HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS		QUICK SEARCH:   [advanced] Author: Keyword(s): Year:  Vol:  Page:

This Article Abstract Figures Only Full Text (PDF) Free Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in ISI Web of Science Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via ISI Web of Science (15) Citing Articles via Google Scholar Google Scholar Articles by Stuczynski, T. I. Articles by Siebielec, G. Search for Related Content PubMed PubMed Citation Articles by Stuczynski, T. I. Articles by Siebielec, G. Agricola Articles by Stuczynski, T. I. Articles by Siebielec, G. Related Collections Heavy Metals Soil Pollution Soil Biochemistry

TECHNICAL REPORTS
Heavy Metals in the Environment

Response of Soil Microbiological Activities to Cadmium, Lead, and Zinc Salt Amendments

^a Institute of Soil Science and Plant Cultivation, Pulawy, Poland
^b Environmental Quality Laboratory, Building 007, Room 202, BARC-West, Beltsville, MD 20705

^* Corresponding author (mccartyg{at}ba.ars.usda.gov)

Received for publication April 22, 2002.

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS REFERENCES

 
Heavy metal pollution of soil has been recognized as a major factor impeding soil microbial processes. From this perspective, we studied responses of the soil biological activities to metal stress simulated by soil amendment with Zn, Pb, and Cd chlorides. The amounts of heavy metal salts added to five metal-polluted soils and four nonpolluted soils were selected to match the total metal concentrations typically found in polluted soils of the Silesia region of Poland. From the perspective of soil quality, metal mobility in amended soils could not be described by simple functions of pH or organic matter. Reaction of Pb with the soil caused strong immobilization with less than 1% of the Pb amendment recovered by 0.01 M CaCl₂ extractions. Immobilization of Cd was also significant, whereas immobilization of the Zn amendment was much weaker than that of Cd or Pb. The Zn amendment had substantial inhibitory effect on soil dehydrogenase, acid and alkaline phosphatase, arylsulfatase, urease, and nitrification potential. Generally, Cd and Pb had limited or stimulatory effect on most of these biological activities, with an exception of Pb strongly inhibiting soil urease. The effect of the metal amendments on biological activities could not be satisfactorily accounted for by metal toxicity because no strong relationship was observed between extractable metal content and the degree of inhibition. The Zn amendment had a significant effect on soil pH, resulting in confounding effects of pH and Zn toxicity on activities. Metal amendment experiments seem to be of limited utility for meaningful assessment of metal contamination effects on soil quality.

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS REFERENCES

 
THE CONCEPT OF DEFINING CRITERIA for assessing changes in soil quality is a well-accepted approach that has been widely addressed in the literature (Blum, 1993; Brookes, 1995; Pankhurst et al., 1997; Leirós et al., 1999). Whereas physical and chemical soil properties help define soil fertility and productivity, soil biological functions are of equal importance. The existing regulatory values regarding soil pollution with heavy metals are mainly designed to protect the food chain and to control the risk of excessive accumulation of metals in plants. Recently, there has been a growing interest in protecting soil habitat function, which requires a quantitative assessment of toxicity factors influencing soil processes mediated by microorganisms. In the Netherlands, regulatory values were proposed for heavy metals thresholds, which should be indicative for potential deleterious effects on biological processes, such as nitrification, or on soil fauna population, represented by earthworms (Eisenia fetida) (Van Hesteren et al., 1999). This concept is based on ecotoxicology criteria that have been designed to provide protection for the soil biological processes important for sustaining soil fertility and quality in the ecosystem.

There is a substantial amount of published data assessing the behavior of microorganisms under metal stress as measured by enzyme activities, bacterial counts, soil respiration, and biomass carbon and nitrogen determinations, which has been extensively reviewed (Duxbury, 1985; Bååth, 1989; Brookes, 1995). Mechanisms for apparent metal tolerance of metals by microorganisms after long-term exposure have been also addressed (Tyler et al., 1974; Duxbury and Bicknell, 1983; Diaz-Ravina and Bååth, 1996). The use of biological activities as indicators of metal stress seems to be an attractive approach due to its simplicity. There is a concern, however, that the variability in biological activities driven by other soil parameters may be greater than effects attributed to metal pollution (Duxbury, 1985; Brookes, 1995).

The classical approach to investigating metal effect on biological activities involves laboratory experiments in which clean or polluted soils are amended with single or multiple metal salts, often resulting in soil metal contents much higher than in natural soil ecosystems (Chander et al., 1995; Marzadori et al., 1996; Hemida et al., 1997; Ping and Tieheng, 1996; Leirós et al., 1999; Welp, 1999; Kandeler et al., 2000). It is well established that metals entering soil environments undergo different transformations, usually leading to reduction of their mobility through different binding mechanisms such as precipitation or sorption by organic matter, clay minerals, hydrous oxides, and complexation (Chaney et al., 1988; Arnfalk et al., 1996; Asami et al., 1995; Wilkens and Loch, 1994; Ma and Rao, 1997; Martinez and McBride, 2001). A combination of these processes can occur simultaneously, and their overall influence is thought to be principally driven by organic mater, pH, soil texture, and mineralogy. Soil heterogeneity makes it difficult to establish universal toxicity levels and the toxicity sequence among metals for a microbial process (Welp, 1999). Additionally, large instantaneous loadings of soluble metal to soil usually do not occur in natural ecosystems.

Another aspect of the complexity of metal-polluted soil ecosystems occurs when different anthropogenic sources of metal loading interact with the preexisting pedogenic sources of metals that originate from metal-rich parent material. Such conditions are frequently found in areas with metal mining operations. The Zn, Pb, and Cd pollution of soil has been a major environmental concern in some parts of Silesia, a region of Poland with intensive Zn and Pb mining and smelting activity (Dudka et al., 1995; Chlopecka et al., 1996; Terelak et al., 1997). Soil pollution with these three metals has considerable effect on quality of crops that tend to accumulate excessive amounts of metals (Gzyl, 1990; Kabata-Pendias et al., 2000; Terelak et al., 2000), even though the vegetative productivity of soils in the region does not seem to be affected (Witek et al., 1992).

Sustainable ecosystems require robust microbial processing of nutrients in soil. Clearly, the long-term stability and function of metal-polluted ecosystems is affected by the extent to which soil microbial processes are inhibited by the pollution. The objective of our work was to assess utility of measuring biological activities involved in C, N, P, and S cycles as a means for assessing metal influence on quality of metal-polluted soils.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS REFERENCES

 
Properties of Unamended Soils
In terms of soil taxonomy, soils from both Silesia and Pulawy regions were formed on glacial till; however, the parent materials of Silesian soils were affected by Zn and Pb mineral outcroppings and mine spoils (Witek et al., 1992). Soils from Silesia contained a similar amount of clay, and on average, a significantly higher amount of organic matter than soils from the Pulawy region. Notably, others have observed that the accumulation of organic matter in metal-contaminated soils may be related to heavy metals impeding the mineralization cycle (Chander and Brookes, 1991; Valesecchi et al., 1995), but without full knowledge about site-specific soil development factors, it is difficult to speculate about influence of metal pollution on organic matter content of soils in the Silesian region. One of the Silesian soils (S5) was much higher in organic matter (Table 1) , as it was developed under the influence of shallow ground water, whereas all other soils were typical examples of rain-fed systems.

Application rates were chosen to reflect moderately high levels of pollution in Silesian soils, which on average (geometric mean) contain only 1.06, 50.9, and 166 mg kg^-1 of Cd, Pb, and Zn, respectively (Terelak et al., 1997), although much higher extreme total concentrations can occur near smelter and mining operations (Gzyl, 1990; Chlopecka et al., 1996; Terelak et al., 1997). Metal additions to the clean soils were thought to reflect the responses of microbial processes occurring in soils that were not previously under metal stress and, therefore, were less likely to develop metal tolerances as widely reported for soils with long-term metal exposure (Doelman and Haanstra, 1979; Angle et al., 1993; Duxbury and Bicknell, 1983; Diaz-Ravina and Bååth, 1996). Even before metal addition, the Silesian soils used in this study contained much greater concentrations of metals than the regional average and fall into the category of polluted soils with substantial risk for excessive metal uptake by plants.

To simulate realistic conditions, ratios between metal additions matched very closely their average ratios found in soils from the Silesian industrial region. Metals were added individually to separate soil samples (about 0.6 kg of moist soil) in 50-mL aliquots of aqueous solutions of Zn, Pb, and Cd chlorides. The concentrations of applied solutions were 107, 24, and 0.89 mM for Zn, Pb, and Cd, respectively. Those solutions were sprayed over a thin layer of soil. Soils were then mixed thoroughly to obtain an even distribution of added elements. Homogeneous soil material of each metal treatment and control was subdivided into three portions for replication. Soil moisture content was adjusted to 33 kPa water tension by the addition of water. Before assay for enzyme activities, the metal-treated soils were incubated for 14 d in a growth chamber supplied with fresh air with the temperature maintained at 25°C. Untreated soils were incubated in the same manner as a reference. The soil containers were weighed periodically to monitor soil water losses during incubation, and such losses were replaced by water.

Soil Analyses: Chemical and Physical Properties
Total metal concentrations were analyzed after sample digestion in aqua regia (a mixture in 3:1 ratio of 12 M HCl and 16 M HNO₃) as described by McGrath and Cunliffe (1985). The mobility of metals in unamended and amended soils extracted with 0.01 M CaCl₂ was assessed using the procedure described by Houba et al. (1990). The CaCl₂ extraction was performed after termination of the incubation by the procedure described above. Total C and N levels were measured using a CNS combustion analyzer (LECO Corporation, St. Joseph, MI). Soil analyses for particle size distribution were performed by the hydrometer method as described by Gee and Bauder (1986). Soil pH was measured in water and in 1 M KCl using a 1:2.5 soil to liquid ratio. At the end of the 14-d incubation, pH measurement in water was repeated to check for the pH change resulting from the metal amendments.

Enzyme Measurements
Activity measurements followed procedures described by Tabatabai (1994) and included a range of enzymes: alkaline phosphatase, acid phosphatase, and arylsulfatase. Determination of dehydrogenase was conducted as described by Casida et al. (1964). For the urease, this procedure was slightly modified: the activity was measured as the amount of ammonia produced and not by measurement of the urea remaining. Nitrification potential was determined as described by Hart et al. (1994), using soil slurries incubated with ammonium sulfate as a substrate for 48 h with sampling for NO^-₃ at 0, 24, and 48 h. The percentage inhibition of a biological activity was calculated from (C - T)/C x 100, where T is the activity in the metal-treated soil and C is the activity in the control soil. Means for each treatment were evaluated using the Duncan range test at P < 0.05. The statistical significance of regression models was tested with F tests.

	RESULTS AND DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS REFERENCES

 
The results of studies conducted in Silesia (Gzyl, 1990; Dudka et al., 1995) provide evidence that crops grown on soils containing comparable metal contents to those used in this study can accumulate excessive amount of metals from a food safety perspective. This sets an important context for our further discussion regarding metal pollution effects on biological processes and using these processes as indicators of soil quality. As demonstrated in Table 2, much larger amounts and proportions of total metal content were extractable by 0.01 M CaCl₂ from Silesian soils as compared with the soils from the Pulawy region. This is indicative of higher metal bioavailability in Silesian soils, assuming that the CaCl₂–extractable fraction represents mainly the water-soluble and exchangeable metal pools, which are considered the forms of metal available for uptake by both microorganisms and plants. There is evidence from speciation studies conducted with Tarnowskie Gory soils that most of the Cd and Pb industrial inputs appeared to be immobilized in oxide forms, whereas Zn industrial inputs are found in both oxide and residual (tightly bound) forms (Chlopecka et al., 1996).

Properties of Soil Amended with Cadmium, Lead, and Zinc
An important finding of this study was the substantial change in pH that can occur for soils amended with metal salts. The pH decreased nearly one unit in soils amended with ZnCl₂ (Table 3) . The mechanism of lowering pH by salt additions such as ZnCl₂ is through hydrolysis, yielding well-dissociated HCl and weakly dissociated Zn(OH)_2. Organic matter appeared to ameliorate change in pH caused by Zn addition, as evident from a strong correlation between these two parameters (Fig. 1) . The weaker relationship between changes in extractable Zn content and organic matter relative to that for changes in pH indicates that the primary influence of organic matter was pH buffering and not metal binding.

View larger version (18K): [in this window] [in a new window]   Fig. 1. Relationships between (A) organic matter and increases in CaCl2–extractable Zn, (B) organic matter and change in soil pH, and (C) soil pH and increases in CaCl2–extractable Zn for soils amended with Zn.

Our data indicate that soils can interact differently with soluble forms of metals from external sources. Surprisingly, we did not detect strong relationships between Zn extractability, pH, and organic matter, even though these properties should be indicative of soil potential to immobilize metals either through precipitation driven by pH or by adsorption and complexation mediated by organic matter (Wilkens and Loch, 1994; Soon and Bates, 1982). The differences observed between the two soils from Pulawy (P1 and P2) and other soils in ability to bind Zn were difficult to explain by variation of texture, organic matter, and pH because the variability of these parameters did not account for the fundamental difference observed in Zn adsorption (Table 1). An additional aspect of metal mobility in our experiment is reflected by the relationship between final soil pH, resulting from the addition of Zn, and the change in Zn-extractable form. These two parameters were weakly correlated, which indicates that there are other soil properties playing significant roles in control of Zn mobility (Fig. 1). This inconsistent pattern of metal adsorption is a common phenomenon observed in soils. Chlopecka et al. (1996) did not see any consistent relationship between distribution of metals in different fractions, including exchangeable forms, and texture, organic matter, pH, and soil type in the Tarnowskie Gory area of Silesia.

Biological Activities of Unamended Soils
Notably, the contaminated soils from Silesia, before metal addition, had a similar range of enzyme activities (with the exception of the low-pH soil, S1) to that of noncontaminated soils from Pulawy region (Table 4) . In many cases, the biological activities found in soils from Silesia were substantially higher than in our reference soils, indicating that high metal concentrations do not necessarily imply suppression of biological processes. This also suggests that the measured levels of 0.01 M CaCl₂–extractable metals, with the exception of S1, were not detrimental to biological processes in metal contaminated soils from Silesia. Metal mobility in both polluted and clean soils, as characterized by CaCl₂ extraction, did not correlate with the enzymes activities measured (Table 5) .

Although our soil samples may not be representative of all polluted soils from Silesia, it seems likely that the levels of metal content typically found in regional soils do not generally explain variability of biological activity in soil. This is in agreement with data reported by Marzadori et al. (1996), who found that dehydrogenase and phosphatase activities in mining soils, which had developed from metal-rich parent material, were sometimes higher than that detected in corresponding reference soils with low metal content. However, soils receiving metal inputs from industrial sources can also produce high activities, including processes susceptible to chemical stress such as nitrification. Sauve et al. (1999) showed that in industrial soils containing up to 6000 mg Pb kg^-1, nitrification was often several times higher than in much less polluted orchard soils.

Biological Activities of Soils Amended with Zinc, Lead, and Cadmium Salts
Soils amended with Cd, Pb, and Zn chloride salts produced different responses in biological activities, depending on the element added and soil properties. Figure 2 shows the distribution of activity inhibition or stimulation responses with Cd, Pb, and Zn additions to the nine soils studied.

View larger version (30K): [in this window] [in a new window]   Fig. 2. Ranges in response of biological activities (inhibition or stimulation) for Cd-, Pb-, and Zn-amended soils. The whiskers represent the 10th and 90th percentiles, boxes the 25th and 75th percentiles, and solid lines the mean.

The Pb treatment strongly impeded urease activity in all soils, and the level of this inhibition in most soils was between 30 and 40%. Other activities, which were negatively affected by Pb, included nitrification and acid phosphatase, but their inhibition was usually lower than 10% (Fig. 2). Activity stimulation, or no effect, was the dominating response to Pb addition observed for dehydrogenase, arylsulfatase, and particularly for alkaline phosphatase, whose activity was increased in all soils by 10 to 20%. As previously discussed, the Pb amendment was not recovered by 0.01 M CaCl₂ extractions, which suggests that it was rapidly bound to the soil matrix and the amendment had little, if any, effect on its mobile soluble forms. This indicates that the interactions between Pb and enzyme activities may not directly depend on the Pb activity in soil solution, which is the often-suggested mechanism of microbial process exposure to metal pollution. Clearly, further investigation is needed to elucidate microbial interactions with heavy metals.

Kurek et al. (1982) demonstrated that both dead and live bacterial cells pose significant binding capacity for heavy metals. Stimulatory effects of Cd and Pb are not necessarily indicative of a lack of negative effect of these metals on microbial processes. The Pb- and Cd- induced increases in biological activities may be related to their lethal effect on sensitive microbial populations, promoting growth of resistant species, which may feed on cell debris, leading to restructuring of soil microbial populations. Our data characterizing biological activity responses to Cd and Pb are in contrast with most of the existing literature, which reports strong inhibitory effects of these metals (Marzadori et al., 1996; Ping and Tieheng, 1996; Welp, 1999; Kandeler et al., 2000). This may be related, however, to the fact that metal-amendment experiments similar to ours usually involve use of higher levels of metal addition and, in some cases, several metals in combination. These large additions of different metals often do not reflect conditions representative of natural ecosystems.

The relative nature of metal toxicity studies and concerns regarding their validity for the assessment of natural ecosystems was extensively addressed in some reviews (Duxbury, 1985; Brookes, 1995). Sauve et al. (1999) measured nitrification potential in soils from an ecosystem subjected to long-term Pb pollution and found that the variation in biological activity could not be explained by a simple relationship with metal activity, organic matter, or pH. The multiple regression models derived showed that it was primarily sensitive to soil pH and organic matter and, to a much lesser extent, metal levels. They concluded from these findings that nitrification potential is not a straightforward bioindicator of soil metal contamination. Tyler et al. (1974) observed stimulation of nitrification in Cd-amended soil, suggesting that nitrifying bacteria are inherently resistant to metal pollution.

The Zn treatment produced a fundamentally different response of the measured biological activities when compared with that of Cd and Pb. Activities of Zn-amended soils, with the exception of two outliers for alkaline phosphatase and dehydrogenase, reacted with a strong inhibition (Table 4). The degree of these inhibitions greatly varied among activities and soils. Arylsulfatase had the widest range of response from little inhibition in the high organic matter Silesian soil (S4) to a complete suppression in low pH Silesian soil (S1) (Fig. 2, Table 4). Arylsufatase inhibition did not correlate with any of the soil properties measured (Table 6) .

View this table: [in this window] [in a new window]   Table 6. Comparison of regression models for relationships between the percentage inhibition of biological activities and extractable Zn, organic matter, and pH in soils after amendment with ZnCl2.

The degree of inhibition of biological activities generally did not correspond to Zn availability as measured by 0.01 M CaCl₂ extractions. Only the inhibition of nitrification and dehydrogenase were strongly correlated with extractable Zn (Table 6), whereas inhibition of other enzymes did not correspond to Zn availability, even though this availability exhibited changes over a wide range. These weak relationships may indicate that Zn mobility was not the principal parameter influencing the observed inhibitory effects. As previously discussed, Zn amendment at the rate used (700 mg Zn kg^-1 soil) had a significant effect on soil pH (Table 3). The protective role of organic matter is demonstrated by the strong reduction of dehydrogenase and nitrification inhibition with the increasing soil organic matter content (Table 6). This relationship is even stronger than the correlation between change in pH and inhibition of these two activities (Table 6). To a certain extent, organic matter also reduced susceptibility of urease. One aspect of the protective role of soil organic matter is probably related to pH buffering. The role of soil organic matter as a buffering agent for soil pH becomes evident from the strong negative relationship between pH change due to metal salt addition and soil organic matter content (Fig. 1).

Our data show that the degrees of inhibition for dehydrogenase, nitrification potential, and urease are correlated with the change in pH (Table 6). For activities such as dehydrogenase and urease, the relationship with change in pH is even stronger than with extractable Zn. The confounding nature of the relationship between pH and mobility of metals makes it difficult to separate the influence of metals on biological activities from that of pH. However, in studies involving Zn salt additions to less buffered soils, Zn toxicity may be overestimated and some of the observed detrimental effects can be accounted for by a simple change in soil pH.

The strong relationship between change in pH and inhibition of nitrification, plotted for all soils amended with the three metals, suggests that there is major contribution of pH to activity inhibition, considering that in amended soils, Pb and Cd amendments have either little negative or stimulatory effect on nitrification inhibition (Fig. 3) . It is obvious from these data that inhibition of nitrification as related to change in pH resulting from all metal additions can be described by a simple linear model. The important role of pH is also reflected in a considerable correlation between pH, urease, and nitrification in control (unamended) soils. As previously discussed, these soils had a wide range of total metal contents and metal extractability, including high values found in soils from Silesia, and these conditions did not seem to suppress activities. Recent work by Smolders et al. (2001) clearly demonstrated that the effect of pH on nitrification can be as great as that caused by the metal additions.

View larger version (21K): [in this window] [in a new window]   Fig. 3. Relationship between change in pH and biological activity response in Cd-, Pb-, and Zn-amended soils.

Stimulation and Inhibition of Biological Activities in Soil
As previously discussed, Cd and Pb did not always have an inhibitory effect on biological activities. In many cases, stimulatory effects were observed, but the extent of a given activity increase did not correlate well with any of the soil properties measured. To gain a better understanding of how soil properties influence activity stimulation or inhibition to metal additions, a simple correlation analysis was used. The correlation matrix included all measured soil parameters and the number of cases when stimulatory or inhibitory effect was observed in each soil, regardless of the metal type or activity of concern (Table 7) . The strongest correlation between the occurrences of biological activity stimulation was found for organic matter and pH. Positive correlation between stimulatory effects, organic matter, and pH lends some support for the validity of population restructuring in accounting for activity stimulation, as biomass growth strongly depends on substrate availability, reflected by organic matter and optimal pH conditions. The occurrences of biological inhibition in soils were negatively correlated with organic matter and silt content and positively correlated with sand fraction. As the clay content of most of our soils was small, it is likely that the main compartment for microbial populations was associated with the silt fraction. The study by Kandeler et al. (2000) demonstrates significant effect of soil texture on distribution of activities in soils, which are mainly distributed among silt and clay fractions. The increased susceptibility of biological activities to inhibition in soils with higher sand content may be due to their lower metal binding and pH buffering capacities and, as a consequence, larger exposure of microbial population associated with this coarser fraction.

	CONCLUSIONS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS REFERENCES

	REFERENCES

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS REFERENCES

 

• Angle, S., R.L. Chaney, and D. Rhee. 1993. Bacterial resistance to heavy metals related to extractable and total metal concentrations in soil and media. Soil Biol. Biochem. 25:1443–1446.
• Arnfalk, S., S.A. Wasay, and S. Tokunaga. 1996. A comparative study of Cd, Cr(III), Cr(VI), Hg, and Pb uptake by minerals and soil materials. Water Air Soil Pollut. 87:131–148.
• Asami, T., M. Kubota, and K. Orikasa. 1995. Distribution of different fractions of cadmium, zinc lead, and copper in unpolluted and polluted soils. Water Air Soil Pollut. 83:187–194.
• Bååth, E. 1989. Effects of heavy metals in soil on microbial processes and populations (a review). Water Air Soil Pollut. 47:335–379.
• Blum, W. 1993. Sustainable land management with regard to socio–economic and environmental soil functions: A holistic approach. p. 115–124. In R.C. Wood and J. Dumanski (ed.) Sustainable land management for the 21st century. Vol. 2. Lethbridge Univ., Lethbridge, AB, Canada.
• Brookes, P.C. 1995. The use of microbial parameters in monitoring soil pollution by heavy metals. Biol. Fertil. Soils 19:269–279.
• Casida, L.E., D.A. Klein, and T. Santoro. 1964. Soil dehydrogenase activity. Soil Sci. 98:371–376.
• Chander, K., and P.C. Brookes. 1991. Effects of heavy metals from past applications of sewage sludge on microbial biomass and organic matter accumulation in a sandy loam and silty loam UK soil. Soil Biol. Biochem. 23:927–932.
• Chander, K., P.C. Brookes, and S.A. Harding. 1995. Microbial biomass dynamics following addition of metal-enriched sewage sludges to a sandy loam. Soil Biol. Biochem. 27:1409–1421.
• Chaney, R.L., H.W. Mielke, and S.B. Sterrett. 1988. Speciation, mobility and bioavailability of soil lead. p. 105–129. In B.E. Davies and B.G. Wixon (ed.) Lead in soils: Issues and guidelines. Science Reviews, Northwood, UK.
• Chlopecka, A., J.R. Bacon, M.J. Wilson, and J. Kay. 1996. Forms of cadmium, lead, and zinc in contaminated soils from southwest Poland. J. Environ. Qual. 25:69–79.
• Diaz-Ravina, M., and E. Bååth. 1996. Development of metal tolerance in soil bacterial communities exposed to experimentally increased metal levels. Appl. Environ. Microbiol. 62:2970–2977.[Abstract]
• Doelman, P., and L. Haanstra. 1979. Effects of lead on the soil bacterial microflora. Soil Biol. Biochem. 11:487–491.
• Dudka, S., M. Piotrowska, A. Chlopecka, and T. Witek. 1995. Trace element contamination of soils and crop plants by mining and smelting industry in southwest Poland. J. Geochem. Explor. 52:237–250.
• Duxbury, T. 1985. Ecological aspects of heavy metal responses in microorganisms. p. 185–235. In K.C. Marshall (ed.) Advances in microbial ecology. Vol. 8. Plenum Press, New York.
• Duxbury, T., and B. Bicknell. 1983. Metal tolerant bacterial populations from natural and metal polluted soils. Soil Biol. Biochem. 15:243–250.
• Gee, G.W., and J.W. Bauder. 1986. Particle size analysis. p. 383–411. In A. Klute et al. (ed.) Methods of soil analysis. Part 1. 2nd ed. Agron. Monogr. 9. ASA and SSSA, Madison, WI.
• Gzyl, J. 1990. Lead and cadmium contamination of soil and vegetables in the Upper Silesia region of Poland. Sci. Total Environ. 96:199–209.[Medline]
• Hart, S.C., J.M. Stark, E.A. Davidson, and M.K. Firestone. 1994. Nitrogen mineralization, immobilization, and nitrification. p. 985–1018. In R.W. Weaver et al. (ed.) Methods of soil analysis. Part 2. Microbiological and biochemical properties. SSSA Book Ser. 5. SSSA, Madison, WI.
• Hemida, S.K., S.A. Omar, and A.Y. Abdel-Mallek. 1997. Microbial populations and enzyme activity in soil treated with heavy metals. Water Air Soil Pollut. 95:13–22.
• Houba, V.J.G., I. Novozamsky, T.M. Lexmond, and J.J. Van der Lee. 1990. Applicability of 0.01 M CaCl₂ as a single extraction solution for the assessment of the nutrient status of soils and other diagnostic purposes. Commun. Soil Sci. Plant Anal. 21:2281–2290.
• TsutsumiKabata-Pendias, A., and H. Pendias. 2001. Trace elements in soils and plants. 3rd ed. CRC Press, Boca Raton, FL.
• TsutsumiKabata-Pendias, A., H. Terelak, and C. Pietruch. 2000. Trace metals in potato tubers as a function of their contents in arable soils in Poland. p. 54–55. In Proc. 1st Int. IUPAC Symp. on Trace Elements in Food, Warsaw. 9–11 Oct. 2000. Int. Union of Pure and Applied Chem., Research Triangle Park, NC.
• Kandeler, E., D. Tscherko, K.D. Bruce, M. Stemmer, P.J. Hobbs, R.D. Bardgett, and W. Amelung. 2000. Structure and function of the soil microbial community in microhabitats of a heavy metal polluted soil. Biol. Fertil. Soils 32:390–400.
• Kurek, E., J. Czaban, and J.M. Bollag. 1982. Sorption of cadmium by microorganisms in competition with other soil constituents. Appl. Environ. Microbiol. 43:1011–1015.[Abstract/Free Full Text]
• Leirós, M.C., C. Trasar-Cepeda, F. Garcia-Fernandez, and F. Gils-Sotres. 1999. Defining the validity of a biochemical index of soil quality. Biol. Fertil. Soils 30:140–146.
• Ma, L.Q., and G.N. Rao. 1997. Chemical Fractionation of cadmium, copper, nickel, and zinc in contaminated soils. J. Environ. Qual. 26:259–264.[Abstract/Free Full Text]
• Martinez, C.E., and M. McBride. 2001. Cd, Cu, Pb, and Zn co-precipitates in Fe oxide formed at different pH: Aging effects on metal solubility and extractability by citrate. Environ. Toxicol. Chem. 20:122–126.[ISI][Medline]
• Marzadori, C., C. Ciaviatta, D. Montecchio, and C. Gessa. 1996. Effects of lead pollution on different soil enzyme activities. Biol. Fertil. Soils 22:53–58.
• McGrath, S.P., and C.H. Cunliffe. 1985. A simplified method for the extraction of the metals Fe, Zn, Cu, Ni, Cd, Pb, Cr, Co and Mn from soils and sewage sludges. J. Sci. Food Agric. 36:794–798.[ISI]
• Pankhurst, C.E., B.M. Doube, and V.V.S.R. Gupta. 1997. Biological indicators of soil health synthesis. p. 419–435. In C.E. Pankhurst et al. (ed.) Biological indicators of soil health. CABI Publ., Wallingford, UK.
• Ping, G., and S. Tieheng. 1996. Side effects of organic and inorganic pollutants on soil nitrification and respiration. J. Environ. Sci. (China) 8:66–76.
• Sauve, S., A. Dumestre, M. McBride, J.W. Gillet, J. Berthelin, and W. Hendershot. 1999. Nitrification potential in field collected soils contaminated with Pb or Cu. Appl. Soil Ecol. 12:29–39.
• Smolders, E., K. Brans, F. Coppens, and R. Merckx. 2001. Potential nitrification rate as a tool for screening toxicity in metal-contaminated soils. Environ. Toxicol. Chem. 20:2469–2474.[ISI][Medline]
• Soon, Y.K., and T.E. Bates. 1982. Chemical pools of cadmium, nickel and zinc in polluted soils and some preliminary indicators of their availability to plants. J. Soil Sci. 33:477–488.
• TsutsumiTabatabai, M.A. 1994. Soil enzymes. p. 775–826. In R.W. Weaver et al. (ed.) Methods of soil analysis. Part 2. SSSA Book Ser. 5. SSSA, Madison, WI.
• TsutsumiTerelak, H., A. Kabata-Pendias, and C. Pietruch. 2000. Trace metals in cereal grains in Poland. p. 63–64. In Proc. 1st Int. IUPAC Symp. on Trace Elements in Food, Warsaw. 9–11 Oct. 2000. Int. Union of Pure and Applied Chem., Research Triangle Park, NC.
• Terelak, H., T. Stuczynski, and M. Piotrowska. 1997. Heavy metals in agricultural soils in Poland. Pol. J. Soil Sci. 30:35–42.
• Tyler, G., B. Mörnsjo, and B. Nilsson. 1974. Effects of cadmium lead, and sodium salts on nitrification in mull soil. Plant Soil 40:237–242.
• Valesecchi, G., C. Gigliottti, and A. Farini. 1995. Microbial biomass, activity, and organic matter accumulation in soils contaminated with heavy metals. Biol. Fertil. Soils 20:253–259.
• Van Hesteren, S., M.A. Van de Leemkule, and M.A. Pruiksma. 1999. Minimum soil quality: A use-based approach from an ecological perspective. Part 1: Metals. Tech. Soil Protection Committee, The Hague, the Netherlands.
• Welp, G. 1999. Inhibitory effects of the total and water-soluble concentrations of nine different metals on the dehydrogenase activity of loess soil. Biol. Fertil. Soils 30:132–139.
• Wilkens, B.J., and P.G. Loch. 1994. Accumulation of cadmium and zinc from diffuse emission on acid sandy soils, as a function of soil composition. Water Air Soil Pollut. 96:1–16.
• Witek, T., M. Piotrowska, and T. Motowicka-Terelak. 1992. Scope and methods of changing the structure of the agriculture in the most contaminated areas of Katowice voivodeship. 1. Tarnowskie Gory area. (In Polish.) Technical report. Inst. of Soil Sci. and Plant Cultivation, Pulawy, Poland.

This article has been cited by other articles:

				M. Tejada, M. T. Hernandez, and C. Garcia Application of Two Organic Wastes in a Soil Polluted by Lead: Effects on the Soil Enzymatic Activities J. Environ. Qual., January 9, 2007; 36(1): 216 - 225. [Abstract] [Full Text] [PDF]

				A. J. Franzluebbers, S. R. Wilkinson, and J. A. Stuedemann Bermudagrass Management in the Southern Piedmont, USA: IX. Trace Elements in Soil with Broiler Litter Application J. Environ. Qual., March 1, 2004; 33(2): 778 - 784. [Abstract] [Full Text] [PDF]

This Article Abstract Figures Only Full Text (PDF) Free Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in ISI Web of Science Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via ISI Web of Science (15) Citing Articles via Google Scholar Google Scholar Articles by Stuczynski, T. I. Articles by Siebielec, G. Search for Related Content PubMed PubMed Citation Articles by Stuczynski, T. I. Articles by Siebielec, G. Agricola Articles by Stuczynski, T. I. Articles by Siebielec, G. Related Collections Heavy Metals Soil Pollution Soil Biochemistry