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TECHNICAL REPORT
Heavy Metals in the Environment

In Situ Stabilization of Soil Lead Using Phosphorus and Manganese Oxide

Influence of Plant Growth

Department of Agronomy, Throckmorton Plant Sciences Center, Kansas State Univ., Manhattan, KS 66506-5501

* Corresponding author (hettiarachchi.ganga{at}epa.gov)

Received for publication November 22, 2000.

	ABSTRACT

TOP NOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS REFERENCES

 
In situ stabilization of Pb contaminated soils can be accomplished by adding P and Mn(IV) oxide. However, the long-term efficacy of in situ stabilization under continual P removal through plant growth is unknown. Moreover, the effects these treatments have on phytoavailability of other metals (Cd and Zn) commonly associated with Pb in soil are not well understood. Greenhouse experiments using sudax [Sorghum vulgare (L.) Moench] and Swiss chard [Beta vulgaris (L.) Koch] were carried out to evaluate the effects of plant growth on soil Pb bioavailability to humans after addition of P and other amendments, and the effects of these treatments on Pb, Cd, and Zn phytoavailability in three metal-contaminated soils. Eight treatments were used: zero P; 2500 mg of P as triple superphosphate (TSP); 5000 mg of P as TSP or phosphate rock (PR); 5000 mg of Mn oxide/kg; and combinations of Mn oxide and P as TSP or PR. The addition of P and/or Mn oxide significantly reduced bioavailable Pb, as measured by the physiologically based extraction test (PBET), in soils compared with the control even after extensive cropping. The PBET data also suggested that removal of P from soluble P sources by plants could negate the beneficial effects of P on bioavailable Pb, unless sufficient soluble P was added or soluble P was combined with Mn oxide. In general, Pb, Cd, and Zn concentrations in shoot tissues of sudax and Swiss chard were reduced significantly by TSP and did not change with the addition of PR. The combination of PR and Mn oxide significantly reduced Pb concentrations in plants compared with the control.

Abbreviations: AR, active repository • CRYP, cryptomelane • HA, hydroxyapatite • ICP–AES, inductively coupled plasma–atomic emission spectroscopy • PBET, physiologically based extraction test • PR, phosphate rock • TCR, time-critical repository • TSP, triple superphosphate

	INTRODUCTION

TOP NOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS REFERENCES

 
HUMANS MAY ASSIMILATE toxic metals from soil through two primary pathways: soil ingestion and the food chain. For Pb, translocation from the soil to plant roots and through the roots to the shoots is minimal because of chemical immobilization in soils as well as in roots (Laperche et al., 1997; Chaney and Giodriano, 1977). In assessments of risk associated with Pb-contaminated soils, ingestion by children is one of the major exposure pathways of concern. The bioavailability of soil Pb determines the physiological effect after ingestion. Many researchers have suggested that Pb bioavailability may depend on the forms of Pb in soils and their solubility (Cotter-Howells and Thornton, 1991; Ruby et al., 1994, 1996, 1999) and site-specific soil chemistry (Chaney et al., 1989; Ruby et al., 1999).

Lead phosphates, particularly pyromorphites, are one of the most stable forms of Pb in soils under a wide range of environmental conditions (Nriagu, 1974). Ma et al. (1993) showed that hydroxyapatite [Ca₅(PO₄)₃OH] has the potential to immobilize Pb in solution by formation of hydroxypyromorphite. Formation of pyromorphites upon addition of apatite or soluble inorganic P amendments has been observed in Pb-contaminated soil materials (Cotter-Howells and Caporn, 1996; Laperche et al., 1997). The formation of Pb phosphates in soils contaminated with both Pb and P may be responsible for immobilizing Pb and thereby reducing its bioavailability (Ruby et al., 1994; Hettiarachchi et al., 2001).

In addition to the formation of insoluble Pb compounds, adsorption of Pb represents another potentially important process for reducing bioavailability. Specific adsorption of Pb to Mn(IV) (hydr)oxide is known to be greater than that to any other metal (hydr)oxide. McKenzie (1980) demonstrated that adsorption of Pb to Mn oxides was 40 times greater than adsorption to Fe oxides and was more or less irreversible, suggesting that Mn oxides can be used as strong adsorbents or scavengers for Pb. Hettiarachchi et al. (2000) showed that the combination of P and Mn oxide reduced soil Pb bioavailability more than either amendment alone.

After applications of P and other soil amendments to remediate Pb-contaminated residential soils, vegetation would be necessary to keep the treated soil intact. Typically the vegetation would be turf grasses. In addition, vegetables may be grown by home gardeners. Continual removal of P and other soil chemical changes induced by plant growth may affect soil Pb bioavailability in P-treated soils. Information on soil-Pb bioavailability after plant growth on in situ–treated Pb-contaminated soils is lacking.

In this manuscript the term bioavailability is used to describe the amount of soil Pb that could be soluble in the human gastrointestinal tract and potentially available for absorption into the human blood stream. Phytoavailability will be used to describe the portion of soil Pb available for plant uptake.

Soil Pb bioavailability can be estimated by several methods. Typically, the USEPA relies on feeding studies using immature swine as the model animals, because their digestive systems are similar to those of humans. However, because of the high cost associated with animal feeding studies, they are not practical as routine procedures for determining soil Pb bioavailability. A physiologically based extraction test (PBET) (also known as an in vitro test system) developed by Ruby et al. (1996) can be used to predict the bioavailability of metals from a solid matrix as a surrogate for animal feeding studies. For Pb and As, this method has proven to be well correlated with animal feeding studies using weanling rats (Ruby et al., 1996) and young swine (Medlin, 1997). We selected a modified PBET procedure to determine the influence of continual removal of P and other soil chemical changes induced by plant growth on soil Pb bioavailability.

Cadmium (Cd) and zinc (Zn) are commonly associated with Pb in contaminated soils, and Cd is considered highly toxic to humans. When soils are co-contaminated with Pb, Cd, and Zn, the effects of P and other amendments on Cd and Zn bioavailability are not well understood. The soil–plant barrier limits food-chain transmission of heavy metals either by a chemical process (Pb) or by limiting plant growth before uptake reaches levels that would cause injury to consumers (Zn) (Chaney and Giodriano, 1977). However, this barrier is not effective for Cd and the Cd content of plants can reach levels that are potentially harmful.

The objectives of this study were to evaluate the effects of plant growth on soil Pb bioavailability after the soil was amended with P and Mn oxide, and to determine the effects of P and other soil amendments on Pb, Cd, and Zn phytoavailability.

	MATERIALS AND METHODS

TOP NOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS REFERENCES

 
Materials
Three metal-contaminated soils were collected from Joplin, MO. Two soils were from repositories used to store soils that had been excavated from residential areas as part of ongoing remediation activities. These samples were designated AR for the active repository and TCR for the time-critical repository, which is no longer receiving soils. The third contaminated soil was collected from a vacant lot directly adjacent to an abandoned Zn–Pb smelter site. This sample was designated Joplin. Selected chemical properties of the soils are given in Table 1. All three soils contained total Pb concentrations higher than the current limit for residential land use in the United States, which is about 400 mg Pb/kg soil (Berti and Cunningham, 1997).

Preparation of Manganese Oxide
Cryptomelane was chosen as the representative MnO₂ mineral because of its greater affinity for Pb compared with other Mn oxides (McKenzie, 1980). The cryptomelane used in this study was KMn₈O₁₆–potassium manganese oxide (JCPDF File no. 20-908). It was prepared according to procedures described by Hettiarachchi et al. (2000).

Methods
Eight treatments in triplicate were evaluated: no P (control); 2500 mg P/kg soil as TSP fertilizer (TSP2500); 5000 mg P/kg soil as TSP (TSP5000) or PR (PR5000); 5000 mg of cryptomelane/kg soil (CRYP); 2500 mg P as TSP plus 5000 mg of CRYP/kg of soil (TSP2500 + CRYP); and 5000 mg of CRYP/kg of soil plus 5000 mg P as TSP (TSP5000 + CRYP) or PR (PR5000 + CRYP). The amount of P required for each treatment was calculated on the basis of the total P content of the P source. Treatments were applied evenly onto the soil and mixed thoroughly. Deionized water was added to bring the samples back to 20% gravimetric water content (_m), and soils were mixed thoroughly a second time. Twenty-four hours after P additions, predetermined amounts of CaO were added to some samples as necessary to ensure that the final soil pH was 7.0 or above.

Six days after CaO treatment, subsamples of soil (1.25 kg/pot) from each treatment were placed in pots lined with a cellophane bag (with fewer holes on sides) to avoid free drainage. Pots were seeded with sudax, a hybrid of sorghum [Sorghum bicolor (L.) Moench] and sudangrass (Sorghum vulgare var. sudanese). Sudax was chosen for the greenhouse pot experiment because it produces high forage yield, grows well under greenhouse conditions, and has been proven to accumulate Pb readily (Laperche et al., 1997). Approximately 2 wk after seeding, plants were thinned to eight per pot. Pots were watered daily with distilled water, and every 14th day supplied with P-free nutrient solution containing N, K, Mg, and S. Aboveground biomass was harvested four times at 7- to 9-wk intervals. The lower one-third of the plant materials was washed with a 5 g/kg solution of sodium lauryl sulfate [CH₃-(CH₂)₁₀CH₂OSO₃Na] and then with deionized water to remove adhering soil particles before plants were oven-dried at 55°C for 5 d and then weighed. Finely ground subsamples of 0.25 g plant material were digested with concentrated H₂SO₄ and 9.7 M H₂O₂ for determining plant P uptake (Thomas et al., 1967). Phosphorus concentrations in the digests were analyzed using inductively coupled plasma–atomic emission spectroscopy (ICP–AES) (Accuris 141; Fisons Instruments, Beverly, MA).

After the fourth cutting, soil samples were collected, air-dried, and analyzed for soil pH (1:1 soil to deionized water), NaHCO₃–extractable P (Olsen et al., 1954), and bioavailable Pb. Sodium bicarbonate–extractable P is an appropriate test for measuring plant-available P in both acidic and alkaline soils, particularly those containing free carbonates (Kuo, 1996). This procedure was chosen because of the desire to maintain soil pH above 7.0; maintaining soil pH above 7.0 would be suitable for controlling mobility of these metals. Soils were sieved through a 250-µm stainless steel sieve before determining bioavailable Pb using a modified PBET procedure as described by Hettiarachchi et al. (2000). The pH of stomach phase extract was maintained at 2.00 ± 0.2 while intestinal phase extract pH was maintained at approximately 7.0. Soluble Pb in the stomach and intestinal phases was analyzed using ICP–AES. Quality assurance–quality control (QA– QC) consisted of approximately 12.5% of samples run as duplicates, check samples, or blanks for each extraction. Extractions were done in batches of nine comprised of eight samples and a QA–QC sample to reduce random error. Bioavailable Pb is expressed as a percentage of bioavailable Pb in the control sample.

A second set of pots was seeded with Swiss chard (variety Fordhook giant). Swiss chard is a known heavy metal accumulator (Chaney and Giodriano, 1977) and can be used to assess food chain risk from heavy metals to humans. Three replicates for each treatment containing 1.0 kg soil were used. After 2 wk, pots were thinned to 7 to 8 plants/pot. Swiss chard was grown for 8 wk before aboveground biomass was harvested. The plants were washed with a 5 g/kg solution of sodium lauryl sulfate [CH₃(CH₂)₁₀CH₂OSO₃Na] followed by deionized water, and then processed as described for sudax grass.

Finely ground subsamples of 0.5 g of both plant materials were digested with trace metal grade, concentrated HNO₃ acid for 4 h at 120°C. Filtered digest solutions of sudax were analyzed for Pb using a PerkinElmer (Wellesley, MA) graphite tube atomizer (GTA, equipped with Zeeman baseline correction) connected to an atomic absorption spectrometer (AAS) while those for Swiss chard were analyzed for Pb using a Varian (Palo Alto, CA) GTA-95 connected to an AAS (Varian AA-1475 Series). Cadmium and Zn were analyzed using ICP–AES.

Data Analyses
Plant studies were set up with three replications as a randomized complete block design (RCBD). Statistical analyses were performed using SAS for Windows Version 6.12 (SAS Institute, 1985). For mean separations, least significant difference (LSD) values were used at P < 0.05.

	RESULTS AND DISCUSSION

TOP NOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS REFERENCES

 
Soil pH and Sodium Bicarbonate– Extractable Phosphorus
Calcium oxide additions helped to maintain pH above 7.0 in most soil samples (Table 2). Samples that received 5000 mg P/kg soil as TSP (TSP5000 and TSP5000 + CRYP) had the lowest pH, which were slightly less than 7.0 for the Joplin and AR soils. Triple superphosphate–amended samples showed significantly greater NaHCO₃–extractable P levels compared with all other treatments after four cuttings of sudax (Table 3). Further, P concentrations were well above those required for normal plant growth. The increase from 2500 to 5000 mg P/kg as TSP also significantly increased NaHCO₃–extractable P levels. However, NaHCO₃–extractable P levels observed in PR-treated soils were not significantly different from those in the control samples for all three soils. This was not surprising, because all three soils had near-neutral soil solution pH levels. Excessive levels of plant-available P have been correlated with higher P losses in runoff. Thus, PR may present less of an environmental risk from enhanced eutrophication compared with the other P sources.

The highest plant tissue P concentrations were observed in TSP treatments, indicating that the P uptake by sudax was enhanced by the presence of a soluble P source (data not shown). Trends for cumulative P uptake by sudax were similar for all three soils, and, therefore, only data for Joplin material are presented (Fig. 1) . Because biomass production was also highest for the TSP treatments, cumulative P uptake was significantly higher than in all other treatments. The addition of PR with or without cryptomelane did not change P uptake significantly compared with the control. This is expected because PR would not undergo dissolution to greater extent when applied to nearly neutral soils. Net removal of P by sudax ranged from 1.2 to 2.7% of the P added for TSP-amended soils.

View larger version (44K): [in this window] [in a new window]   Fig. 1. Cumulative P removal by sudax grass aboveground biomass after four cuttings in the Joplin soil. Means with the same letter within a soil are not significantly different at P < 0.05.

View larger version (50K): [in this window] [in a new window]   Fig. 2. Bioavailable Pb by physiologically based extraction test (PBET) for the (a) Joplin, (b) active repository (AR), and (c) time-critical repository (TCR) soil after four cuttings of sudax. Bioavailable Pb is expressed as a percentage of bioavailable Pb in the control sample. Means with the same letter within a phase are not significantly different at P < 0.05.

Unlike the TSP2500 treatment, the TSP2500 + CRYP maintained significantly lower bioavailable Pb levels compared with the control after plant growth in all three soils despite comparable levels of P uptake (Fig. 1 and 2). The surfaces of Fe and Al oxides modified by phosphates are known to adsorb greater amounts of cations, including Pb, compared with unmodified oxides (Bolland et al., 1977; Kuo and McNeal, 1984; Weesner and Bleam, 1998). Weesner and Bleam (1998) suggested that pyromorphite could form on the surfaces of phosphate-modified Fe-oxide surfaces. Similarly, the presence of Mn oxide may have enhanced the reactions between applied P and soil Pb. Moreover, for the AR and TCR soils, the TSP2500 + CRYP treatment had significantly lower bioavailable Pb than the TSP5000 treatment. This indicates that addition of cryptomelane would permit addition of less P without compromising the reductions in bioavailable Pb, consequently reducing environmental risk associated with applications of large amounts of soluble P.

Without exception, the greatest reductions in bioavailable Pb were observed with PR5000 + CRYP or TSP5000 + CRYP, indicating that even after plant P removal and the soil chemical changes induced by plant growth, these treatments were able to maintain up to a 50% reduction in Pb bioavailability compared with the control. Possible mechanisms for these results have been discussed previously (Hettiarachchi et al., 2000). Our results showed little indication that PR dissolved enough to supply P for plant growth or to react with Pb (Fig. 1). This may be advantageous, since it would minimize the potential for offsite movement of P and the associated environmental problems. Still, the data demonstrated that the combination of PR and cryptomelane provided reductions in bioavailable Pb comparable with those found with TSP + CRYP (Fig. 2).

Plant Lead Concentrations
In general, trends of sudax tissue Pb concentrations in all four cuttings were similar, and, therefore, Pb concentrations in the fourth cuttings of sudax are shown in Table 4. They ranged from 0.23 to 3.07 mg/kg with little overall variation. In the Joplin soil, P additions from either TSP or PR generally reduced Pb concentrations in sudax compared with the control. The main mechanism of Pb immobilization by TSP is likely the dissolution of P and precipitation of pyromorphite-like minerals in soils as described elsewhere (Ma et al., 1995). However, PR may not undergo sufficient dissolution to immobilize Pb via precipitation of pyromorphite-like minerals in near-neutral soils. Instead, PR may reduce Pb phytoavailability by surface adsorption, substitution, or surface precipitation (Ma et al., 1995; Hettiarachchi et al., 2001). The addition of cryptomelane significantly reduced sudax tissue Pb concentration compared with the control in the last three cuttings. Because sorption of Pb to Mn oxides is considerably higher than that to any other metal oxides, the addition of cryptomelane could result in reductions in plant Pb uptake via specific sorption of Pb. McKenzie (1978) also observed reduced uptakes of Pb and Co by subterranean clover (Trifolium subterraneum L.) grown on three Pb-contaminated soils after addition of two varieties of Mn oxides (cryptomelane and birnessite) separately.

Laperche et al. (1997) investigated the effects of different apatite amendments on Pb availability to sudax grass. The Pb-contaminated soil used in their study contained a total Pb concentration of 37026 mg/kg and the soil was contaminated by paint. The initial pH of the soil was 7.7 (Laperche et al., 1996). In the absence of apatite, Pb concentrations in sudax shoot tissue were as high as 170 mg Pb/kg. Different apatite treatments reduced sudax Pb concentrations to 3 mg/kg in some cases. In the present study, the Pb concentrations observed in sudax were considerably lower, possibly because of the lower total soil Pb concentrations.

Leaf tissue Pb concentrations of Swiss chard were higher compared with sudax and ranged from 1.5 to 16.2 mg/kg (Fig. 3) . The highest Pb concentration was observed for the TCR control, whereas the lowest occurred for the TSP2500 treatment with AR (Fig. 3). Treatment effects varied depending on the soil. For the AR soil, Pb concentrations in Swiss chard leaves were low, and no significant treatment effects occurred. Lead concentrations in leaves were reduced significantly with any treatment receiving TSP for the Joplin soil. The PR5000, CRYP, and PR5000 + CRYP treatments had no significant effect on Pb concentrations. For the TCR soil, all treatments receiving cryptomelane resulted in significantly lower Pb concentrations in Swiss chard compared with the control.

View larger version (46K): [in this window] [in a new window]   Fig. 3. Swiss chard leaf tissue Pb concentration for all soils. Means with the same letter are not significantly different at P < 0.05.

View larger version (24K): [in this window] [in a new window]   Fig. 4. Sudax shoot tissue concentration of (a) Cd and (b) Zn for the Joplin soil. Means with the same letter within a soil are not significantly different at P < 0.05.

Successive removal of sudax biomass substantially reduced Zn concentrations in plants (Fig. 4). The highest Zn concentrations (433 mg/kg) were observed in sudax grown on the TCR soil, which also had the highest total Zn concentration (data not shown). The addition of TSP with any treatment reduced Zn concentrations in sudax on all three soils. The addition of cryptomelane or PR alone did not change Zn concentrations compared with the control. For two out of three soils, however, the PR5000 + CRYP treatment resulted in significantly lower Zn concentrations in sudax compared with the control.

Cadmium concentrations in Swiss chard ranged from 5.6 to 29.5 mg/kg and were considerably greater than those in sudax grass (Fig. 5) . Reported Cd concentrations for Swiss chard grown on uncontaminated soils with similar soil pH values range from 0.28 to 1.8 mg/kg (Chang et al., 1987, 1997). Similar to sudax, the highest Cd concentration was observed in Swiss chard grown on the TCR soil. The addition of TSP reduced Cd concentrations in Swiss chard significantly compared with the control for all soils. In general, the addition of cryptomelane or PR did not influence Cd concentrations in Swiss chard significantly compared with the control.

View larger version (54K): [in this window] [in a new window]   Fig. 5. Swiss chard leaf tissue (a) Cd and (b) Zn concentration for all soils. Means with the same letter are not significantly different at P < 0.05.

Zinc concentrations in Swiss chard are shown in Fig. 5. These leaf Zn concentrations were considerably higher than the leaf Zn of Swiss chard grown on uncontaminated soils, which ranged from 42 to 51 mg/kg (Chang et al., 1987; Neilsen et al., 1998). Similar to sudax, additions of TSP significantly reduced Zn concentrations for two of the three soils. The addition of some soil amendments increased Zn concentrations in Swiss chard grown in the TCR material; lower soil pH for some treatments may partly be responsible (Table 2).

Some researchers have suggested the possibility of precipitation of Pb, Zn, or Cd phosphates or mixed-metal phosphates upon P addition (Nriagu, 1984; Ma et al., 1994, 1995). Chen et al. (1997) reported that the disappearance of Zn, like that of Cd, from aqueous solutions with apatite addition was due to sorption reactions rather than precipitation reactions. However, unlike Cd, removal of Zn increased as pH decreased. Moreover, they suggested that hopeite [Zn₃(PO₄)₂ · 4 (H₂O)] might precipitate only under very acidic conditions. In our previous studies, we did not observe XRD peaks that could be attributed to hopeite in P amended soils (Hettiarachchi et al., 2001). We also did not see a great influence of these treatments on soluble Zn levels in the PBET extractions (data not shown).

McKenzie (1980) reported that the affinity of cryptomelane for different metals followed the order of Pb >> Cu > Mn > Co > Zn > Ni. This indicates that Zn is not a good competitor for adsorption by cryptomelane in the presence of Pb, which may be the reason for lack of changes in plant Zn concentrations for the cryptomelane treatment.

	CONCLUSIONS

TOP NOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS REFERENCES

 
Results from this study indicate that the addition of P or/and Mn oxide significantly reduced bioavailable Pb in soils compared with the control even after plant P removal and the soil chemical changes induced by plant growth. The greatest reduction in bioavailable Pb was observed in samples treated with a combination of P and Mn oxide for all soils. Plant tissue concentrations of all three metals of interest were consistently reduced in the presence of soluble P, possibly through the formation of mixed-metal phosphates. The lower solubility of these metal phosphates could have restricted metal uptake by plants. The addition of PR and cryptomelane reduced Pb concentrations in plant tissue, and to a lesser extent Cd and Zn concentrations, possibly through enhanced sorption mechanisms.

	ACKNOWLEDGMENTS

 
The authors wish to thank Dr. Rufus Chaney, Dr. James Ryan, and Dr. David Whitney for their helpful insights in the preparation of this work; and the Kansas State University Dep. of Agronomy, Kansas Technology Enterprise Corporation, and the USEPA EPSCoR program for funding of this project.

	NOTES

TOP NOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS REFERENCES

 
G. Hettiarachchi, current address: Remediation and Containment Branch, National Risk Management Research Laboratory, USEPA, 5995 Center Hill Av., Cincinnati, OH 45224-1702. Contribution no. 00-391-J from the Kansas Agric. Exp. Stn.

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