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a Dep. of Soil, Water, and Environmental Science, Univ. of Arizona, 429 Shantz Building #38, Tucson, AZ 85721-0038
b Environmental Research Lab., 2601 E. Airport Drive, Tucson, AZ 85706
* Corresponding author (rmaier{at}ag.arizona.edu)
Received for publication May 17, 2006.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONREFERENCES |
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106 CFU g–1 dry tailings) and dominated the rhizosphere. Therefore, with compost amendment, quailbush has good potential as a native species candidate for phytostabilization of mine tailings in semiarid environments.
Abbreviations: BNM, basal nutrient medium • CC, compost control • CEC, cation exchange capacity • CFU, colony forming units • DTPA, diethylenetriaminepentaacetic acid • EC, electrical conductivity • ICP–MS, inductively coupled plasma mass spectrometry • MPN, most probable number • MSM, minimal salts medium • OS, off-site control sample • SBRP-HIC, Superfund Basic Research Program-Hazard Identification Core • SPL, soil plant toxicity level • SRL, soil remediation level • TOC, total organic carbon • TRTMT, treatment • Tukey's HSD, Tukey's Honestly Significant difference • WQARF, Water Quality Assurance Revolving Fund • WQC, Water Quality Center
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONREFERENCES |
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The establishment of a permanent vegetative cap is recognized as a potentially cost-effective and ecologically sound approach to containment of mine tailings and for initiation of soil formation processes (Munshower, 1993; Brooks, 1998). In particular, there is interest in phytostabilization, a process wherein plants are established and function primarily to accumulate metals into root tissue or aid in their precipitation in the root zone (Cunningham et al., 1995). Use of native plants is a focus of this technology because they often demonstrate tolerance for local environmental conditions and provide a foundation for natural ecological succession. One of the largest cost factors associated with revegetation is the requirement for large amounts of organic amendments, e.g., compost or biosolids. These amendments mitigate the toxicity of the tailings and plants fail to grow in their absence (Sabey et al., 1990; Ye et al., 2001; Brown et al., 2003).
In this study we evaluated quailbush [Atriplex lentiformis (Torr.) S. Wats.]for its ability to establish in extremely and moderately acidic lead-zinc mine tailings typically found in semiarid areas. Quailbush is a perennial halophytic subshrub that is native to Arizona, California, Nevada, and Utah (USDA-NRCS, 2005) and has been examined for use in the reclamation of salt-affected lands (Malik et al., 1991; Blank et al., 1998; Malcolm et al., 2003). Quailbush is considered drought-tolerant and has previously been observed encroaching into historical mine tailings sites (USDA-SCS, 1977; Booth et al., 1999; Arunachalam et al., 2004; Jefferson, 2004). In addition, Atriplex spp. have demonstrated accumulation of metals primarily in the roots, which is favorable for phytostabilization strategies (Williams et al., 1994; Jordan et al., 2002). The objectives of this study were to determine (i) the minimum level of compost required for establishment of quailbush in lead-zinc tailings by evaluating seed germination and seedling growth; (ii) metal accumulation in shoot tissue during growth of quailbush; and (iii) the impact of plant establishment on the microbial community as measured by enumeration of autotrophic and heterotrophic bacterial community before and after planting.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONREFERENCES |
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Sampling
Two samples (80 L) were collected from the Klondyke upper tailings pile: K4 from 28 to 53 cm below the surface (32°51'0'' N; 110°20'34'' W) and K6 from 21 to 42 cm (35°51'1'' N; 110°20'33'' W). An off-site control sample (OS) was taken from 17 to 28 cm below the surface of a vegetated area adjacent to the tailings pile at 32°51'3'' N and 110°20'32'' W. The compost (EKO Compost, Richland Turf Food, Plateville, CO) used in this study was a mixture of poultry manure, forest products, and recycled wood products. All materials were stored at 4°C and thoroughly mixed before use. The off-site control sample and compost were sieved with a 5 x 5 mm mesh screen.
Mine Tailings and Compost Analysis
For pH analysis, triplicate samples were air-dried for 2 d and sieved through a 2-mm mesh screen. A 10-g aliquot was placed into a 50-mL centrifuge tube and 20 mL deionized water was added to achieve a 2:1 ratio of deionized water to soil (v/w). Each solution was shaken for 1 h, centrifuged for 5 min at 15 000 x g, and the pH of the supernatant was determined. Plant-available metals were analyzed using a DTPA (diethylenetriaminepentaacetic acid) extracting solution as described by Lindsay and Norvell (1978). The DTPA extraction was chosen based on its effective chelation of a mixture of plant micronutrients such as Fe, Zn, Cu, and Mn. In triplicate, an air-dried 10-g aliquot of each sample was mixed with 20 mL of DTPA extracting solution at pH 7.3. The solution was shaken in a 125-mL flask at 150 rpm for 2 h, vacuum filtered through a Whatman no. 42 filter paper, and finally filtered through a 0.45-µm hydrophilic polyethersulfone membrane (Supor-450, Pall Life Sciences, East Hills, NY). Samples were analyzed by inductively coupled plasma mass spectrometry (ICP–MS) for As, Cd, Cu, Fe, Mn, Pb, and Zn by The University of Arizona Superfund Basic Research Program's Hazard Identification Core (SBRP-HIC) using USEPA Method 6020 (USEPA, 2004). For the remaining analyses, single composite samples of K4, K6, OS, and compost were oven-dried at 105°C and sieved through a 2-mm mesh screen. These samples were then analyzed for texture by the hydrometer method; electrical conductivity (EC; 1:1 H2O extraction); cation exchange capacity (CEC) by the sodium acetate method (Chapman, 1965); plant-available PO4–P by the ammonium bicarbonate method (Olsen et al., 1954); total organic carbon (TOC), total carbon, and total nitrogen by high temperature combustion; and total elements (As, Cd, Cu, Fe, K, Mn, Na, Pb, Zn). These analyses were conducted by the Water Quality Center (WQC) Laboratory (University of Arizona, Tucson, AZ) except the total elemental analysis for which samples were prepared by microwave acid digestion (EPA 3051; USEPA, 2004) by the WQC Laboratory and then analyzed by ICP–MS by the SBRP-HIC. For the compost sample the C/N ratio and total nitrogen values were provided by Richland Turf Food, and used to calculate the TOC.
Germination and Plant Growth Study
Two experiments were performed to determine the minimum amount of compost required for growth of quailbush. Compost was selected to serve as a slow-release fertilizer and an organic amendment for both reduction of metal bioavailability and enhancement of heterotrophic microbial growth. Quailbush was selected because Atriplex spp. have performed well in disturbed and contaminated sites (Williams et al., 1994; Booth et al., 1999; Jordan et al., 2002; Arunachalam et al., 2004; Jefferson, 2004), it is native to the area as well as salt-tolerant (Blank et al., 1998; USDA-NRCS, 2005), and it performed similarly or better compared with other native species in a preliminary screening study.
In the first experiment, seed germination and plant growth were examined in four K4 and K6 tailings-compost mixtures (25, 50, 75, and 100% tailings by mass). Results of this study indicated equally good germination and growth of quailbush at all three compost levels tested. Therefore, a second experiment was performed to further titrate the level of compost required. In this experiment seed germination and plant growth were determined in five K4 and K6 tailings-compost mixtures (75, 85, 90, 95, and 100% tailings), as well as compost (100% compost control, CC) and the off-site sample (100% OS) alone.
For each experiment, quailbush seeds (Mistletoe-Carter Wholesale Seeds, Goleta, CA, USA) were sown in 12 x 8.5 x 3 cm plastic pots (with six 1.6-mm drainage holes) containing the various tailings or control treatments. Each treatment contained five replicates with 20 seeds per replicate (100 seeds per treatment). Seeds were irrigated with approximately 84 mL of tap water d–1 in a fiberglass greenhouse with temperatures ranging from 24 to 38°C. On Day 23, germination was quantified, and seedlings of similar size were transferred into 3.8-L pots (15.2 cm top diameter x 17.8 cm height x 12.7 cm bottom diameter) lined with fiberglass screen and containing the same tailings or control treatment. Fiberglass screen material prevented tailings from leaking and allowed water to drain. All pots were prepared and wetted 3 d before seedling transfer. Following transplantation, pots were irrigated with 360 mL of tap water d–1. Each treatment was comprised of five replicates with one plant per pot. During the study, seedling height, number of leaves, and basal diameter of each plant were measured every 7 d. Plants were harvested 68 d after transplantation (Day 91 of the experiment) for determination of shoot and root dry mass and metal content.
Plant Dry Mass and Metal Analysis
At the end of the experiment (Day 91), plants were harvested for shoot and root dry mass measurements. The shoots were separated from the roots and placed in a preweighed paper bag. Root tissues were washed with tap water followed by a thorough rinse with distilled water to remove soil and particulate matter and then blotted with a paper towel and wrapped in a preweighed piece of aluminum foil. All samples were dried in a forced air oven at 65°C and weighed after 3 d to obtain the shoot and root dry mass.
Quailbush shoot tissue was analyzed for total metal (Na, K, Mn, Fe, Cu, Zn, As, Cd, and Pb) concentrations. Three plants from each treatment were selected for metal analysis. Plant material was dried at 65°C, ground with a Wiley Mill, and passed through a 40-mesh (0.419 mm) screen. Shoot tissue was prepared by microwave acid digestion by the WQC Lab and analyzed by ICP–MS by the SBRP-HIC.
Enumeration of Heterotrophic Bacteria
Initial (before seed germination) and final (post-harvest) heterotrophic bacterial counts were measured for all treatments. Ten grams of each treatment were placed in a 250-mL jar containing 95 mL of Zwittergent extractant (8.5 g NaCl and 200 µL of 1% Zwittergent solution per liter), shaken vigorously for 2 min, serially diluted in triplicate, and then plated on R2A agar (Becton, Dickinson and Company, Sparks, MD) amended with 200 mg L–1 of cycloheximide to inhibit fungal growth. Plates were incubated for 5 d at 23°C and then enumerated. Counts are reported as colony forming units (CFU) per gram dry weight of each sample.
For planted treatments, heterotrophic bacterial counts were also performed on rhizosphere samples at the end of the experiment. Three plants from each treatment were removed from the pots and all loose soil or tailings material was shaken off the roots. Roots along with adhering soil were immediately stored at 4°C until processed. For each plant, 0.1 g of fresh root material was consolidated from three separate 2-cm root tip sections, 0.5 cm of the root-shoot transition region, and 1.5 cm of the main root axis. The roots were placed in 9.9 mL of 1X PBS, sonicated twice for 30 s, and serially diluted in 1X PBS (Ausubel et al., 1995). All treatments were plated in triplicate on R2A agar amended with 200 mg L–1 of cycloheximide, incubated for 5 d at 23°C, and enumerated.
Enumeration of Autotrophic Bacteria
Initial and final counts of autotrophic bacteria, specifically iron- and sulfur-oxidizing bacteria, were assessed using a modification of the most probable number technique (Cochran, 1950; Woomer, 1994). Ten-gram samples of each treatment were placed into 250-mL jars containing 95 mL of Zwittergent extractant and shaken vigorously for 2 min. Each slurry was serially diluted from 10–2 to 10–8 in 4.5 mL with five replicates for each dilution. For the rhizosphere samples, the initial 10–1 dilution for each plant within a treatment was consolidated and serially diluted from 10–3 to 10–6 in 4.5 mL with five replicates for each dilution. All samples were inoculated into both iron and sulfur oxidizer enrichment media. Iron oxidizers were grown in modified 9K minimal salts medium (MSM) containing per liter: 3.0 g (NH4)2SO4, 0.1 g KCl, 0.5 g K2HPO4, 0.5 g MgSO4·7H2O, 0.01 g Ca(NO3)2·4H2O, and adjusted to a pH of 2.3 with 10 N H2SO4. The autoclaved 9K MSM was amended with filter-sterilized FeSO4·7H2O at a final concentration of 33.3 g L–1 (Silverman and Lundgren, 1959; Southam and Beveridge, 1992). Sulfur oxidizers were grown in modified Starkey's medium (pH 4.5) consisting of a basal nutrient medium (BNM) and a thiosulfate solution (Starkey, 1925; Knickerbocker et al., 2000). The BNM (900 mL) contained 0.3 g of (NH4)2SO4, 3.5 g of KH2PO4, 0.5 g of MgSO4·7H2O, 0.33 g of CaCl2·2H2O, and 180 µL of a 1% solution of FeSO4·7H2O adjusted to pH 2.3 with H2SO4. A 100-mL solution of sodium thiosulfate with 200 mM Na2SO3 (20 mM Na2SO3 L–1) was autoclaved separately and added to the BNM.
After 47 d of incubation on a shaker at 180 rpm, positive and negative results for growth were documented. Positive results were based on a color change from yellow to orange for the iron oxidizers and a change in turbidity as well as decrease in pH for the sulfur oxidizers. Population estimates were calculated as described by Briones and Reichardt (1999) and reported as most probable number (MPN) g–1.
Statistics
Statistical analyses were generated using SAS Version 9.0 of the SAS System for Windows (SAS Institute, 2002). All data were tested for normality. For cases of nonhomogeneity of variances, data were log-transformed before analyses. Due to plant mortality within some of the treatments, the procedure for unequal sample size was used. The effect of compost addition on mean pH was examined within each mine tailings sample by employing a one-way ANOVA. For plant shoot metal concentrations, values were averaged over all treatments within a sample source and analyzed by a one-way ANOVA. Significant factor effects for both sample source and mine tailings concentration were determined using a two-way ANOVA followed by a one-way ANOVA to compare means for plant growth and microbial counts. For all analyses, significant differences between means at the p < 0.05 level were determined by employing the Tukey's studentized range test (Tukey's Honestly Significant Difference [Tukey's HSD]).
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RESULTS |
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Plant Growth and Dry Mass
Following germination, five seedlings of similar size from each treatment were transplanted into larger pots containing the same treatment and evaluated for plant growth. Results for mean height, mean number of leaves, and mean basal diameter (data not shown) were similar, collectively demonstrating that the mine tailings alone treatment significantly reduced the growth of quailbush (F4, 40 > 16, p < 0.0001). In fact, all plants in the K4–100 treatment died 2 wk after being transplanted, while plants were severely stunted in the K6–100 treatment. In contrast to seed germination, significant differences in growth of quailbush could be attributed to both sample source (K4, K6, OS, or CC) (F3, 40 > 12, p < 0.0001) and mine tailings concentration (F4, 40 > 34, p < 0.0001). However, there was no significant interaction between these factors (F4, 40 < 2, p > 0.5).
At the end of the experiment, plants were harvested and dried to determine the effect of mine tailings concentrations on the total dry mass of quailbush (Fig. 1). Both tailings materials significantly inhibited mean total dry mass of quailbush in the 95% and 100% tailings treatments. Plants in the K4–100 treatment all died within 2 wk, while those surviving the K6–100 treatment produced extremely low plant mass. For the 95% treatment, the total dry mass in K4 and K6 was 6 and 13% of the OS dry mass, respectively. Growth of quailbush was similar to the off-site control at 75, 85, and 90% mine tailings concentration. Furthermore, growth was enhanced in some of the 75 and 85% mine tailings treatments compared with the OS. Although not significant, there was a 14 to 27% increase in total dry mass when quailbush was grown in K4–75, K4–85, and K6–75 compared with the OS sample.
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Fe Mn > Pb > Cu > As > Cd on a mass basis (Table 3). Thus, accumulation in shoots was selective with nutrient metals, particularly Mn and Zn, taken up preferentially over the three nonessential metals As, Cd, and Pb, as well as Cu. Additionally, we observed a trend suggesting that as compost increased, shoot metal accumulation decreased (data not shown).
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For both autotrophic iron and sulfur oxidizers, initial bulk counts in K4 and K6 tailings were between 105 and 106 MPN g–1 dry material. These counts were not impacted by the addition of compost to the tailings (Fig. 2). Comparing the K4 and K6 treatments, initial counts for iron oxidizers were generally one log higher in the K6 treatments, whereas sulfur oxidizers were 0.5 log greater in the K4 treatments. No iron or sulfur oxidizers were present in the OS or CC samples at the detection limit of 102 MPN g–1 dry material. Post-harvest autotrophic counts showed a 1 to 5 log reduction in iron oxidizers and a 0.5 to 2 log reduction for sulfur-oxidizers across all samples. For post-harvest counts, compost addition further decreased autotrophic population estimates, particularly for iron-oxidizers which were not detected in either the K4–75 or K6–75 treatments. Iron and sulfur oxidizers were not detected in any rhizosphere samples (data not shown).
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Finally, as expected, heterotrophic rhizosphere counts (Fig. 3C) were higher than both initial and final bulk heterotrophic counts ranging from 2.4 x 109 to 2.0 x 1010 CFU g–1 with no significant differences among treatments with surviving plants (F11, 23 = 0.64, p = 0.7607).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONREFERENCES |
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In terms of metals, both tailings samples contain total As and Pb that exceed the limits for remedial action in Arizona nonresidential areas (10 and 1200 mg kg–1 respectively), and thus are considered to be hazardous waste (ADEQ, 2002). In regard to phytotoxicity, several metals at the Klondyke site exceed reported soil plant toxicity levels (SPL). This is true for Pb (SPL = 100 to 500 mg kg–1) in the K4, K6, and OS samples, for As and Cu (SPL = 15 mg kg–1 and 200 mg kg–1, respectively) in the K4 and K6 samples, for Zn (SPL = 400 mg kg–1) in the K6 and OS samples, and for Cd and Mn (SPL = 3 and 3000 mg kg–1 respectively) in the K6 sample (Munshower, 1993; Mulvey and Elliott, 2000; Kataba-Pendias and Pendias, 2001). The reported values are not specific for quailbush but provide a general reference for plant health.
Establishment of Quailbush in Mine Tailings
This study suggests that germination is not a good indicator for quailbush establishment in mine tailings since germination results were similar for all treatments except the extremely acidic unamended K4 sample. These results are similar to the few studies that have examined seed germination in lead-zinc mine tailings. While none of the studies used Atriplex spp., they showed that germination in mine tailings is related to a threshold pH of 3.0 (Yang et al., 1997; Ye et al., 2000; Ye et al., 2001, 2002). Specifically, in the absence of an amendment, germination of Bermuda grass (Cynodon dactylon [L.] Pers.) and tall wheatgrass (Agropyron elongatum [Host] Beauv.) was not significantly inhibited if the mine tailings had a pH > 3 (Ye et al., 2000). Taken together, these results suggest that seed germination is dependent on the pH of the mine tailings sample and is impacted only at very low pH.
In contrast, growth data indicate that establishment of quailbush in the Klondyke mine tailings requires an organic amendment such as the compost used in this study. Although establishment occurred with 5% compost, quailbush required at least 10% compost to produce growth statistically similar to that in the off-site control. Other studies have similarly demonstrated stunted plant growth of grasses and shrubs in lead-zinc tailings alone compared with amended tailings material and minimal survival past the seedling stage (Yang et al., 1997; Ye et al., 2000; Ye et al., 2001; Shu et al., 2002). For example, the height and biomass of four-wing saltbush (Atriplex canescens [Pursh] Nutt.) grown in an acidic copper mine spoil sample alone was stunted compared with sludge-amended spoil (Sabey et al., 1990). Similarly, Hennessy (1985) found that four-wing saltbush grown in an amended mine spoil sample at 50% v/v produced a normal height compared with plants grown in topsoil alone, and its biomass even exceeded that in the topsoil.
While this study did not identify mechanisms of establishment, compost addition increased the organic matter and nutrient content as well as CEC, pH, and heterotrophic bacteria in the tailings. In general, compost addition to mine tailings is known to increase water-holding capacity, CEC, and help to improve the structure of mine tailings by forming stable aggregates (Ye et al., 1999; Stevenson and Cole, 1999; Schippers et al., 2000; Krzaklewski and Pietrzykowski, 2002). Furthermore, added compost can sorb and stabilize metals thereby decreasing their bioavailability (Stevenson and Cole, 1999), although we observed little change in metal bioavailability as measured by DTPA extraction in this study.
Quailbush as a Candidate for Phytostabilization
Phytoremediation of metal-contaminated soils can focus on extraction (hyperaccumulation) of metals into plant tissues, phytoextraction, or the stabilization of metals in the plant rhizosphere and roots, phytostabilization. In phytostabilization shoot accumulation of metals is undesirable as these plants may eventually serve as forage material. Thus, information on plant tissue metal accumulation in mine tailings environments is important since Atriplex spp. are sometimes the preferred grazing food of livestock or wildlife living in the area of remediated mine tailings sites (Wood et al., 1995). Only a few studies have investigated the accumulation of metals in the shoot tissues of Atriplex grown on mine tailings (Sabey et al., 1990; Jordan et al., 2002). Furthermore, only a single study has observed metal accumulation trends in Atriplex spp. while grown in mine tailings with organic amendments (Sabey et al., 1990). From the plant metal analysis results of quailbush grown in the Klondyke mine tailings, this species can be considered metal tolerant as well as a good candidate for phytostabilization strategies.
Of the nine metals measured, quailbush accumulated high levels of K and Na into shoot tissues (Table 3). This was expected since Atriplex spp. are commonly found in saline soils (Osmond et al., 1980; Malik et al., 1991; Blank et al., 1998) and is not of concern for foraging animals. Quailbush also shoot-accumulated some metals to levels of concern for plant growth reaching reported plant leaf tissue toxicity limits for Mn (400 to 1000 mg kg–1), Pb (30 to 100 mg kg–1), and Zn (100 to 400 mg kg–1) (Table 3). However, this does not seem to have impacted growth in most cases suggesting that quailbush is metal-tolerant. Shoot tissue metal concentrations are also of concern with respect to domestic animal toxicity limits. A recent National Research Council report (National Research Council, 2005) indicates that these limits are 400 to 2000 mg kg–1 for Mn, 30 mg kg–1 for Pb, and 500 mg kg–1 for Zn. In examining the data, it appears that quailbush metal accumulation exceeded these limits in some cases, particularly for Zn. However, it is unlikely that the mine tailings site would provide the only forage for wildlife in the area. Thus, it may not be critical (or possible) to use plants that will never exceed the domestic animal toxicity limits in shoot materials.
The Microbial Community as an Indicator of Plant Establishment
This appears to be the first study to have measured both autotrophic and heterotrophic microbial numbers in bulk soil and rhizosphere samples during the revegetation of a tailings site. Autotrophic iron and sulfur oxidizers were enumerated because of their ability to create an acidic environment in the tailings and impede revegetation (Schippers et al., 2000). In this study, the initial presence of iron and sulfur oxidizers served as an indicator of an acidic, disturbed environment. This was confirmed by the measured acid-generating potential at the site which was extremely high with an acid neutralization potential to acid generating potential ratio of 0.01 (ADEQ, 2001a). Enumeration of the heterotrophic community, which is dependent on available organic matter and is sensitive to environmental stressors, served both as an indicator of disturbance (low initial numbers) as well as an indicator of improvement of the mine tailings for plant growth (high post-harvest numbers). Although we recognize that culture techniques are limited in assessing the total microbial community, they can serve as a comparison between the treatments for inferring soil health.
Other studies have shown similar results either measuring heterotrophic numbers during revegetation or characterizing both heterotrophs and autotrophs in bulk tailings. For example, Mummey et al. (2002) and Moynahan et al. (2002) linked increased heterotrophic numbers and biomass to normal plant growth in the revegetation of mine tailings. Southam and Beveridge (1992, 1993) and Schippers et al. (2000) have shown that unamended bulk tailings contained high numbers (up to 106 MPN g–1 dry tailings) of iron- and sulfur-oxidizing bacteria while heterotrophic bacteria ranged from as low as 101 to 105 CFU g–1.
The results of this study demonstrate that the composition of the microbial community in a disturbed environment like mine tailings is an important indicator of the extent of disturbance and the potential success of a remediation strategy such as phytostabilization. For highly disturbed sites, one impact of compost addition is the immediate infusion of a substantial heterotrophic microbial community that is requisite for plant growth and long-term ecosystem health. Heterotrophic bacteria, as well as fungi, are required for a number of critical functions: organic matter cycling, formation of soil aggregates, and enhanced nutrient uptake in metal-contaminated environments (Bearden and Petersen, 2000; Moynahan et al., 2002). Also, bacterial involvement in redox reactions can decrease metal availability as has been demonstrated with Pb (Blake et al., 1993). Garcia-Meza et al. (2006) demonstrated a reduction in exchangeable Cu, Mn, Pb, and Zn with direct inoculation of tailings with bacteria, as well as an increase in organic matter. In addition, increased plant biomass, enhanced nutrient uptake, and reduced metal accumulation has been documented in plants grown in inoculated mine tailings (Carrillo-Castaneda et al., 2003; Petrisor et al., 2004).
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CONCLUSION |
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ACKNOWLEDGMENTS |
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