Published in J Environ Qual 38:2253-2259 (2009)
DOI: 10.2134/jeq2009.0038
© 2009 American Society of Agronomy, Crop Science Society of America, and Soil Science Society of America
677 S. Segoe Rd., Madison, WI 53711 USA
TECHNICAL REPORTS
Heavy Metals in the Environment
Phytotoxic Effects of Cu and Zn on Soybeans Grown in Field-Aged Soils: Their Additive and Interactive Actions
Bojeong Kima and
Murray B. McBrideb,*
a Center for NanoBioEarth, Dep. of Geosciences, Virginia Tech, Blacksburg, VA 24061
b Dep. of Crop and Soil Sciences, Cornell Univ., Ithaca, NY 14853
* Corresponding author (mbm7{at}cornell.edu).
Received for publication June 16, 2006.
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ABSTRACT
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A field pot experiment was conducted to investigate the interactive phytotoxicity of soil Cu and Zn on soybean plants [Glycine max (L.) Merr.]. Two soils (Arkport sandy loam [coarse-loamy, mixed, active, mesic Lamellic Hapludalf] and Hudson silty clay loam [fine, illitic, mesic Glossaquic Hapludalf]) spiked with Cu, Zn, and combinations of both to reach the final soil metal range of 0 to 400 mg kg–1 were tested in a 2-yr bioassay after 1 yr of soil-metal equilibration in the field. The soluble and easily-extractable fraction of soil Zn (or Cu), estimated by dilute CaCl2, increased linearly in response to the total Zn (or Cu) added. This linearity was, however, strongly affected where soils were treated with both metals in combination, most notably for Zn, as approximately 50% more of soil Zn was extracted into solution when the Cu level was high. Consequently, added Zn is less likely to be stabilized by aging than added Cu when both metals are present in field soils. The predictive model relating soil metal extractability to plant Zn concentration also revealed a significant Cu–Zn interaction. By contrast, the interaction between the two metals contributed little to explain plant Cu uptake. The additive action of soil Cu and Zn was of considerable importance in explaining plant biomass reduction. This work clearly demonstrates the critical roles of the properties of the soil, the nature of the metal, and the level of other toxic metals present on the development of differential phytotoxicity due to soil Cu and Zn.
Abbreviations: CEC, cation exchange capacity • ICP, inductively coupled plasma • OM, organic matter • ST, soil type
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INTRODUCTION
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LAND management activities may pose a long-term risk for agricultural environments. For example, Cu and Zn are essential micronutrients for plant growth when present in soils at trace levels (Römheld and Marschner, 1991). However, due to repeated applications of fungicides, sewage sludge, and animal manure to agricultural lands, both Cu and Zn exist in excess of plant requirements in some soils, and could potentially become toxic to plants (Magalhães et al., 1985; McBride, 1995; McBride and Spiers, 2001). The majority of metal-contaminated soils are associated with two or more metals (Förstner, 1995), and therefore, it is likely that more than one metal is responsible for the plant growth reduction and induced micronutrient imbalances found at some contaminated sites (Kim et al., 2007). Yet, little has been done to investigate the combined toxic effects of these metals on plants in field soils.
In the particular case of Cu and Zn, the metal cations are absorbed by roots through the same mechanism (Graham, 1981), and therefore, a considerable Cu–Zn interaction is expected to occur, presumably as a result of competition between the two metals for root absorption sites. Hydroponic studies with Cu and Zn showed that plant Zn uptake was significantly inhibited with an increase of Cu concentration in nutrient solution, supporting the model of an antagonistic effect of Cu on both absorption and translocation of Zn in plants (Beckett and Davis, 1978; Kabata-Pendias and Pendias, 1992; Swiader, 1985). However, analysis of the impact of Cu and Zn mixtures on plants grown in hydroponic systems only provides a partial explanation for metal interaction in the environment of plant roots. In soils, the metal concentration available to plants generally increases with the amount of metal added, but metal retention properties that vary from soil to soil determine the quantity of bioavailable metal in a soil at a given metal loading. Furthermore, the nature of the adsorbing metal and the concentrations of the competing metal ions also exert a significant influence on the bioavailable fraction of the metal in soils (Kinniburgh et al., 1976; McBride 1989; Stevenson, 1977).
Despite the importance of understanding metal interactive effects in soils, few studies have been conducted to investigate the nature of Cu–Zn interactions on plants grown in the soil environment. Luo and Rimmer (1995) reported the synergistic interaction of Cu with Zn in spring barley grown in metal-spiked soils, suggesting that enhanced Zn extractability and bioavailability due to the soil Cu addition could be responsible for the synergistic effect. Another case of a synergistic effect on yield reduction was observed in soybean plants, and the authors proposed induced Fe deficiency in the presence of Cu and Zn in a soil for this synergistic phytotoxicity (Wallace et al., 1980). Both plant assays were, however, designed to test a soil spiked for a short time with metal salt solutions, in which the greater availability of freshly-added metals would be expected to have more severe adverse effects on bioassay end points (Lock and Janssen, 2003a, 2003b; McBride, 2000; Pedersen and van Gestel, 2001). Biological and chemical disturbances in the soils created by metal spiking procedures can also have unfavorable impacts on plant responses. Furthermore, more than one soil type is desirable in this kind of study to address the role of soil properties on expression of differential metal toxicity on plants.
Therefore, in the present study, a systematic investigation into soil interactions of Cu with Zn was made by using soybean plants [Glycine max (L.) Merr.] grown in field-aged soils that had been spiked with Cu, Zn, and combinations of both. The impact of soil characteristics on metal availability was studied by testing two different soil series (Arkport fine sandy loam and Hudson silty clay loam), typical soil types for the Northeast of the United States. We developed predictive equations for both plant growth and metal uptake by using the easily-extractable fraction of total soil Cu and Zn, which was estimated by a dilute CaCl2 extraction method. The results of this long-term field-plant assay illustrate the complicated interactions in soil-metal-plant systems, and thereby, will increase our understanding of the combined impact of two metals on phytotoxicity in agricultural soils contaminated by Cu and Zn at various loading rates.
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Materials and Methods
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Field Pot Experiment
An Arkport fine sandy loam and a Hudson silty clay loam soil series were collected from the surface layer of uncontaminated agricultural research fields on the Cornell University campus (Ithaca, NY) in May 2003. The surface soil was thoroughly mixed and stored in sealed plastic bins before use, and the moisture content of the soil was determined using six subsamples collected from the bins. Calibrated amounts of 0.5 mol L–1 CuSO4 and ZnSO4 solutions were sprayed on the soil samples to achieve targeted concentration of 0, 50, 100, 200, and 400 mg kg–1 of Cu and Zn both singly and in all combinations of these levels, based on soil dry weight. Deionized water was used to dilute the metal sulfate solutions to ensure that the same volume of solution was applied to all soils regardless of treatment. Then, the moist and metal-spiked soils were placed in a V-blender for 5 min to mix completely. Approximately 8.80 kg of moist metal-spiked Hudson soil (6.88 kg dry weight) and 10.0 kg of Arkport soil (8.26 kg dry weight) samples were put into a 24 cm-diam. by 22 cm-tall plastic pots fitted with a piece of polyester landscape fabric to cover the bottom drain holes. Those 50 Hudson and Arkport soil pots were then taken to the field, and sunk into holes dug for the pots so that the soil surface in the pots was level with the soil surface in the field. The metal-spiked and control soils were allowed to age under field conditions until the following year.
Subsequent total soil metal analyses showed that the Cu concentration in the Arkport soil thought to be treated with 200 mg kg–1 Cu was the same as that in the 100 mg kg–1 Cu treatment, indicating an error in the spiking process for this one level of Cu. Therefore, the data obtained from this Arkport soil pot were treated as a replicate of the 100 mg kg–1 Cu treatment in all analyses.
Plant Analyses
After 1 yr of soil-metal equilibration, soybean plants [cultivar Pioneer 91 B91] were grown in the field pots during 2004, and again in 2005. Eight seeds were sown per pot in early June, and were thinned to three after emergence. Neither inorganic N fertilizer nor pesticide was applied during the growing season. After 9 wk of growth (mid-August), soybean plants were harvested, and divided into aboveground tissue and below-ground root parts.
Plant tops were oven-dried at 65°C, weighed, ground in a stainless steel Wiley mill, and stored in paper bags until metal analyses could be performed. Nodules, carefully removed from roots, were also weighed after rinsing in deionized water, and stored in a freezer at – 20°C until further analyses. The highest levels of soil Cu and Zn caused severe damage to soybean plants (e.g., foliar chlorosis and stunting), producing insufficient tissue and nodule samples to treat three plants as three separate measurements of plant growth. Therefore, it was decided to combine all plants from each pot into a single sample.
Soil Characteristics
Each year after harvest, surface soils were sampled from the pots, air-dried, crushed with an agate mortar and pestle to pass through a 2-mm stainless-steel sieve, and then stored in plastic bags for subsequent analyses. Measured characteristics of the uncontaminated (control) soils were as follows: pH values of the Arkport and the Hudson soils were 5.63 and 5.86, respectively (1:1 soil/deionized water). Organic matter (OM) contents of the soils were estimated by weight loss on ignition, and were 4.10% for the Arkport and 3.84% for the Hudson soils. Textural analysis by the pipette method (Gee and Bauder, 1986) revealed that the Arkport soil had 2% clay, 62.1% sand, and 35.9% silt, whereas the Hudson consisted of 15% clay, 16% sand, and 69% silt. The effective cation exchange capacity (CEC) of the Arkport soil was 6.28 cmol kg–1, and of the Hudson 12.5 cmol kg–1, measured by the amount of Ca2+ and Mg2+ displaced from exchange sites by BaCl2 solution.
The amount of metal loaded into these soils had little impact on the above-measured soil chemical properties after prolonged equilibration under field conditions. This conclusion was reached by comparing the soil pH, OM contents, and CEC in the control to those in the soil treated with the highest metal loadings (Cu and Zn at 400 mg kg–1).
Extractions and Metal Analysis
A microwave-assisted hydrofluoric acid digestion technique (USEPA 3052) and a microwave-assisted nitric acid digestion technique (USEPA 3051) were employed to measure total metal concentrations in soil and plant samples, respectively. The result of the total soil metal analysis suggested that most of the added Cu and Zn were retained in the potted soils after over a year of field-aging (data not shown). The actual soil metal concentrations are therefore very close to the values targeted by spiking.
To estimate the soluble and readily-extractable fraction of soil Cu and Zn, 10 g of dry soil were reacted with 25 mL of 0.01 mol L–1 CaCl2 solution. The soil-slurry mixture was shaken for 24 h in a reciprocal shaker at 200 rotations per minute (rpm) at room temperature, followed by filtering the suspension through Whatman No. 42 filter paper. Filtrates were transferred to 25 mL polyethylene vials, acidified with concentrated HNO3 (ultrapure grade), and then, stored at 4°C until analyzed. The metal concentrations in both the soil (or plant) digests and extracts were analyzed by inductively coupled plasma (ICP) emission spectrometry (SPECTRO CIROS CCD– ICP Spectrophotometer).
Data Analyses
The SAS statistical procedure (SAS Institute, 1999), proc mixed model was used to detect significant treatment effects (P = 0.05) on soybean plant weight and metal uptake in this study. In brief, the whole plot is the soil type, the Arkport (A) and the Hudson (H) soil series, with a 5 by 5 factorial treatment with varying amounts of Cu and Zn. Treatment levels include 0, 50, 100, 200, and 400 mg of the metal per kg of the soil. Therefore, the experimental unit is each soil pot, and there are three observational units, the soybean plants, per each experimental unit. We totaled the three observational unit responses for each experimental unit to avoid artificially inflating our degrees of freedom. Harvest year (Yr) was assigned as repeated measures' factor as plant growth and metal uptake were measured repeatedly from the both metal-spiked and control soils during two successive growing seasons. The model assumed that the plant responses were a linear function of the CaCl2–extractable soil Cu and Zn concentrations (Cus and Zns, respectively), the soil type (ST), and their interactions. For the metal extractability, the results of the CaCl2–extraction obtained in 2004 were used for both years in the model, after testing the year-to-year variation with the paired t test on the SAS program. If necessary, data were transformed to log10–scale before the analyses to meet the assumption of homoscedasticity. In the model, the ST serves as a fixed effect, whereas Yr is treated as a random effect. The best prediction model was selected on the basis of the lowest AIC value, –2 log-likelihood and BIC, in which the predictive variables were chosen by the backward elimination technique.
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Results and Discussion
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Total and CaCl2–extractable Copper and Zinc in the Soils
There was a strong linear relationship between total soil Cu (or Zn) and the concentration of CaCl2–extractable Cu (or Zn) for both soils, indicating that a nearly constant portion of the added metal was readily extractable and potentially available to plants (Fig. 1
). The results also displayed a significant influence of both the soil type and the nature of the metal on the percentage of total metal extracted by the CaCl2 solution. For example, greater metal extractability was found in the coarse-textured Arkport soil than in the finer-textured Hudson soil at any given metal treatment. This observation indicates that the Hudson soil with much higher clay content and CEC possesses a greater binding ability for the added metals than the Arkport. For a given soil, more Zn than Cu was extracted by dilute CaCl2 when they were loaded at the equivalent level, implying much stronger Cu sorption on the soil solid phases than Zn.
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Fig. 1. Relationship of metal extractability to total metal concentration in the aged metal-spiked soils.
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Interestingly, when total Zn treatment was fixed at 400 mg kg–1, there was a noticeable variation in measured Zn extractability for both soils depending on how much total Cu was present (Fig. 1). A similar but less pronounced pattern was found for extractable soil Cu when the Cu treatment was held at 400 mg kg–1 and total Zn varied. Based on these observations, we hypothesized that the presence of Cu would increase the readily-extractable Zn pools in aged metal-spiked soils, and vice versa, but the impact of added Cu on Zn extractability would be greater than that of added Zn on Cu extractability at the equivalent level of loading.
By comparing the Zn extractability measured from the soils treated with the highest level of Cu (400 mg kg–1) to those without Cu treatment (0 mg kg–1) at any given Zn loading, the extent of increase in the Zn extractability by added Cu was estimated to be from 46.8 to 63.4% in the Arkport, and from 42.8 to 65.5% in the Hudson soil (Table 1
). Simultaneously, the percentage of increase in soil Cu extractability due to the 400 mg kg–1 of added Zn was calculated to be from 6.52 to 26.8% in the Arkport and from 14.6 to 31.0% in the Hudson soil (Table 2
). We therefore conclude that the fraction of soil Zn extractable by dilute CaCl2 solution increases markedly as soil Cu increases, whereas Cu extractability is only moderately increased by increasing soil Zn.
Luo and Rimmer (1995) also reported changes of the partitioning of total Zn into the soluble and easily-extractable fraction of Zn in the presence of Cu (and vice versa) using freshly metal-spiked soils; however, it should be stressed that the spiked soils tested here had been aged for more than a year following Cu and Zn addition, yet displayed the same pattern of metal behavior. Based on our long-term field-experiment and their short-term laboratory results, we suggest that: (i) Cu sorption on the soil solid phases, presumably organic matter, occurs faster and more strongly than Zn, (ii) Zn adsorption may be limited to weak sorption sites under competitive conditions, and (iii) the degree of Zn stabilization by aging is substantially suppressed by the presence of the competitive metal, especially as the amount of this metal added is increased.
The Predictive Model for the Two-Year Field Bioassay: I. Plant Weight
In the present study, there were two measures of the impact of the added Cu and Zn on the growth of the soybean plant: aboveground plant tissue and root nodule weights. When plotting plant top against root nodule weights that were measured in 2004, we found a strong linear relationship between those two measurements with R2 values of 0.917 and of 0.833 for the Arkport and the Hudson soil, respectively. Therefore, either one can serve as a dependent variable in the model, accounting for the observed biological effects as a function of soil extractable metals. However, due to difficulties associated with collecting root nodules from soil, which were exacerbated in the Hudson soil by its finer texture, we decided to use aboveground plant dry weight as the growth parameter for this study.
As mentioned earlier, the growth of soybean plants was repeatedly measured from the potted soils treated with various levels of Cu and Zn in both 2004 and 2005. Therefore, the year-to-year variation in soil metal availability, plant biomass, and plant metal uptake needed to be tested before fitting 2-yr of data to the mixed linear model. First of all, the results of the paired t test showed that the harvest year (Yr) had little effect on soil Cu and Zn extractability, with P values of 0.5989 and 0.3513, respectively. This indicates that there was no substantial aging effect on metal availability in the time between the two soybean bioassays, which allowed us to use CaCl2–extractable metals in soils measured in 2004 as a predictor for the 2-yr plant responses in the statistical analyses.
On the other hand, the climatic conditions in the field, were very different in 2004 and 2005, and had an impact on both measured plant responses. For any given metal treatment, higher vegetative yield and elevated tissue metal concentrations were recorded in the soybean plants harvested in 2005. Briefly, the average temperature measured from June to August ranged from 16.9 to 19.9°C in 2004 and from 21.1 to 22.4°C in 2005. Monthly precipitation was 17.9 cm for July and 19.4 cm for August in 2004, but only 3.43 and 7.11 cm during the same period of time in 2005 (available at http://www.nrcc.cornell.edu/climate/ithaca/index.html). The soybean plants were, therefore, regularly irrigated with tap water in 2005. Although field conditions for the crop during two successive growing seasons were not controllable, this year/climate effect on soybean response to metals could be avoided by treating a Yr as random block in the model for this study.
Log10–transformed plant biomass was related to the CaCl2–extractable Cu and Zn concentrations (Cus and Zns, respectively), the soil type (ST), and the interaction terms of those variables to test for phytotoxicity in response to the soil metal addition. The best-fit model for predicting soybean growth was found to have Cus, Zns, ST, Cus x ST, and Zns x ST with statistical significance, and their estimates and P values are summarized in Table 3
. This form of equation implies that the increase of the readily-extractable fraction of Cu and Zn in the soils by added metals caused the reduction of soybean plant biomass mainly through their additive phytotoxic effects. The equation also implies that Cu is more phytotoxic than Zn. A Cu–Zn interaction term, although having a clear effect on metal extractability by CaCl2, was found to be insignificant in predicting the plant biomass. Similarly, the type of soil was statistically significant only when interacting with the added metal. Graphic presentation of dry plant weight against soil metal extractability is given in Fig. 2
. The patterns of the graphs are similar for both 2004 and 2005 of plant assays; however, only data obtained in 2004 are displayed in the figure for a clearer presentation of the results. Abbreviation used for Table 3, for example, Cus and Zns, are also used for Fig. 2.
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Fig. 2. Relationship of soil metal extractability to dry plant weight. Cus (or Zns): CaCl2–extractable Cu (or Zn) concentration (mg kg–1); Log: Log10–transformed; Plant Weight: estimated on a dry weight basis.
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The Predictive Model for the Two-Year Field Bioassay: II. Plant Metal Uptake
Dilute CaCl2 extraction has proven to provide a good prediction of plant metal uptake by reflecting the soluble and labile metals in soils (Rooney et al., 2006; Sanders et al., 1987). Therefore, we attempted to investigate plant tissue concentrations of Cu (or Zn) in relation to the CaCl2–extractable soil metals, the ST, and their interaction terms. The best-fit model for log10–transformed plant Cu uptake was found to contain Cus, Zns, ST, and Cus x ST terms with statistical significance (Table 3). This suggests that Cu uptake by soybean plants was largely determined by the bioavailable Cu fraction in soil as estimated by the CaCl2 extraction, and also to a small degree by soil-extractable Zn.
We also observed reduced plant Cu concentration in the finer-textured Hudson soil in the unfavorably wet growing conditions of 2004. By contrast, no such effect was found in the coarser-texture Arkport soil. In addition to the critical role of soil properties in controlling the bioavailable fraction of Cu in the soil environment, it is also plausible that this sensitivity of Cu to wet conditions, exacerbated by the fine soil texture of the Hudson, may be partly responsible for statistical significance detected for ST and Cus x ST in the analyses. The effect of a wet soil environment during the growing season in reducing plant tissue Cu concentration has been also reported in other studies (Barber, 1995; Merwin and Stiles, 1994).
Similarly, log Zns, ST, log Zns x ST, and log Cus x log Zns significantly contributed to the predicted plant Zn concentration, but not log Cus. Both plant Zn and soil extractable metal concentrations were log10–transformed in this model to meet the assumption of homoscedasticity. Zinc concentration in plant tissue increased with increasing soil Zn extractability, but decreased by Zn interaction with Cu. Compared to plant Cu uptake, a greater degree of Zn–Cu interaction was detected in the model for plant Zn, supporting a strong, inhibitory action of Cu on Zn uptake by soybean plants. As expected, the amount of Zn accumulated in the plant tops was found to be greater than that of Cu, consistent with the observed higher soil Zn extractability compared to Cu at the same level of metal loadings and the well-known strong translocation barrier for Cu between root and shoot (De Vos et al., 1991; Lexmond and van der Vorm, 1981). Figures 3
and 4
were generated for plant tissue Cu and Zn concentration, respectively, by using the results of the 2004 plant assay. The figures are helpful in visualizing the results of statistical analyses and their interpretation described above.
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Fig. 3. Relationship of soil metal extractability to Cu concentration in plant tissue. Cus (or Zns): CaCl2–extractable Cu (or Zn) concentration (mg kg–1); Log: Log10–transformed; Plant Cu: Cu concentration in plant tissue samples (mg kg–1).
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Fig. 4. Relationship of soil metal extractability to Zn concentration in plant tissue. Cus (or Zns): CaCl2–extractable Cu (or Zn) concentration (mg kg–1); Log: Log10–transformed; Plant Zn: Zn concentration in plant tissue samples (mg kg–1).
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The presence of Cu and Zn in excess can induce iron (Fe) and manganese (Mn) deficiencies in plants, exacerbating the degree of phytotoxicity (Lee et al., 1969; Wallace et al., 1980). Decrease in plant Fe and Mn uptake was evident in the present study as well, especially at high levels of Cu and/or Zn loadings. The results of the statistical analyses showed that the total concentrations of Cu and Zn in soils were statistically significant as predictors of total Fe and Mn uptake by plants. Specifically, for plant Fe uptake, P values for total soil Cu and Zn contents were 0.0019 and 0.0034, respectively, and for Mn, P values for both parameters were < 0.0001. Therefore, Fe and Mn deficiencies can contribute to the observed metal toxicity in plants grown in soils with high Cu and/or Zn. It is, however, challenging or impossible to determine the degree of their contribution to metal phytotoxicity, mainly because the plant root systems already damaged by high levels of added Cu and/or Zn, have a much-diminished ability to take up other trace metals such as Mn and Fe.
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Conclusions
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The degree of phytotoxicity of soil Cu and Zn was estimated by measuring the responses of soybean plants grown in field-aged soils treated with the metals singly and in combination over two successive growing seasons. A series of statistical models was then developed to predict both plant weight and metal uptake based on soil metal extractability estimated using dilute CaCl2 solution. The best-fit model for plant weight showed that both extractable soil Cu and Zn retarded plant growth, mainly through an additive action, but with a greater phytotoxic effect from Cu than from Zn. The predictive equation for plant Cu uptake showed that the concentration of Cu accumulated in plant tops was largely explained by the extractable fraction of soil Cu, weakly explained by the soil extractable Zn, but hardly at all by the interactivity of Zn with Cu. By contrast, a statistically significant Zn–Cu interaction with negative sign was detected in the prediction of Zn uptake, supporting the model of an antagonistic effect of Cu on both Zn absorption and translocation in soybean plants. Our study also revealed evidence of a decrease in Fe and Mn uptake by plants grown in the soils with high Cu and/or Zn that might exacerbate toxicity to soybean plants, although reduced Fe and Mn uptake may have been largely a consequence of damaged root systems from the effects of Cu and Zn. Unlike previously reported laboratory studies with freshly metal-spiked soils, however, we did not observe synergistic phytotoxicity by soil Cu and Zn when they were present together in this long-term field study.
The results of the metal interactions on soil extractable Cu and Zn are of special interest. At a given Zn level, the amount of Zn extracted by dilute CaCl2 was significantly elevated with increasing total Cu contents in soils. Similarly, Zn addition increased soil Cu extractability, but the changes caused by the increase of total soil Zn were comparably lower than those caused by Cu on Zn. The statistical significance detected on the interactive term of the metal with the soil type would indicate a critical role of the soil properties on controlling the soil metal extractability. Thus, phytotoxiciy of Cu and Zn in soybean plants can be expected to vary, depending not only on the metal-retentive properties of the soil, but also the levels of other toxic metal present. Furthermore, the stabilization process of added Zn by aging in the soil occurs to a smaller degree under competitive conditions, with the more strongly adsorbing Cu leaving a significant portion of the Zn readily extractable by CaCl2 in spite of long-term (> 1 yr) field equilibration with exposure to leaching. Aging effects on metal bioavailability were, however, difficult to discern for added Cu and Zn in this long-term field study, as both plant vegetative growth and metal uptake responses were strongly influenced by growing conditions in the field, making it difficult to accurately attribute any temporal changes in metal bioavailability to time-dependent stabilization processes.
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ACKNOWLEDGMENTS
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We would like to thank Laura Freeman (Interim Director, Laboratory for Interdisciplinary Statistical Analysis, Department of Statistics, Virginia Tech) for her assistance in the SAS analyses.
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NOTES
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All rights reserved. No part of this periodical may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, recording, or any information storage and retrieval system, without permission in writing from the publisher.
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ABSTRACT
INTRODUCTION
