nitrate solution on concentration ratios of 137Cs in the three plant species tested at the Hazardous Waste Management Facility.
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Several other plant species from this experimental site were analyzed for 137Cs. Marigolds (Tagetes spp.) were grown around the perimeter of the site to help repel insect pests. The 137Cs content of four samples of these plants averaged 17.7 kBq/kg with an average CR of 2.58. Sassafras [Sassafras albidum (Nutt.) Nees] grows wild on this site. The concentration of 137Cs in its leaves was 0.56 kBq/kg, while the 90Sr concentration was 1.26 kBq/kg. Goldenrod (Solidago spp.) accumulated 137Cs and 90Sr to activities of 4.7 and 1.2 kBq/kg, respectively. A native grass contained 2.6 kBq/kg of 137Cs.
Accumulations of 90Sr, in shoots of Indian mustard, redroot pigweed, and tepary bean, are shown in Fig. 3
. There is no apparent linear relationship between the concentrations of 90Sr in the plants and in the associated soil. For individual Indian mustard plants, CR values ranged from 1.4 to 21.5, averaging 12.2 (n = 6) (Table 2). Values of CR for redroot pigweed ranged from 0.2 to 13.2, averaging 5.6 (n = 7). For tepary bean, the range of CR was 6.3 to 22 with an average CR of 15.0 (n = 7).
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Fig. 3. Strontium-90 concentration in plants relative to its concentration in soil at the Hazardous Waste Management Facility.
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Figure 4
is a histogram of CR values for both 90Sr and 137Cs in the same samples. All three species had greater CR values for 90Sr than they did for 137Cs. Tepary bean had greater CR values for 90Sr than did the other plants tested. In contrast, redroot pigweed had the greatest CR values for 137Cs.
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Fig. 4. Concentration ratios of 90Sr and 137Cs for the three plant species tested. Each bar represents a measurement of an individual plant and soil set.
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The relationship between the concentrations of 137Cs in redroot pigweed and its concentrations in soil is linear. This relationship for tepary bean is less clear. For Indian mustard, accumulation of 137Cs was unchanged as the concentration in the soil increased. This relationship is different for 90Sr, with the data indicating no systematic trend for any of the species tested. We see two possible reasons for this. The first is that plants may employ different mechanisms for uptake of Cs (an analogue of K) and Sr (an analogue of Ca). Differences in the behavior of Cs and Sr in plants are apparent in a recent study of the concentrations of radionuclides of these elements in different organs of bracken fern [Pteridium aquilinum (L.) Kuhn] over the course of a year (Tyson et al., 1999a,b). Cesium-134 was readily mobile within the plant and was present in relatively high concentrations in young and growing tissue as compared with older tissue. In contrast, 85Sr, behaving as an analog of Ca, concentrated in woody and structural tissues of bracken fern and accumulated in older and dead material.
The other possibility is based on the nature of the retention of 137Cs on soil compared with 90Sr. Cesium is strongly held on micaceous minerals. In fact, in separate experiments by Lasat et al. (1997) and Fuhrmann et al. (1996) on soil from this site, relatively little 137Cs could be eluted from the soil by a variety of solutions. Even concentrated HCl and HNO3 moved only 38% of the 137Cs into solution, while NH4F and several solution strengths of NH4 Cl eluted about 10%. While no elution experiments were analyzed for 90Sr, as discussed earlier, the 90Sr does migrate with addition of rainwater. In this soil it is most likely associated with iron oxide coatings on minerals.
Application to Phytoremediation
Capacity of plants to remove contaminants from the soil is a function of biomass per unit area and concentration of the contaminant in the plants. These parameters and the total fraction of 137Cs removed from the soil are shown in Table 1. These results each represent averages of six or seven cells. The fractional uptake in plants was calculated by dividing the amount of 137Cs in the crop by the amount of 137Cs in the soil of the same cells. As shown in Table 1, tepary bean had the lowest concentration of 137Cs and the lowest CR. Redroot pigweed had the highest concentration, CR, and biomass production, and removed 2.1% of the 137Cs present in the surface soil of the cells in which it was grown. Redroot pigweed provided the greatest uptake of both 137Cs and 90Sr because of its relative high concentrations and greater biomass production.
Fractional uptake of 90Sr by the three plant species is greater than that of 137Cs, as would be expected given the capacity of the soil to retain Cs. For Indian mustard, 0.7% of the 90Sr present in the soil at the start of the experiment was incorporated into the crop. The relatively low shoot biomass was an important factor limiting removal of 90Sr. Redroot pigweed provided a much greater yield and somewhat higher concentrations of 90Sr, accumulating 4.5%. Tepary bean had the greatest concentration of 90Sr, averaging 0.79 kBq/kg, but its low biomass production resulted in uptake of 3.1%. Application of ammonium nitrate solutions to the soil before harvest had no effect on uptake of 90Sr.
Using the data generated in this work we have estimated the time required to reduce the level of contamination in the soil at the experimental site. We have assumed that the top 15 cm (the plowed layer) of the soil will be remediated, that the CR and biomass produced is constant over time, and that redroot pigweed is used. We have also assumed that contaminants are removed from the soil according to the following equation (Tuin and Tels, 1990):
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where Ct is the concentration of the contaminant after phytoremediation for time t, Co is the initial concentration of the contaminant, k is (plant mass per year per square meter/soil mass) x concentration ratio, and t is the time of remediation in years.
As shown in Fig. 5
, the model results indicate that 50% of the 90Sr will be removed in about 7 yr. Approximately 18 yr are needed to remove 50% of the 137Cs.
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Fig. 5. The fraction of 137Cs and 90Sr remaining in soil as a function of time, not accounting for radioactive decay. These curves are based on the concentration ratio (CR) and mass of redroot pigweed determined in this work.
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It is not known if this model is appropriate to estimate phytoextraction of radionuclides from soils. It is possible that the initial CR value is high because of a limited reservoir of contaminant that is bioavailable. In this case removal of that contaminant will be a step function that decreases. Moreover, from the data presented it appears that the concentrations of 137Cs and 90Sr in plants have very different relationships to their respective concentrations in the soil. This implies that different models (rather than simply different values for CR) may be needed for each contaminant. It may be appropriate to estimate concentrations of contaminants in the aqueous phase through the use of geochemical speciation and sorption codes and then use those estimates to help predict uptake in plants.
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ACKNOWLEDGMENTS
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This work was funded by the U.S. Department of Energy, Federal Energy Technology Center, under Contract no. DE-AC22-p6W96405 to MSE Technology Applications. The authors thank all those who helped in the field work: Bhavesh Patel, Anna Bou, Carlee Beecher, Huan Zhou, Teresa Baker, Paul Lageraan, and Gary Stoner. We also thank Gail Penny and James Brower for use of their site and Mel Cowgill for his comments.
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ABSTRACT
INTRODUCTION
