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TECHNICAL REPORTS
Ecosystem Restoration

Reduction of Arsenic Uptake by Lettuce with Ferrous Sulfate Applied to Contaminated Soil

Department of Soil Science, The Univ. of Reading, Whiteknights, P.O. Box 233, Reading, RG6 6DW, UK

^* Corresponding author (g.p.warren{at}reading.ac.uk)

Received for publication October 22, 2001.

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION CONCLUSIONS REFERENCES

 
Soil contamination by arsenic (As) presents a hazard in many countries and there is a need for techniques to minimize As uptake by plants. A proposed in situ remediation method was tested by growing lettuce (Lactuca sativa L. cv. Kermit) in a greenhouse pot experiment on soil that contained 577 mg As kg^-1, taken from a former As smelter site. All combinations of iron (Fe) oxides, at concentrations of 0.00, 0.22, 0.54, and 1.09% (w/w), and lime, at concentrations of 0.00, 0.27, 0.68, and 1.36% (w/w), were tested in a factorial design. To create the treatments, field-moist soil, commercial-grade FeSO₄, and ground agricultural lime were mixed and stored for one week, allowing Fe oxides to precipitate. Iron oxides gave highly significant (P < 0.001) reductions in lettuce As concentrations, down to 11% of the lettuce As concentration for untreated soil. For the Fe oxides and lime treatment combinations where soil pH was maintained nearly constant, the lettuce As concentration declined in an exponential relationship with increasing FeSO₄ application rate and lettuce yield was almost unchanged. Iron oxides applied at a concentration of 1.09% did not give significantly lower lettuce As concentrations than the 0.54% treatment. Simultaneous addition of lime with FeSO₄ was essential. Ferrous sulfate with insufficient lime lowered soil pH and caused mobilization of Al, Ba, Co, Cr, Cu, Fe, K, Mg, Mn, Na, Ni, Pb, Sr, and Zn. At the highest Fe oxide to lime ratios, Mn toxicity caused severe yield loss.

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION CONCLUSIONS REFERENCES

 
ARSENIC POSES serious health risks to humans and animals, and As-contaminated soils and sediments are major sources of contamination in the food chain and water supplies (Frankenberger, 2002). Hazardous inputs of As to soil come from some natural waters and man-made sources, which include mine spoils, emissions from the smelting of metal ores, glass and metal production, and the use of pesticides and timber preservatives. Unfortunately, there is a shortage of proven methods for lowering the risks caused by As contamination in soil.

Recent reviews of the forms and cycling of As in soils and waters (Smith et al., 1998; Inskeep et al., 2002) find that H₃AsO⁰₃, H₂AsO^-₄, and HAsO^2-₄ are the inorganic species that are thermodynamically stable in soil interstitial waters under realistic conditions for plant growth. In most aerobic soils, H₂AsO^-₄ is dominant. Speciation influences (i) sorption of soluble As on soil minerals, (ii) plant uptake (Asher and Reay, 1979), and (iii) toxicity, which generally follows the trend: As(III) > As(V) > organically combined As (Smith et al., 1998). The redox potential of the As(V)/As(III) couple falls within the dynamic range of values that may be observed in sediments, aquifers, and soils with fluctuating water contents (Inskeep et al., 2002). Flooding lowers the soil redox potential (Eh), reducing As(V) to the more-toxic As(III), and causing reductive dissolution of the Fe(III) minerals that sorb As strongly (McGeehan and Naylor, 1994). This increases As solubility in incubated soil (Deuel and Swoboda, 1972) and phytotoxicity to rice (Oryza sativa L.) (Marin et al., 1993).

Extraction and sorption studies show that As in soil is associated primarily with Fe oxides and hydroxides (Jacobs et al., 1970; Fassbender, 1974; Fordham and Norrish, 1983; Hale et al., 1997). Studies of Fe oxides show that they have high sorption capacities for As (Hingston et al., 1968; Matis et al., 1997; Garcia-Sanchez et al., 1999). Both As(III) and As(V) are held to goethite (FeOOH) strongly by binuclear bridging complexes (Sun and Doner, 1996). The adsorption of As on variable-charge minerals such as Fe oxides is pH dependent and, for example, the sorption maximum for As(V) on goethite decreases with increasing pH (Hingston et al., 1968). This effect is also observed in soils with high contents of Fe oxides (Manful et al., 1989; Smith et al., 1999). In contrast, As(III) sorption shows a relatively slight pH dependence at pH values typical of soils (Inskeep et al., 2002). Thus, the soluble fraction of soil As depends on mineral components, redox status, and pH in a complex way.

One approach to the in situ remediation of soil contaminated with potentially toxic elements is the application of a sorptive mineral, intended to lower the soluble fraction of the element and thus reduce uptake by plants. Because of the strong sorption of As on Fe oxides, As can be removed from water with precipitated goethite (Matis et al., 1997), granular ferric oxide (Driehaus et al., 1998), and iron oxide–coated sand (Joshi and Chaudhuri, 1996), so Fe oxides could do the same for soil solution. Iron oxides applied to soil have been proposed as sorptive mineral amendments for the remediation of As contamination (Boisson et al., 1999; Garcia-Sanchez et al., 1999). Instead of adding bulk Fe oxides, they can be precipitated in situ by adding an Fe²⁺ salt, which should give Fe oxides with a high surface area and sorption capacity. In a laboratory study, FeSO₄ was applied to soil contaminated by effluents from a timber treatment plant, and the As in soil solution reduced from 3802 to 0.64 µg L^-1 (Moore et al., 2000), showing that FeSO₄ can reduce As solubility greatly. Leaching of As from contaminated soil has been successfully reduced by mixing the soil with FeSO₄ and Portland cement (5–20% soil mass) to coprecipitate Fe arsenates and so reduce As solubility (Voigt et al., 1996; Miller et al., 2000). However, this solidification treatment with cement makes the soil unsuitable for growing plants. Phytotoxic effects suffered by crops grown on soil with residues of lead arsenate insecticide could be corrected by applying FeSO₄ alone to the soil (Vandecaveye et al., 1936; Thompson and Batjer, 1950). However, there have been no recent bioassays of the effectiveness of Fe oxides or FeSO₄ in reducing As uptake by crops and probably none for contamination sources other than pesticides. The first objective of this work was to find out whether FeSO₄ added to soil could reduce the bioavailable fraction of soil As in a typical soil contaminated by mining activities.

The FeSO₄ applied to soil as a solid or in solution is oxidized quickly to Fe oxides, here represented as Fe₂O₃, although it is recognized that the Fe oxides are actually in a hydrated form. The transformation can be described by the following equation:

[1]

Sulfuric acid is liberated, so to offset acidification and keep the soil suitable for plants, lime (CaCO₃) was also added. Because of the dependence of As sorption on pH, an interaction between added FeSO₄ and lime seemed possible, so the second objective was to assess this potential interaction.

Soil composition, pH, and sorption capacity for As vary widely, so the effectiveness of remediation with FeSO₄ is likely to differ between locations. For the same reasons, it can be difficult to demonstrate unequivocally the efficacy of a remediation treatment in field trials. Therefore, a recently concluded research program included both (i) a pot experiment to assess the potential effect of the proposed remediation treatment under controlled environment conditions with a typical soil and crop and (ii) a set of field trials to assess the effects under field conditions with several different soils and crops. This paper reports the former results and a subsequent paper will report the field trials.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION CONCLUSIONS REFERENCES

 
Clay loam soil (0–10 cm depth) was taken from one plot of the companion field trial in Cornwall (UK), located at the site of an As smelter that had ceased operation about 80 yr ago. The soil was of the Denbigh series, which occurs extensively in Cornwall and on low hills in other parts of England and Wales, overlying solid or shattered rock (Findlay et al., 1984), slate in this case. This series is well-drained, suitable for pasture and arable production, and is classified as a typical brown earth (Typic Eutrochrept). Relevant properties were: pH in water (1:2.5) = 7.2, total C = 2.61%, total As = 577 mg kg^-1, and the percentages of sand, silt, and clay were 40.8, 37.5, and 21.7, respectively. The soil was mixed without drying, crumbled by hand to pass a plastic sieve (6-mm mesh), and thoroughly remixed. A subsample was air-dried and ground to pass a 2-mm sieve, for measurement of the total metal content.

The greenhouse pot experiment was set up with all combinations of the following treatments, applied in a complete factorial design with three replicates: Fe oxides (0.00, 0.22, 0.54, and 1.09% w/w, designated F0, F1, F2, and F3, respectively) and lime (0.00, 0.27, 0.68, and 1.36% w/w, designated L0, L1, L2, and L3, respectively). All treatments are expressed on the basis of air-dry soil. The Fe oxides treatments were made by adding solid FeSO₄·7H₂O (commercial grade, 93% purity; Ellis and Everard Ltd., Middlesbrough, UK) at concentrations calculated to supply the required amounts of Fe₂O₃. The concentrations of lime (agricultural ground lime, 95% CaCO₃) were calculated to neutralize the sulfuric acid released in the numerically corresponding level of Fe oxides treatment. Soil (1 kg field-moist per pot, containing 828 g air-dry soil) was weighed and mineral amendments were added, and the soil was then mixed by hand. Additional water (50 mL per pot) was added to create better conditions for seedling growth and the soil was placed in 12.5-cm-diameter plastic pots. One week was allowed for reaction to take place. Seedling lettuce plants (from Gerway Nurseries, Ottery St. Mary, Devon, UK), which had been germinated and grown in peat blocks for five weeks under glass, were planted, one per pot, and the soil surface mulched with black plastic granules. The pots were placed in a greenhouse with natural light and watered ad lib by filling the saucers daily. Two applications in solution of major nutrients (each 100 mg N, 50 mg P, and 62.5 mg K per pot) were made during growth. Six weeks after planting, all plant matter above 1 cm from the soil surface was harvested, rinsed quickly in demineralized water, dried at 80°C in a forced-draft oven, and ground to pass a 0.5-mm sieve. The soil was removed from each pot and mixed, and a portion of air-dried soil was ground to pass a 2-mm sieve.

Plant material (0.5 g) was weighed into a 100-mL block digestion tube. Concentrated HNO₃ (10 mL) was added, and the material was allowed to stand overnight. It was then heated for 3 h at 60°C followed by 6 h at 110°C, and then cooled. Filter paper (no. 540 filter; Whatman, Maidstone, UK) was prewashed with water. The digest sample was passed through the paper and water was used to rinse the digestion tube and filter three times and to make up the volume to 100 mL. Arsenic in the digest was measured by hydride-generation atomic absorption (AA) spectrometry (Model 1100B; PerkinElmer, Wellesley, MA). The concentrations of Al, Ba, Ca, Co, Cr, Cu, Fe, K, Mg, Mn, Na, Ni, Pb, Sr, and Zn were measured by inductively coupled plasma–optical emission spectrometry (ICP–OES) (Optima 3000; PerkinElmer). For the initial soil sample, metals extractable by aqua regia were measured. Soil (1.5 g) was weighed in duplicate into a 100-mL block digestion tube. Concentrated HNO₃ (3 mL) and concentrated HCl (10.5 mL) were added and the soil was allowed to stand overnight. It was then heated for 1 h at 50°C, followed by 3 h at 140°C, and then cooled. Filtration, rinsing, dilution to volume, and measurement of As and metals followed the same procedure as for plant tissue analysis except that 0.5 M HNO₃ was used instead of water. Soil pH was measured in water at a 1:2.5 w/v ratio. Statistical analysis of the data was performed with GENSTAT (Lawes Agricultural Trust, 1996).

	RESULTS

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Soil
The As concentration in the pot experiment soil was 577 mg kg^-1, which is representative of the field site, where the soil As concentrations of the plots varied from 489 to 1184 mg kg^-1 with a median value of 718 mg kg^-1. These As concentrations are well above the recommended limit of 50 mg kg^-1 for agricultural soils in the UK (Ministry of Agriculture, Fisheries and Food, 1993). However, As contamination declined sharply with distance from the contamination source to concentrations (approximately 100 mg kg^-1), which are not remarkable for Cornwall, a region with many As-bearing ore bodies. Concentrations of other potentially toxic elements were well within UK limits except for 236 mg Cu kg^-1, in comparison with the limit of 135 mg kg^-1. After the pot experiment, the pH of the soil with no amendments was 6.9. Soil pH was reduced by Fe oxides and increased by lime, as expected (Table 1). Soil pH was almost maintained in the treatments with "balanced" additions of Fe oxides and lime (F0L0, F1L1, F2L2, and F3L3), although this series showed a significant (P < 0.05) but small pH decline with increasing treatment rate, which is attributed to slowness of dissolution by the agricultural-grade lime and/or the presence of free H₂SO₄ as an impurity in the FeSO₄.

View larger version (14K): [in this window] [in a new window]   Fig. 1. Lettuce dry matter (DM) yield (treatment mean, g pot-1) in relation to soil pH and the Fe oxide treatments of soil.

[2]

View larger version (18K): [in this window] [in a new window]   Fig. 2. Relationship between As concentration in lettuce dry matter (mg kg-1) and soil concentration of added Fe oxides (%), for each pot of the treatment combinations F0L0, F1L1, F2L2, and F3L3, and the fitted exponential curve (Eq. [2]).

	DISCUSSION

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The in situ creation of precipitated Fe oxides with FeSO₄ was successful in lowering the bioavailability of As. For unamended soil, lettuce As concentration was 13.78 mg kg^-1 dry matter (1.42 mg kg^-1 fresh weight). The dry weight concentration was substantially above the typical range of 0.08 to 0.43 mg kg^-1 for field-grown lettuce reported by Liebig (1966). The fresh weight concentration was over the statutory general limit of 1.0 mg kg^-1 fresh weight in food for sale in the UK (Arsenic in Food Regulations, 1959), although it is very unlikely that consumption of this lettuce as part of a typical diet would result in unacceptably high As intakes. The treatment of soil with 1.09% Fe oxides and 1.36% lime reduced lettuce As concentration to 1.45 mg kg^-1 dry matter (0.14 mg kg^-1 fresh weight), far below the legal limit, and did not decrease dry matter yield. The bioavailable fraction of soil As could not be completely eliminated, as shown by the significant value of the asymptote of Eq. [2], and there was no significant difference in lettuce As concentration between the Fe oxides amendment concentrations of 0.54 and 1.09%. This suggests that the practical maximum reduction is achieved at an amendment concentration of approximately 0.5%.

The only comparable literature report is that of Vandecaveye et al. (1936), who applied FeSO₄ at a concentration equivalent to 0.4% Fe₂O₃, to two Californian orchard soils of pH 7.4 and 8.1. Barley (Hordeum vulgare L.) yield in these pots was increased by about 3.5 times in both soils and uptake of As was reduced by 47 or 75%. Similar results were found for the 0.54% Fe oxides treatment in the present work: although lettuce yield was little changed, the As concentration (and thus uptake) was reduced by 76%. Therefore, the application of FeSO₄ was effective in reducing As bioavailability, in line with the early reports on remediation of phytotoxicity (Vandecaveye et al., 1936; Thompson and Batjer, 1950) and recent laboratory studies of As solubility in response to added FeSO₄ (Moore et al., 2000). Therefore, FeSO₄ can be used to remediate soil containing old smelter residues as well as residues of a soluble source (lead arsenate) used as a pesticide. However, important questions remain about the stability of the treatment and effects of soil management systems.

The influence of pH on As sorption by soil depends on soil mineralogy (Smith et al., 1998, 1999), so divergent results for the influence of pH on As uptake may be expected. Marin et al. (1993) found that a pH increase from 5.5 to 7.5 lowered As uptake by rice, but on the other hand, Chen and Liu (1993) found that an increase in pH increased As toxicity problems in rice. Smith et al. (1999) found that pH change had little effect on arsenate sorption for soils low in oxidic minerals (Al and Fe oxides), while arsenate sorption decreased with pH increase in soils rich in oxidic minerals. The application of FeSO₄ to the Cornwall soil added oxidic minerals, suggesting that the pH increase caused by lime might decrease As sorption and increase lettuce As concentration for the FeSO₄–treated soils. In the present work, increasing soil pH (Table 1) lowered lettuce As concentration (Table 3), both with and without FeSO₄. Further investigation of the speciation of soil As and soil minerals before and after FeSO₄ addition should enable the result in this particular case to be understood. However, the effect of lime on lettuce As concentration was small compared with the main effect of FeSO₄. Therefore, for the purpose of developing a practical remediation method, the relevant feature of the lime component is that it is required simply to maintain a soil pH favorable to plant growth. The reduction in bioavailability caused by the treatment can be attributed to sorption or coprecipitation rather than a pH effect, because of the highly significant lowering of lettuce As by Fe oxides in the soils for which pH was approximately constant (Fig. 2).

Simultaneous application of lime was shown to be essential. Without enough lime, Mn in particular was mobilized to bioavailable concentrations that were phytotoxic. Concentrations of several other potentially toxic trace elements were also increased in the crops but they did not reach unacceptable values. Where Ni and Zn are present in soil at high concentrations, they too could be mobilized undesirably, but only if insufficient lime was applied. The resulting increases in lettuce Cu and Pb concentrations were modest (Table 4). The FeSO₄ to lime ratio calculated as indicated in the Materials and Methods section appears to be appropriate since it maintained yield, soil pH, and crop metal concentrations.

The occurrence of reducing conditions could lower the effectiveness of the remediation treatment, by causing reduction of As(V) to more toxic As(III) species and dissolution of Fe minerals. The initial addition of the Fe(II) salt introduces localized reducing conditions around FeSO₄ crystals but observations of the companion field experiment (to be reported later) showed that oxidation of the applied FeSO₄ occurred with a few days and normal aerobic conditions would be resumed, so it is considered that reduction by added Fe(II) would have only a transient effect before crop planting. However, flooding would cause a more persistent drop in Eh. The recently precipitated Fe oxides created by the proposed remediation treatment would probably be more liable to dissolution than preexisting Fe oxides, so the method is likely to be unsuitable for soils liable to flooding.

Fertilizer P is likely to affect As availability and remediation because phosphate and arsenate are similar in their chemical behavior and may be expected to compete for sorption sites in soil and for uptake by plant roots. The outcome of the competition is not predictable at present. On one hand, added P displaces sorbed As (Peryea, 1991) but on the other hand, the addition of P lowers the ratio As/(P + As) in the soil solution, which should reduce As plant uptake. Thus, Woolson et al. (1973) found that fertilizer P lowered As phytotoxicity to maize (Zea mays L.) in a silty clay loam, but increased it in a sandy loam and suggested that the difference was associated with higher As and P sorption in the silty clay loam. Since the proposed remediation treatment with FeSO₄ increases anion sorption capacity, it is possible that P fertilizer would assist remediation in the treated Cornwall soil, but this aspect will need to be investigated.

	CONCLUSIONS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION CONCLUSIONS REFERENCES

 
A potential remediation method to reduce As uptake by plants from soil is the application of commercial-grade FeSO₄ at 1.89% (w/w), giving an Fe oxides concentration of 0.54%, accompanied by 0.68% (w/w) of ground agricultural lime. This lowered lettuce As concentration by 84% in a greenhouse pot experiment with a neutral Denbigh series soil, for which As was the only important contaminant. The results are as relevant to field conditions as possible for a greenhouse since the FeSO₄, lime, and plants were commercial products, the same as those used at companion field trials (to be reported later), and the soil series is geographically well spread and suited to a variety of agricultural and domestic uses. The cost of materials (2002 prices in the UK) of the suggested method is high, being approximately $4500 ha^-1, so the proposed treatment is likely to be appropriate only for the redevelopment of contaminated land with industrial or governmental funding, but could be justified by site-specific public health considerations. Additional investigations are justified to assess (i) the suitability of the method in other soil types, especially if they contain other contaminant metals, (ii) different crops, (iii) longevity of the treatment, (iv) effects of P fertilizer, and (v) effects of liming.

	ACKNOWLEDGMENTS

 
We acknowledge financial support by the UK Food Standards Agency (Project C01021) and the UK Environment Agency, Mrs. K. Carter for maintenance of the pot experiment, and the associate editor and anonymous referees for suggested improvements to the manuscript.

	REFERENCES

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION CONCLUSIONS REFERENCES

 

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