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TECHNICAL REPORT

Heavy Metals in the Environment

Source-Separated Municipal Solid Waste Compost Application to Swiss Chard and Basil

^a Department of Plant and Animal Sciences, Nova Scotia Agricultural College, PO Box 550, Truro, NS, B2N 5E3 Canada
^b Department of Environmental Sciences, Nova Scotia Agricultural College, PO Box 550, Truro, NS, B2N 5E3 Canada

^* Corresponding author (vjeliazkov{at}nsac.ns.ca).

Received for publication March 2, 2003.

	ABSTRACT

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A growth room experiment was conducted to evaluate the bioavailability of Cu, Mn, Zn, Ca, Fe, K, Mg, P, S, As, B, Cd, Co, Cr, Hg, Mo, Na, Ni, Pb, and Se from a sandy loam soil amended with source-separated municipal solid waste (SSMSW) compost. Basil (Ocimum basilicum L.) and Swiss chard (Beta vulgaris L.) were amended with 0, 20, 40, and 60% SSMSW compost to soil (by volume) mixture. Soils and compost were sequentially extracted to fractionate Cu, Pb, and Zn into exchangeable (EXCH), iron- and manganese-oxide-bound (FeMnOX), organic-matter (OM), and structurally bound (SB) forms. Overall, in both species, the proportion of Cu, Pb, and Zn levels in different fractions followed the sequence: SB > OM >> FeMnOX > EXCH for Cu; FeMnOX = SB > OM > EXCH for Pb; and FeMnOX > SB = EXCH >> OM for Zn. Application of SSMSW compost increased soil pH and electrical conductivity (EC), and increased the concentration of Cu, Pb, and Zn in all fractions, but not EXCH Pb. Basil yields were greatest in the 20% treatment, but Swiss chard yields were greater in all compost-amended soils relative to the unamended soil. Basil plants in 20 or 40% compost treatments reached flowering earlier than plants from other treatments. Additions of SSMSW compost to soil altered basil essential oil, but basil oil was free of metals. The results from this study suggest that mature SSMSW compost with concentrations of Cu, Pb, Mo, and Zn of 311, 223, 17, and 767 mg/kg, respectively, could be used as a soil conditioner without phytotoxic effects on agricultural crops and without increasing the normal range of Cu, Pb, and Zn in crop tissue. However, the long-term effect of the accumulation of heavy metals in soils needs to be carefully considered.

Abbreviations: EC, electrical conductivity • EXCH, exchangeable fraction of metals • FeMnOX, iron- and manganese-oxide-bound fraction • OM, metals bound to organic matter • SB, structurally bound fraction • SSMSW, source-separated municipal solid waste

	INTRODUCTION

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SOURCE-SEPARATED municipal solid waste compost is a relatively new product that may have a potential for agricultural use (Epstein, 1997). Unlike most industrial composts, because of the source-separation, SSMSW compost would not normally have high concentrations of heavy metals and toxic elements (Deportes et al., 1995; Epstein et al., 1992; Epstein, 1997; Richard and Woodbury, 1992). The production of SSMSW compost in the Atlantic Provinces of Canada and around the world increased dramatically over the last few years (Barth, 2000; Hoitink, 2000), and research is needed to evaluate the agricultural value of composts as a soil amendment (Warman et al., 2002). A concern with the application of industrial composts to agricultural crops has been the high concentration of heavy metals and other toxic elements (Cook and Beyea, 1998), leading to the establishment of guidelines for maximum trace element concentrations in compost in Canada and elsewhere (Barth, 2000; Canadian Council of Ministers of the Environment, 1996; Chaney and Ryan, 1993; Epstein, 1997; Tontti and Makela-Kurtto, 2000). The elements subject to Canadian guidelines for compost quality include As, Cd, Co, Cr, Cu, Hg, Mo, Ni, Pb, Se, and Zn. Based on the concentration of the above elements, quality types of compost have been defined in Canada as Type AA and A or Type B (Canadian Council of Ministers of the Environment, 1996). The maximum permissible trace element concentrations for the two quality types are given in Table 1. Type AA and A has unrestricted agricultural use. However, a concern of researchers and operators of composting facilities is that the guidelines are based on the total rather than available amount of elements, and are difficult to meet, especially for Cu and Zn (Zheljazkov and Warman, 2000b; Zheljazkov and Warman, 2002). Hence, even SSMSW compost may have limited use in agriculture due to excessive levels of Cu, Pb, and Zn, or other elements such as Mo. Research has shown, however, that the application of industrial compost to agricultural soils may increase the total concentrations of heavy metals and other toxic elements, without increasing their phytoavailability (Drozd et al., 1999; Murillo et al., 1995; Rodd et al., 2001; Tisdell and Breslin, 1995; Warman et al., 1995). Still, reports indicate increased accumulation of some heavy metals and other elements in plants grown in soil amended with industrial composts (Warman et al., 1995).

Two crops were chosen as model plants: Swiss chard, a known metal accumulator and a good reference plant (Luo and Christie, 1998; Warman et al., 1995), and basil, an aromatic crop that is not polyploid (Ryding, 1994; Zheljazkov et al., 1996) and hypothetically would be sensitive to adverse environmental signals. Swiss chard is a well-known agricultural crop, while basil has been grown on a limited land base and in greenhouses, but it is an increasingly popular cash crop in Nova Scotia.

	MATERIALS AND METHODS

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Plant and Growth Conditions
A container experiment was conducted in an Econair Plant Growth Room GR-192 at the Nova Scotia Agricultural College using Swiss chard (cv. Fordhook Giant) and basil (cv. Italian Broadleaf). The experiment was conducted in 20-cm-diameter and 15-cm-tall plastic containers (Classic 600; Nursery Supplies, Fairless Hills, PA) in four replicates. Plants were started as seeds by placing 9 to 12 seeds in every container. After emergence the number of plants was reduced to about five seedlings per container. After a week, seedlings were then further reduced to three plants per container. Plants were grown for 10 weeks under a 14 h day and 10 h night regime, with a day temperature of 25°C and night temperature of 18°C. Plants were irrigated once every 24 h by using automatic watering drip emitters. Plastic trays were placed under each container to prevent leaching of nutrients and trace elements out of the system. Throughout the duration of the experiment, plants were fertilized weekly with 1.8 g of 20–20–20 N–P₂O₅–K₂O dissolved in 300 mL of distilled water. All basil and Swiss chard were harvested at the same time, at the beginning of blossoming of basil, by cutting at 3 to 4 cm above the soil. Half of the basil shoots (aboveground plant material) from each treatment were air-dried for extraction of the essential oils. The remaining basil and Swiss chard plants were placed in a dryer at 65°C for 3 d.

Treatments consisted of 0 (100% soil), 20, 40, and 60% compost to soil by volume. In other words, we added 175, 350, and 525 g of air-dry compost to about 3 kg of soil, resulting in 20, 40, and 60% compost to soil by volume. Constituents of growth medium in greenhouse and container production systems are usually added and/or mixed by volume, but soil amendments in field production systems are added on an area or weight basis. The results from this study are valid for both greenhouse and field production systems. We have chosen the 20 and 40% treatments by volume based on previous studies (Zheljazkov and Warman, 2003) and the usual practices under greenhouse production systems. The 60% treatment was chosen to "push the system" and observe if such a high rate would translate into phytotoxicity, or the significant accumulation of metals and other trace elements in plant tissue, or in the suppression of plant growth, development, and productivity. These application loads exceed the normal rates of compost application to agricultural land, but help to magnify investigating effects. The weight of the growth medium in each container after moisturizing and before seeding was between 2780 and 3200 g, depending on the percent of compost.

The soil used was a Pugwash sandy loam (Humo-Ferric Podzol). The SSMSW compost was from the Lunenburg Regional Recycling and Composting Facility (Nova Scotia), which was prepared in 1997, allowed to mature, and used in 1999. The in-vessel system is used at the Lunenburg Composting Facility. Feedstocks include food and yard waste, paper products, municipal sewage sludge, sawdust, bark, wood chips, and fish processing waste. At maturity, the compost had a moisture content of 60 to 65%, 11.1% C, 1.16% N, C to N ratio of 9.57, pH (H₂O) of 7.17, and an EC of 0.051 S m^–1. The C and N content of the compost were measured using a LECO (St. Joseph, MI) CNS analyzer. Compost moisture content, pH, and EC were determined in fresh compost samples. All analyses were conducted in four replicates. Compost samples were dried at 105°C in an oven for 24 h to determine the moisture content. Compost and soil pH and electrical conductivity were determined in a 1:2 compost–water extract solution (Dellavalle, 1992). Compost pH was determined using an Acumet 910 pH meter (Fisher Scientific, Hanover, NH) while the electrical conductivity was determined with a Radiometer (Copenhagen, Denmark) type CDM2e.

According to the National Standard of Canada for compost quality (Canadian Council of Ministers of the Environment, 1996), a compost could be considered mature if it meets two of the following three requirements: (i) C to N ratio of 25, (ii) oxygen uptake rate of 150 mg O₂/kg of volatile solids/h, and (iii) germination of cress (Lepidium sativum L.) seeds and radish (Raphanus sativus L.) seeds in compost of >90% of the germination rate of the control sample and a difference in the growing rate between the control sample and the plants grown in compost–soil mixture of <50%. A seed phytotoxicity test to evaluate compost maturity was conducted by using cress and marigold (Calendula officinalis L.) seeds and a direct seed test (Warman, 1999). To each petri dish, either 15 cm³ of compost or peat was added, and moistened to saturation with deionized water. A petri dish with filter paper was used as a reference control. Each treatment was conducted in five replicates with 10 seeds per petri dish. Seeds germinated for 2 to 3 d, plantlets were left to grow for one week, and heights were recorded.

Trace Element Analysis
Plants were oven-dried at 65°C for 72 h following the harvest. The weight of dry matter was recorded and samples were ground with a Wiley mill to pass a 1.0-mm screen. Soil samples were taken immediately after the harvest; half of each soil sample was air-dried at 20°C, and the other half was oven-dried at 65°C for 72 h and ground to pass 2.0-mm screen. Plant, soil, and air-dry compost samples (4 g of subsample in 250-mL digestion tubes) were digested in concentrated nitric acid (Zheljazkov and Warman, 2002). For the analysis of As, Hg, and Se, half of the HNO₃–digested sample was transferred into a digestion tube and boiled at 100°C until the sample volume was reduced to 5 mL. After that, 5 mL of 6 M HCl were added, and the sample was left on the digestion block for another 18 min, then cooled to room temperature and quantitatively transferred to a 25 mL volumetric flask and made up to volume with 6 M HCl. The remaining half of the HNO₃ digested samples were analyzed for nitric acid–extractable (pseudo-total) concentrations of Cu, Mn, Zn, Ca, Fe, K, Mg, P, S, B, Cd, Co, Cr, Mo, Na, and Ni by inductively coupled argon plasma spectrometry (ICAP Model 61, with simultaneous vacuum spectrometer, gas argon, and fixed cross flow nebulizer; Thermo Elemental, Franklin, MA).

Sequential Extraction
Metal fractionation of Cu, Pb, and Zn was conducted by using the Community Bureau of Reference (BCR) protocol (Quevauviller et al., 1994) recommended by the BCR of the Commission of European Communities. This particular procedure was developed to harmonize the methodology for leaching-extraction steps for soils and sediments (Chwastowska and Sterlinska, 2000; Quevauviller et al., 1994; Ure et al., 1993). This is a three-step procedure that includes acetic acid (0.11 mol L^–1), hydroxylamine chloride (0.1 mol L^–1) and hydrogen peroxide (8.8 mol L^–1), and ammonium acetate (1 mol L^–1). The residue remaining after Step 3 was digested in aqua regia, a procedure recommended by the International Organization for Standardization (International Organization for Standardization, 1995; Vercoutere et al., 1995). In addition, soil samples were digested in aqua regia to determine the percentage of recovery of the sequential extraction relative to the aqua regia–extractable Cu, Pb, and Zn. The sequential extraction procedure steps assume that the following chemical forms of metals exist in soils and are respectively recovered by each of the steps: (i) water-soluble, exchangeable, and weakly bound to OM, (ii) occluded in Fe or Mn oxides, (iii) organically bound and sulfides, and (iv) structurally bound (residual fraction recovered with aqua regia). We have chosen to fractionate the above three elements since the concentrations of Cu, Pb, and Zn in the SSMSW compost were higher than maximum permissible levels for these elements in Compost Type AA and A, but within the limits of compost Type B established by the Canadian Council of Ministers of the Environment (1996) (Table 1). The Mo content of the SSMSW compost was also higher than the maximum permissible level for Mo in AA and A compost types. The sequential extraction procedure outlined above and the sequential extraction procedure of Luo and Christie (1998) did not separate Mo very well (data not shown).

All extraction steps were performed in 250-mL polypropylene centrifuge tubes with screw caps. The sample size was 2.5 g of soil. The extraction was performed by shaking in a mechanical, end-over-end shaker at a speed of 300 rpm and at a room temperature of 22 ± 2°C. The chemical fractions were operationally defined as followed:

• Exchangeable fraction of metals (EXCH): 100 mL of 0.11 mol L^–1 acetic acid was added to the samples (2.5 g). The samples were shaken for 16 h at room temperature of 22 ± 2°C (overnight) and centrifuged at 1500 x g for 20 min, and the supernatant was filtered through no. 41 Whatman (Maidstone, UK) filter paper and stored in a refrigerator at 4°C for analysis. The residue was washed by adding 50 mL of deionized water, shaken for 15 min on the end-over-end shaker, and centrifuged for 20 min at 1500 x g. The supernatant was decanted and discarded, taking care not to discard any of the solid residues. Conservation of extract was made by adding 1 mL of concentrated HNO₃.
  
• Metals from reducible iron and manganese bound fraction (FeMnOx): 100 mL of 0.5 mol L^–1 hydroxylammonium chloride (hydroxylamine hydrochloride) were added to sample residues from Step 1. The samples were resuspended by manual shaking and then extracted by mechanical shaking for 16 h at room temperature of 22 ± 2°C (overnight) and centrifuged at 1500 x g for 20 min, and the supernatant was filtered through no. 41 Whatman filter paper and stored in a refrigerator at 4°C for analysis. Then the samples were washed as indicated above.
  
• Metals bound to organic matter and sulfides (OM): 25 mL of 8.8 mol L^–1 hydrogen peroxide in small aliquots were added carefully (to avoid losses due to violent reaction) to the residue from Step 2. The vessels were loosely covered with the caps and the samples were digested at room temperature of 22 ± 2°C for 1 h with occasional manual shaking. Digestion was continued for 1 h at 85 ± 5°C in a water bath. The volume was further reduced to 3 mL by further heating of uncovered vessels. Further aliquots of 25 mL were added to the samples. Covered vessels were heated again at 85 ± 5°C in a water bath and digested for 1 h. After that, the vessels were uncovered and the volume reduced to around 1 mL. One-hundred milliliters of 1.0 mol L^–1 ammonium acetate were added to the cool wet residues and the samples were shaken for 16 h at 22 ± 2°C (overnight). The extract was separated from the solid residue by centrifugation and decantation as in Step 1 and further stored in a refrigerator for analysis.
  
• Structurally bound (SB) or residual fraction recovered with aqua regia: the soil samples from Step 3 were transferred to 250-mL Pyrex digestion tubes. The pre-digestion step was performed at room temperature (at 22 ± 2°C) for 16 h in 28 mL of 37% HCl–70% HNO₃ mixture. The suspension was digested at 130°C for 2 h using a reflux condenser. Samples were filtered through Whatman 41 filter, diluted to 50 mL with 0.5 mol L^–1 HNO₃, and stored in refrigerator for analyses.
  
• Aqua regia extraction of soil samples using 3 g of soil and the same digestion procedure as in Step 4: Soil samples from all treatments were digested in aqua regia to estimate the total amount of Cu, Pb, or Zn recovered from all four steps, relative to the total amount of these metals as determined by aqua regia.
  

Samples from the sequential extraction were analyzed using a Varian (Palo Alto, CA) Spectra AA-20 atomic absorption spectrophotometer (AAS) due to the necessity for using different standards for each step of the sequential extraction and the better sensitivity and detection limits of AAS compared with inductively coupled plasma (ICP). To avoid possible interferences of matrices, for each of the extraction steps as well for the aqua regia and nitric acid digestions, separate standards were prepared using the same matrices as the samples from a particular step. Arsenic, Hg, and Se in the HNO₃–digested and HCl-reduced soil and tissue samples were analyzed using a Varian vapor generation accessory (VGA-76) for a Varian Spectra AA-20 AAS. Flame absorption was used for As and Se, while the cold vapor technique was used for Hg (Varian Operation Manual, 1984). The sodium borohydride solution and HCl for As and Se were 0.6% NaBH₄ in 0.5% NaOH and 6 M HCl in the acid container, while for Hg 0.3% NaBH₄ in 0.5% NaOH and 5 M HCl were used. The above conditions are recommended in the instrument's manual by Varian (Varian Operation Manual, 1984).

Essential Oil Analysis
The basil oil content was established in air-dry herbage. Four-hundred grams of dried plant material (leaves, flowers, and stems) were put in 2-L round-bottom flasks and steam-distilled for 3 h in a Clevenger-type apparatus (Craker and Dinda, 1998; Topalov and Zheljazkov, 1991) from Quickfit (England), using our own steam generation unit. The isolated oil was measured and stored at –80°C until further analyses. The essential oil was prepared for gas chromatograph (GC) analyses by dilution of 0.05 mL of oil into 0.95 mL of GC standard-grade hexane and the samples were analyzed on GC the same day. The GC was a Varian 6500 system with a flame ionization detector, nitrogen as a carrier gas, and a flow rate 12 mL/min. The GC was fitted with a J&W Scientific (Folsom, CA) DB-5 column (30 m x 0.53 µm, film thickness = 0.5 µm). The injection sample was 1 µL. The column oven was temperature programmed as follows: 15 min at 50°C, 10 min at 60°C at 2°C/min, and 2 min at 180°C at 10°C/min.

Data analysis of all data sets was performed using two-way analysis of variance (ANOVA) with SAS (SAS Institute, 2000); where the interactions or main effects were found significant, Duncan's test was performed. Constant variance and normality of residuals were tested and some transformations were necessary for the normal distribution of residuals.

	RESULTS AND DISCUSSION

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The seed germination phytotoxicity test did not indicate any suppressing effect of the SSMSW compost on seeds relative to the peat and water controls. This result is not surprising, as the compost used in the experiment was produced in 1997 and had been maturing for two years. Within a treatment, the soil pH at harvest in containers with basil was lower than the pH in the containers with chard, indicating the effect of the plants on pH (Table 2). Within plant species, the increased application of SSMSW compost increased pH, an effect that is due to the higher pH of the compost relative to the soil. As a result, with both plant species, the pH of the unamended soil was lower than the pH of the soil amended with compost. From a practical point of view, one of the possible benefits of the application of SSMSW compost to the mostly acid soils in Nova Scotia would be a reduced need for lime application. The final soil electrical conductivity may also have been influenced by the plant species and compost application. In general, with increased amount of compost application, EC increased. It is assumed that the relatively high EC in all pots was due to the weekly fertilizer application.

Although this particular SSMSW compost had relatively high concentrations of Cu, Pb, Mo, and Zn (Table 1), 20% compost application to the soil had a beneficial effect on the final yields of both basil and Swiss chard. In a field experiment with barley and wheat using similar SSMSW compost, Rodd et al. (2001) also found that compost addition increased grain yields relative to the unamended soil. In a similar container experiment, Warman et al. (1995) reported a yield increase for Swiss chard with increasing additions of biosolids composts to sandy loam soils. Other researchers also reported greater yields in compost-amended soils (Murillo et al., 1995; Sebastiao et al., 2000; Sicora et al., 1980).

Fractionation of Copper, Lead, and Zinc
Fractionation of Cu, Pb, and Zn as a function of treatments is shown in Table 3. Significant interactions were found between crop and compost rate for Cu, Pb, and Zn.

Increasing the proportion of compost in the soil resulted in an increase in tissue Cu content of basil from the compost treatments, from around 6.4 in the unamended to 9.8 mg/kg in the 40% treatment. Tissue Cu in basil in the 20, 40, and 60% treatments remained at the same level. Addition of 20% compost to the soil increased tissue Cu in Swiss chard nearly twofold relative to the unamended soil, but a further addition of 40 or 60% compost resulted in slight decrease in tissue Cu, still significantly greater than in the unamended soil. Overall, both plant species contained similar amounts of Cu; however, because of the greater yields, the overall Cu accumulation in Swiss chard was much greater than Cu accumulation in basil shoots. Warman et al. (1995) reported no changes in tissue Cu of Swiss chard grown in biosolids compost–amended soils.

Lead
Lead distribution in unamended soils followed the sequence SB >> FeMnOx = OM = EXCH. Overall, Pb distribution in all treatments containing the two plants was in the following sequence: FeMnOx = SB > OM > EXCH. The addition of compost to the soil did not increase EXCH Pb but increased FeMnOx Pb in all treatments, OM Pb only in the 60% treatment, and SB Pb in the 40 or 60% treatments. Lead levels in the 60% treatments were increased by 7 to 10, 5, and 2 times, respectively, in the FeMnOx, OM, and SB fractions, relative to Pb fractions in unamended soils. These results are in accordance with the general understanding of very low mobility of Pb and the high affinity of Pb to Mn oxides, Fe and Al hydroxides, clay minerals, and organic matter (Kabata-Pendias and Pendias, 1991). The addition of 60% compost to soil resulted in four-times-greater levels of aqua regia (AR)–extractable Pb relative to unamended soil. Tissue Pb in both crops in all treatments was below the detection limit of the atomic absorption spectrophotometer, suggesting that SSMSW compost that does not meet the Pb regulatory limits of Type AA and A compost may be safely applied to agricultural soils without risk for increased accumulation of Pb in plant tissue.

Zinc
Zinc distribution in the unamended soil was in the following order: SB >> OM > FeMnOX = EXCH. Zinc in the EXCH and in the FeMnOX fraction of the unamended soil was below 0.1 mg/L in the sample solution (our lowest standard). Addition of 60% SSMSW compost increased EXCH Zn and FeMnOX Zn in both basil and chard containers almost three- and sixfold, respectively, relative to Zn levels in the 20% treatment. The OM Zn in the 60% treatment increased by more than 2.5 times, while SB Zn in the 60% treatment was increased only by 1.2 to 1.5 times relative to the respective fractions in the unamended soil. Overall, distribution of Zn in different fractions of treated soils followed the sequence: FeMnOX > SB = EXCH >> OM. Aqua regia–extractable Zn levels of the unamended soil were 42 mg/kg while in the 60% treatment it reached 250 mg/kg, six times more than the aqua regia–extractable Zn in unamended soil. Tissue Zn of both basil and Swiss chard in the 60% treatment was double the amount in the unamended plants, with both plants containing similar amounts. The overall Zn accumulation in basil shoots, however, was much less than the Zn accumulation in Swiss chard shoots, due to the differences in DM yields between the two species. Warman et al. (1995) reported an increase in tissue Zn of Swiss chard grown in biosolids compost–amended soils.

Except for the 20% compost treatment, the largest Zn fraction in the compost-amended soils was FeMnOx Zn, which is in agreement with the reports from other authors (Luo and Christie, 1998; Shuman, 1999). It is generally accepted that Zn has relatively high affinity for sorption on the surfaces of Fe and Mn oxides, especially with an increase of soil pH (Burnham et al., 1992; Luo and Christie, 1998; Shuman, 1975). Shuman (1999) reported that spent mushroom compost and humic acids (HA) could redistribute Zn from EXCH to less bioavailable forms. The EXCH Zn in the SSMSW-amended soils increased with an increase in percent compost addition. In addition, this particular fraction was relatively large, which does not conform to the results of Luo and Christie (1998), who did not find detectable levels of Zn in the EXCH fraction.

The recovery (the sum of the elemental concentrations from all four steps) of Cu, Pb, and Zn with the BCR procedure compared with the levels of these elements extracted with aqua regia were 86 to 134% for Cu, 118 to 136% for Pb, and 73 to 122% for Zn (Table 3). Some authors (Chwastowska and Sterlinska, 2000) reported better levels of recovery, others detected significant variation in percent recovery (Davidson et al., 1998). Also, our results support the notion that although the BCR sequential extraction may be suitable for separating various geochemical fractions in soils (Ho and Evans, 2000; Davidson et al., 1998), it cannot predict the accumulation of heavy metals in plant tissue since redistribution of some metals may occur (Ho and Evans, 2000).

Even though addition of SSMSW compost increased bioavailable forms of Cu and Zn in the soil as well as tissue Cu and Zn in both crops, these elements were within their normal range in plants, and below the values for their critical concentration in tissue (reviewed in Kabata-Pendias and Pendias, 1991). In a similar study, Warman et al. (1995) reported that the addition of biosolids compost, which is high in some heavy metals, increased soil Zn and Cu and tissue Zn, but had no effect on tissue Cu, Co, Ni, or Pb of Swiss chard. In a container experiment with tomatoes (Lycopersicon esculentum Mill.) grown in 100% soil, 100% MSW compost, or in 50% soil–50% compost by volume, Warman (2001) did not find differences among treatments in leaf tissue Cd, Co, Cr, Ni, and Pb. Besides, the addition of 50% of compost to soil did not increase tissue Cu and Zn relative to the unamended soil, although the MSW compost contained 259 mg/kg Cu and 573 mg/kg Zn (Warman, 2001). Murillo et al. (1995), who conducted field experiments with ryegrass (Lolium perenne L.) and low-quality urban compost, with high content of heavy metals, reported that the application of 48 Mg/ha did not increase tissue Cu or Zn. It was concluded, therefore, that mature urban composts even with high content of Cu and Zn can be safely used as organic fertilizers, although long-term effects of accumulation of heavy metals in the soil need to be carefully considered. Our results also suggest that SSMSW compost application may result in significant increase in EXCH Cu or Zn in the soil.

Regression analyses of the data on Cu and Zn content in soil and plant tissue revealed that the EXCH fraction explains very little of the variability in tissue Zn in basil and 38% of the tissue variability in chard (Table 4). Hence, predicting tissue concentration of Cu, Zn, and other elements based on the exchangeable fractions of these metals in soils may be difficult. Aqua regia–extractable metals in soil explained part of the variability in tissue Cu in basil. Interestingly, nitric acid–extractable metals in soil explained a significant part of the variability in tissue Cu in basil. Zheljazkov and Nielsen (1996a) found good relationship between soil HNO₃–extractable and tissue concentration of Cd, Cu, Pb, and Zn. Using romaine lettuce (Lactuca sativa L.), Sloan et al. (1997) also reported significant R² coefficients (0.88, 0.31, 0.41; significant at the 0.05 probability level) for Cd, Cu, and Zn concentrations, respectively, of aboveground lettuce tissue as a function of the total metal concentrations in the soils. In field experiments with catnip (Nepeta transcaucasica Grossh.) grown on metal-polluted soils, Zheljazkov and Warman (2000a) found greater values for these coefficients (R² tissue metal/HNO₃ extracted metal in the soil), a result that may be due to differences in the experimental conditions (soils and plants species). With the exception of soil Cu in basil pots, aqua regia–extractable Cu or Zn in soils did not correlate well to tissue concentrations of these metals.

Cadmium, Co, Cr, Ni, and Pb in the tissue of both plant species from all treatments were below the detection limits of ICP, although the amount of Cd, Cu, Mo, Pb, and Zn in the SSMSW exceeded regulatory limits for Type AA and A compost (Canadian Council of Ministers of the Environment, 1996). Additions of SSMSW to soil resulted in an increased accumulation of Mo in chard but not in basil. Although the addition of SSMSW compost to the soil resulted in a 10-fold increase of HNO₃–extractable Pb, no Pb was found in the tissue of either plant, indicating that Pb was in a nonavailable form, confirming the findings of other authors (Drozd et al., 1999; Gigliotti et al., 1996; Kabata-Pendias and Pendias, 1991). In field experiments, Drozd et al. (1999) found that the application of 30, 60, and 120 Mg/ha MSW compost did not increase Pb content in lettuce despite the relatively high Pb concentration in the applied compost (530 mg/kg).

Probably one of the reasons for the lack of Cd accumulation in plants was the relatively high Zn content of our SSMSW compost. Chaney and Ryan (1993) suggested that Zn in composts might reduce the bioavailability of Cd. In our experiment, increased accumulation of some metals in basil and chard grown on SSMSW-amended soils may have been influenced by increased salt concentrations in these treatments, reflecting the higher EC. Bucher and Schenk (1999) have shown that addition of KCl and MgCl₂ increased phytoavailability of Cd, Cu, Zn, and Mn. Still, in plant tissue from all the treatments, no element was found to be deficient or toxic for plants (Kabata-Pendias and Pendias, 1991).

Effect of Treatments on Essential Oil Composition and Metal Content
Basil essential oil composition changed as a result of the treatments (Fig. 1 and Table 6). The content of linalool (the major compound in basil oil) was greater in the unamended soil or in the 20% treatment, lower in the 40%, and the lowest in the 60% treatment. The content of 1,8-cineole was greater in the oil from the 20% treatment. The content of -terpineol was greater in the 40 or 60% treatments, lower in the unamended soil, and the lowest in the 20% treatment. The content of other oil constituents varied without a clear trend. Heavy metals (Cu, Cd, Pb, and Zn) in the basil oil from all treatments were below the detection limit of the atomic absorption spectrophotometer (below 0.25, 0.06, 0.62 and 0.25 mg/L, respectively). These results confirm the understanding that high heavy metal concentrations in the growth medium may increase metal accumulation in plant tissue, but not in the essential oil, which is the final marketable product (Scora and Chang, 1997; Zheljazkov and Nielsen, 1996a, 1996b). These results imply that basil could be grown as an essential oil crop in soils amended with high rates of MSW compost without the risk of contamination of the end product, the essential oil. Differences in the essential oil constituents (1,8-cineole, linalool, and -terpineol) between the treatments might be related to the compost application. Research has shown that essential oil composition of aromatic plants may vary significantly depending on environmental and genetic factors that influence genetic expression (Bernath, 1986; Charles and Simon, 1990). Previous research has indicated that elevated concentrations of heavy metals did not change oil constituents of peppermint (Mentha x piperita L.) (Scora and Chang, 1997; Zheljazkov and Nielsen, 1996a). Although peppermint and basil belong to the same family, essential oil synthesis and accumulation may be affected unequally as a result of high heavy metals in the growth medium. The current understanding is that secondary metabolites in plants function as defense compounds; however, secondary metabolites may have multiple functions as well (Harborne, 1999; Wink, 1999). Research has demonstrated that adverse environmental conditions may change essential oil constituents (Bernath, 1986). Thus, it is difficult to speculate on whether high heavy metals in the compost, changes in the concentrations of other elements, pH, or EC were responsible for the above alteration in oil composition. More research is needed to see how different heavy metals would affect oil synthesis, accumulation, and quality.

View larger version (15K): [in this window] [in a new window]   Fig. 1. Gas chromatograms of basil essential oil from the unamended soil (above) and the 60% compost treatment (below). 1, 1,8-Cineole; 2, linalool; 3, camphor; 4, -terpineol; 5, bornyl acetate; and 6, ß-caryophyllene.

As indicated earlier, SSMSW composts are more benign to the environment than nonseparated MSW composts or the uncomposted biosolids (municipal sewage sludge). Findings of other authors and the results from this study indicate that mature SSMSW compost with relatively high concentrations of Cu, Pb, Mo, and Zn (311, 223, 17, and 767 mg/kg respectively) may be used as a soil amendment on agricultural crops without a risk for phytotoxicity, or risk of increasing normal range of Cu, Pb, and Zn in crop tissue. Our results suggest a need to reassess current regulatory levels for Cu, Pb, and Zn in compost. Such reassessment must include consideration of metal accumulation from repeated applications, long-term bioavailability of metals, and effects on other environmental endpoints. Although this study focused on the effects of high loading rates of heavy metal in tissues, we have to remark that this is not the only parameter against which environmental sustainability needs to be judged. The problem of the soil acting as a "sink" and the distribution of heavy metals among various soil pools ought to be considered in the long run, thereby potentially affecting uptake of plants, soil biology, and biochemistry.

Our results have relevance to container-grown plants (where soil conditioners are added by volume) and to field crop production systems (where soil conditioners are added by weight). The 20% by volume treatment is equivalent to the application of 200 Mg/ha of air-dry compost in a field production system. Such extreme rates are not reasonable. The addition of SSMSW compost to agricultural soils and/or to container growth mediums may have beneficial effects on crop development and yields and on soil pH. We found that basil is a more suitable plant for evaluation of possible adverse affects of compost on plants than Swiss chard, since high compost additions affected basil development. Besides, basil yields in the 40 and 60% compost treatments did not increase relative to yields in the unamended soils. Further research is needed to evaluate the effect of SSMSW compost to plants from other families and to other soil types.

	ACKNOWLEDGMENTS

 
This work was partially supported by a Natural Sciences and Engineering Research Council of Canada (NSERC) grant awarded to P.R. Warman and by AgriFutures Nova Scotia Grant 190 awarded to V.D. Zheljazkov. We would like to thank Scott Savoy and Paul McNeil for their assistance in the laboratory.

	REFERENCES

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