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TECHNICAL REPORTS
Heavy Metals in the Environment

Effects of Organic Amendments on the Reduction and Phytoavailability of Chromate in Mineral Soil

^a Soil & Earth Science Group, Massey Univ., Palmerston North, New Zealand
^b Savannah River Ecology Laboratory, Drawer E, Aiken, SC 29802

* Corresponding author (n.s.bolan{at}massey.ac.nz)

Received for publication October 22, 2001.

	ABSTRACT

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In this study, seven organic amendments (biosolid compost, farm yard manure, fish manure, horse manure, spent mushroom, pig manure, and poultry manure) were investigated for their effects on the reduction of hexavalent chromium [chromate, Cr(VI)] in a mineral soil (Manawatu sandy soil) low in organic matter content. Addition of organic amendments enhanced the rate of reduction of Cr(VI) to Cr(III) in the soil. At the same level of total organic carbon addition, there was a significant difference in the extent of Cr(VI) reduction among the soils treated with organic amendments. There was, however, a significant positive linear relationship between the extent of Cr(VI) reduction and the amount of dissolved organic carbon in the soil. The effect of biosolid compost on the uptake of Cr(VI) from the soil, treated with various levels of Cr(VI) (0–1200 mg Cr kg^-1 soil), was examined with mustard (Brassica juncea L.) plants. Increasing addition of Cr(VI) increased Cr concentration in plants, resulting in decreased plant growth (i.e., phytotoxicity). Addition of the biosolid compost was effective in reducing the phytotoxicity of Cr(VI). The redistribution of Cr(VI) in various soil components was evaluated by a sequential fractionation scheme. In the unamended soil, the concentration of Cr was higher in the organic-bound, oxide-bound, and residual fractions than in the soluble and exchangeable fractions. Addition of organic amendments also decreased the concentration of the soluble and exchangeable fractions but especially increased the organic-bound fraction in soil.

Abbreviations: DOC, dissolved organic carbon

	INTRODUCTION

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A NUMBER OF industrial activities, including coal-fired power production, electroplating, leather tanning, timber treatment, pulp production, and mineral ore and petroleum refining, generate solid and aqueous waste products that are enriched with various heavy metals including hexavalent chromium [Cr(VI)] (Forstner and Wittman, 1981). The disposal of these wastes in landfills can potentially result in the release of Cr(VI) species to surface and subsurface waters. For example, approximately 6400 and 1600 Mg of tannery and timber treatment effluents, respectively, are generated annually in New Zealand, and these effluents are considered to be the major sources of Cr contamination into aquatic and terrestrial environments (Carey et al., 1996). Chromium is used as Cr(III) in the tannery industry and as Cr(VI) in the timber treatment industry (Barnhart, 1997). Chromium(VI) is highly toxic and carcinogenic even when present in very low concentrations in water (Bartlett and Kimble, 1976; Bartlett, 1991). The maximum recommended concentration of Cr(VI) in drinking water is 0.05 mg L^-1 (World Health Organization, 1996).

While Cr(III) is strongly retained onto soil particles, Cr(VI) is very weakly adsorbed and is readily available for plant uptake and leaching to ground water (James and Bartlett, 1983). Leaching studies have indicated that Cr(VI) is readily leached compared with Cr(III) and anions, such as arsenate (Carey et al., 1996; Bolan and Thiyagarajan, 2001). Chromium(VI) can be reduced to Cr(III) in the environments where a ready source of electrons is available. Suitable conditions for Cr(VI) reduction occur where organic matter is present to act as an electron donor, and Cr(VI) reduction is enhanced in acid rather than alkaline soils (Bartlett and Kimble 1976; Cary et al., 1977). Reduction of Cr(VI) to Cr(III), and subsequent hydroxide precipitation of Cr(III) ion, is the most common method of treating Cr(VI)-contaminated industrial effluents (Besseliever, 1969). Various organic materials, such as powdered leaves (Suseela et al., 1987) and Scotch pine (Pinus sylvestris L.) bark (Alves et al., 1993) have been used to remove Cr(VI) from industrial effluents.

Addition of biological waste materials, such as poultry and livestock manures and biosolid, has often been shown to increase the amount of dissolved organic carbon (DOC) in soils either by acting as a source of DOC or by enhancing the solubilization of the soil organic matter (Schindler et al., 1992). The easily oxidizable organic carbon and the DOC fractions provide the energy source for the soil microorganisms involved in the reduction of metals, such as Cr [i.e., Cr(VI) to Cr(III)], and nonmetals, such as N [i.e., nitrate (NO₃^-) to gaseous nitrogen (NO, N₂O, and N₂) denitrification] (Paul and Beauchamp, 1989; Jardine et al., 1999).

Although a number of workers have examined the phytotoxicity of Cr(VI) (Turner and Rust, 1971; Bishnoi et al., 1993; Srivastava et al., 1994; Mishra et al., 1997), the effect of organic soil amendments (such as manure composts) on the reduction of Cr(VI) and its subsequent availability for plant uptake has not been examined in detail (Losi et al., 1994). The role of different fractions of carbon in organic amendments on the reduction of Cr(VI) has not been elucidated. In this study, the effect of seven organic amendments on the reduction of Cr(VI) in a mineral soil was examined and the contribution of various carbon fractions to the reduction was investigated. In addition, the effect of one of the organic amendments (biosolid compost) on the uptake of Cr from a soil treated with Cr(VI) was evaluated with mustard plants.

	MATERIAL AND METHODS

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Soil and Organic Amendments
A mineral soil low in organic matter content from New Zealand (Manawatu fine sandy loam; Dystric Fluventic Eutrochrept) was used in this study (Table 1). The organic carbon content of the soil was low (9.2 g kg^-1) and the pH of the soil was slightly acidic (6.12). The dominant clay minerals were mica, chlorite, smectite, kaolinite, and halloysite.

Chromium(III) and Chromium(VI) Adsorption
In most studies involving Cr(VI) reduction, the extent of reduction was measured from the changes in Cr(VI) concentration in the soil solution at a known level of Cr(VI) addition. It was often assumed that a negligible amount of Cr(VI) adsorption occurred under optimum pH conditions for plant growth (pH 6–7). Under field pH conditions, most soils carry a net negative charge and adsorb greater amounts of Cr(III) than Cr(VI) (Rai et al., 1987; Bolan et al., 1999b). However, in soils containing positive charge components, significant amounts of Cr(VI) adsorption can occur under acidic pH conditions (Zachara et al., 1989; Fendorf et al., 1997). It is important to account for Cr(VI) adsorption when the extent of Cr(VI) reduction is estimated from the changes in Cr(VI) concentration in soil solution. Phosphate-extractable Cr(VI) is often used as a measure of adsorbed Cr(VI) in soils (Losi et al., 1994; James et al., 1995). In this study, a preliminary experiment was conducted to examine the adsorption of both Cr(III) and Cr(VI) species by the soil.

Chromium adsorption was measured at a known Cr concentration (60 mg L^-1; 600 mg kg^-1 soil) with Cr₂(SO₄)₃ [Cr(III)] and K₂Cr₂O₇ [Cr(VI)] with 0.1 M KNO₃ as the background electrolyte. Addition of organic amendments increased the ionic strength of the soil solution, as measured by electrical conductivity. Since ionic strength affects solute adsorption we used a nonspecific electrolyte (KNO₃) to mask the effect of organic amendment–induced ionic strength on Cr adsorption. Nitrate, being a weakly retained solute, did not affect the adsorption of Cr(VI).

Soil samples were mixed with the Cr solutions at a soil to solution ratio of 1:10 by shaking on an end-over-end shaker for 16 h at room temperature (20°C). The soil suspension was filtered through a 0.45-µm Millipore (Bedford, MA) membrane filter and the solution stored at -4°C for Cr analysis. The residual soil sample was extracted with either deionized water or 1 M KH₂PO₄ at a soil to solution ratio of 1:10 for 16 h and the solution was filtered through a 0.45-µm filter. The concentration of Cr in the soil solutions was measured with an atomic absorption spectrophotometer for total Cr and the colorimetric analysis for Cr(VI) with diphenylcarbazide reagent (James and Bartlett, 1983). From these values the concentration of Cr(III) in the extracts was calculated.

Chromium(VI) Reduction
For the Cr(VI) reduction experiment, the soil sample was mixed with two levels of organic amendments (0 and 50 g OC kg^-1 soil) and incubated at field capacity for 4 wk. These samples were subsequently mixed with two levels of Cr(VI) (0 and 600 mg Cr kg^-1 soil) with K₂Cr₂O₇ and incubated at field capacity. Subsamples were taken at various intervals and extracted with either deionized water or 1 M KH₂PO₄ at a soil to solution ratio of 1:10 for 16 h and the solution was filtered through a 0.45-µm filter. The soil extracts were analyzed for total Cr and Cr(VI).

Plant Growth Experiment
A glasshouse growth experiment was set up to investigate the effect of biosolid compost on the plant uptake of Cr(VI). The soil samples were incubated with various levels of biosolid compost (0–100 g OC kg^-1 soil) for 4 wk. The biosolid compost-amended samples were subsequently treated with various levels of Cr(VI) (0–1200 mg kg^-1 soil) with K₂Cr₂O₇ and further incubated for 4 wk. After incubation with the biosolid compost and Cr(VI), the soil samples were transferred to plastic pots. Indian mustard was used as a test plant due to its ability to tolerate high levels of heavy metals in soils (Anderson et al., 2001). Eight seeds were sown in each pot and the seedlings were thinned to four plants per pot. During the germination period the moisture content of the soil was maintained at 80% of field capacity and after thinning the moisture content was raised to field capacity. Complete Hoagland nutrient solution was added twice per week.

The plants were harvested 12 wk after sowing and dried at 70°C with a forced draft oven. The dry weights were recorded and the plant materials were ground with a Cr-free stainless steel grinder. The plant materials were digested with concentrated HNO₃ and the concentration of Cr in the plant digest was determined with a graphite-furnace atomic absorption spectrophotometer.

Fractionation of Soil Chromium(VI)
A modified sequential fractionation procedure developed by Radmila and Stupar (1995) was used to fractionate different forms of Cr that include soluble Cr (0.015 M KH₂PO₄), exchangeable Cr (1 M NH₄Cl), organic-bound Cr (0.1 M Na₄P₂O₇; pH 10), Fe and Mn oxide-bound Cr (0.04 M NH₂OH·HCl in 25% CH₃COOH; pH 2), and residual Cr (HNO₃ to HCl to HClO₄ ratio = 5:5:7). Soil samples from the plant growth experiment (0 and 600 mg Cr kg^-1 soil levels) were used for the fractionation. After each extraction the tubes were centrifuged at 11 952 x g for 10 min, and the supernatant solution was filtered through Whatman (Maidstone, UK) #42 filter paper and collected for analysis. The amount of entrained solution was monitored at each extraction stage to account for the Cr remaining in the entrained solution. The concentration of total Cr in the soil extracts was measured by atomic absorption spectrophotometry.

The water-soluble fraction of Cr(VI) at all levels of Cr(VI) addition was obtained by shaking 20 g soil with 200 mL deionized water for 2 h. The concentration of Cr(VI) in the water-soluble fraction was measured by the colorimetric analysis.

Carbon Measurements
Soil organic matter provides a source of carbon for soil microorganisms involved in the reduction of Cr(VI). The availability of soil organic matter as an energy source for microorganisms depends on the relative distribution of various fractions of organic carbon. One of the objectives of the study was to relate the extent of Cr(VI) reduction to various fractions of organic carbon. The total carbon in the soil and the organic amendments was measured following the LECO (St. Joseph, MI) combustion technique (Bremner and Tabatabai, 1971). The easily oxidizable organic carbon was measured with chromic acid as the oxidizing agent (Walkley and Black, 1934). For the extraction of dissolved organic carbon (DOC), a 10-g sample was equilibrated with 100 mL 0.5 M K₂SO₄ solution in 250-mL centrifuge tubes (Bolan et al., 1999a). The sample was shaken in an end-over-end shaker for 1 h and the solution was centrifuged at 7649 x g for 10 min. The solution was filtered through a 0.45-µm filter. The organic carbon in the solution was analyzed with the total organic carbon (TOC) analyzer after making correction for the soluble inorganic carbon.

	RESULTS AND DISCUSSION

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Chromium(III) and Chromium(VI) Adsorption
In the batch adsorption experiment, the concentrations of Cr(III) and Cr(VI) in the equilibrium soil solution decreased from 60 mg L^-1 (input concentration) to 53.14 and 55.65 mg L^-1, respectively, for the unamended soil, the decrease being higher in soils treated with the organic amendments (Table 2). In the case of Cr(III), this decrease was attributed mainly to the adsorption–precipitation of Cr(III) because there was no evidence for the oxidation of Cr(III) to Cr(VI). Oxidation of Cr(III) to Cr(VI) has been shown to occur in soils, but requires the presence of high-valency Mn in the soil as an electron acceptor for the reaction to proceed (Bartlett and James, 1979; Fendorf and Zasoski, 1992). Since the soil used in this study contained no detectable Mn oxide, oxidation of Cr(III) was unlikely. Addition of organic amendments resulted in an increase in the adsorption of Cr(III) (e.g., from 68.6 mg kg^-1 in the unamended soil to 254.5 mg kg^-1 in the biosolid-treated soil), which was attributed to an increase in the cation exchange capacity of the soil. Adsorption of Cr(III) by soils resulting from both nonspecific cation exchange and specific adsorption processes at low surface coverage has also been reported (Rai et al., 1987; Fendorf and Sparks, 1994).

Rate of Chromium(VI) Reduction
In the incubation experiment, the concentration of Cr(VI) in both the water and 1 M KH₂PO₄ extracts decreased with increasing time after Cr(VI) addition. The nearly equal concentrations of Cr(VI) between these two extracts indicate negligible Cr(VI) adsorption by the soil, as shown by the adsorption experiment (Table 2). This confirms the results from the batch adsorption, that is, the decrease in the concentration of Cr(VI) in the soil extracts was attributed mainly to the reduction of Cr(VI) to Cr(III).

The amounts of Cr(VI) reduced were estimated from the decrease in the concentration of Cr(VI) in soil solution, which increased with increasing time after Cr(VI) addition, and the maximum Cr(VI) reduction occurred within 2 wk after Cr(VI) addition (Fig. 1) . Reduction of Cr(VI) to Cr(III) in soils has often been found to be rapid, reaching the maximum within a relatively short time, that is, in days (Ross et al., 1981).

View larger version (26K): [in this window] [in a new window]   Fig. 1. Amounts of Cr(VI) reduced during the incubation of Cr(VI) with the unamended and amended soils (•, soil; , soil + horse manure; , soil + farm yard manure; , soil + fish manure; , soil + spent mushroom; , soil + pig manure; , soil + poultry manure; , soil + biosolid compost). Fitted curves are shown as solid lines.

[1]

where Y is the amount of Cr(VI) reduced (mg kg^-1), Y_m is the amount of maximum reduction (mg kg^-1), r is the rate constant, and x is the incubation period (days). The Y_m and r parameters of the equation describing the data are presented in Table 3. Both the maximum reduction (Y_m) and the rate factor (r) increased with the addition of organic amendments. There was a greater variation in the Y_m values than the r values among the soil samples. At the same level of total organic carbon addition, there was a significant difference both in the rate factor and the maximum reduction among the soil samples treated with the organic amendments. The rates of reduction of Cr(VI) in soils treated with organic amendments relative to that of the unamended soil were calculated from the r values (Table 3). These values indicate that the addition of some of the organic amendments, such as biosolid, caused almost twofold increases in the rate of reduction of Cr(VI) in the soil. This is consistent with the findings of Losi et al. (1994), where a substantial increase in the rate of reduction of Cr(VI) in the presence of manure occurred.

View larger version (16K): [in this window] [in a new window]   Fig. 2. Relationship between Cr(VI) reduction and (a) easily oxidizable organic carbon and (b) dissolved organic carbon in the unamended and amended soils.

[2]

In the incubation experiment, the soil pH decreased with the addition of the organic amendments both in the presence and the absence of Cr(VI). The organic amendments were rich in N, part of which was in ammoniacal form. Oxidation of ammoniacal N to nitrate N (nitrification) resulted in the release of protons. This may be one of the reasons for the decrease in soil pH with the addition of the organic amendments (Table 4). In general, the extent of Cr(VI) reduction increased with a decrease in the pH of the unamended and amended soils in the absence of Cr(VI) (Fig. 3a) . The reduction of Cr(VI) to Cr(III), being a proton consumption (or hydroxyl release) reaction (Eq. [2]), was found to increase with a decrease in soil pH (Cary et al., 1977; Eary and Rai, 1991).

View larger version (19K): [in this window] [in a new window]   Fig. 3. Relationships between (a) Cr(VI) reduction and pH of the unamended and amended soils and (b) theoretical and measured amounts of protons consumed during Cr(VI) reduction.

The increase in Cr(VI) reduction in the presence of organic amendments may also result from an increase in microbial activity. Losi et al. (1994) showed that the addition of a manure compost increased Cr(VI) reduction both under sterile (i.e., abiotic) and nonsterile (i.e., biotic) conditions. However, manure addition caused a larger increase in biotic than abiotic Cr(VI) reduction, indicating its greater contribution to the former process. This suggests that the supply of microorganisms was more important than the supply of organic carbon in enhancing the reduction of Cr(VI) with the addition of organic compost. Addition of manure compost has often been shown to increase the microbial activity of soil, as measured by increased respiration (Kanazawa et al., 1988). This resulted from both increased supply of carbon and nutrient sources such as N, phosphorus (P), and sulfur (S) (Wardle, 1992). An increase in microbial activity has often been reported to increase the reduction of Cr(VI) to Cr(III) (Losi et al., 1994). Although Cr(VI) reduction can occur through both chemical (abiotic) and biological (biotic) processes, the latter one is considered to be the dominant process in most agricultural soils that are low in ferrous (Fe²⁺) ion. A range of microorganisms are involved in the reduction of Cr(VI) to Cr(III). It was not clear whether the increase in Cr(VI) reduction due to organic amendment addition resulted either from an enhancement of the microbial population, which was specific to Cr(VI) reduction, or from an increase in the general microbial activity. It is important to point out that no attempt was made to separate the abiotic and biotic processes of Cr(VI) reduction in this study. It was possible that the addition of organic amendments also enhanced the abiotic process of Cr(VI) reduction by supplying readily oxidizable organic carbon (Losi et al., 1994).

Plant Growth and Chromium Uptake
In the absence of biosolid addition, the germination was delayed in low levels of Cr(VI) addition and germination failed at the highest level of Cr(VI). Plant growth decreased with increasing level of Cr(VI) addition (Fig. 4a) . Increasing addition of biosolid enhanced plant growth even at the highest level of Cr(VI) addition (Fig. 4a).

View larger version (20K): [in this window] [in a new window]   Fig. 4. (a) Dry matter yield of mustard plants and (b) the concentration of total Cr in plant tissue at various levels (g organic carbon kg-1 soil) of biosolid compost addition (•, 0; , 25; , 50; , 100).

View larger version (19K): [in this window] [in a new window]   Fig. 5. Relationships between dry matter yield and (a) soil solution Cr(VI) concentration and (b) plant tissue total Cr concentration.

	CONCLUSIONS

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	ACKNOWLEDGMENTS

 
This project was supported by Agricultural Human Resource Development Programme (AHRDP) funded by FAO. The U.S. Department of Energy contract number DE-FC-09-96SR18546 with the University of Georgia's Savannah River Ecology Laboratory supported Dr. Bolan's, Dr. Adriano's, and Dr. Koo's writing and editing time.

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