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Published online 25 January 2007
Published in J Environ Qual 36:379-385 (2007)
DOI: 10.2134/jeq2006.0374
© 2007 American Society of Agronomy, Crop Science Society of America, and Soil Science Society of America
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TECHNICAL REPORTS

Heavy Metals in the Environment

Effect of Dissolved Organic Carbon on Zinc Solubility in Incubated Biosolids-Amended Soils

Vasileios Antoniadisa,*, Christos D. Tsadilasb and Stamatis Stamatiadisc

a Dep. of Agricultural Development, Democritus Univ. of Thrace, 193 Pantazidou St., GR-682 00, Orestiada, Greece
b National Agricultural Research Foundation, Institute of Soil Mapping and Classification, 1 Theofrastos St., Larissa, GR-413 35, Greece
c Soil Ecology and Biotechnology Lab., Goulandris Natural History Museum, GAIA Center, 13 Levidou St., GR-145 62, Kifissia, Greece

* Corresponding author (vasilisrev{at}yahoo.com)

Received for publication September 18, 2006.

   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Soil organic carbon (SOC) and dissolved organic carbon (DOC) affect long-term heavy metal solubility in biosolids-amended soils, but their role needs to be further studied under Mediterranean climatic conditions. We investigated Zn solubility, as assessed by water extraction, in two typical Greek soils amended with biosolids at 0, 20, and 100 Mg ha–1 during a 310-d incubation period. It was found that SOC decreased by nearly 30% over time in the 100 Mg ha–1 treatment. There was evidence that DOC affected Zn solubility, because DOC increased significantly on Day 23, probably due to a flush in microbial activity, and water-extractable Zn followed the same trend. After that, both DOC and water-extractable Zn decreased back to values similar to those of the unamended soils. Although Zn solubility did not increase overall even at high biosolids application rates, this study shows that time-limited fluctuations in Zn solubility due to sudden DOC flushes, can be significant, and need to be further investigated.

Abbreviations: DOC, dissolved organic carbon • IRMS, isotope ratio mass spectrometer • SOC, soil organic carbon


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS
 REFERENCES
 
THE use of sewage sludge in agriculture improves soil fertility (O'Connor et al., 2004; Cogger et al., 2004) and soil physical properties by increasing soil organic matter content (Metzger and Yaron, 1987). However, biosolids-borne heavy metals may pose an environmental risk (Sukreeyapongse et al., 2002; Gaskin et al., 2003). Zinc is a potentially mobile metal that can either be taken up by crops or leached down the soil profile. Li and Shuman (1996) found that Zn moved deeper than Cd and Pb in a contaminated soil. Furthermore, Sukkariyah et al. (2005) found that Zn had a higher uptake coefficient than Cd, Ni, and Cu for radish in a long-term field experiment conducted in biosolids-amended soil. Zinc is also associated with organic matter (Kabata-Pendias, 2001), thus concerns are raised over the long term Zn availability in biosolids-amended soils due to organic matter decomposition. Several studies on Zn solubility have been conducted on temperate climates (Dowdy et al., 1991; White et al., 1997; Bhogal et al., 2003; Granato et al., 2004). However, the conclusions drawn from these investigations may not always be applicable to soils in Mediterranean climates where organic matter decomposition is expected to be faster. Additional studies in semiarid soils are necessary to assess the likely fate of biosolids-borne metals. One way of simulating soil organic C (SOC) decomposition in biosolids-amended soils is incubation in the laboratory. Soil organic C is decomposed faster during incubation than under field conditions, provided that temperature is higher than the mean annual field temperature (Aita et al., 1997). Incubation experiments can provide initial information on SOC decomposition and transformations, as well as on metal mobility, because these parameters can be measured in a systematic manner, under well-controlled conditions (Sleutel et al., 2005).

There is evidence that dissolved organic C (DOC) may have an important effect on Zn solubility (Antoniadis and Alloway, 2002). The fraction of DOC derived from biosolids may be particularly important in affecting Zn solubility in soil. However, the effect of DOC on heavy metal behavior has not been extensively documented. For example, it has been reported that biosolids-derived DOC undergoes composition changes over time (Gigliotti et al., 1997), but it is still unknown how these changes affect heavy metal solubility. The dynamics of introduced DOC can be traced by measuring the natural abundance of 13C/12C ({delta}13C) in amended soils. This technique is usually applied to studies of SOC dynamics (Van Kessel et al., 1994), but rarely to investigations that link SOC dynamics to metal solubility. Monitoring {delta}13C may provide insights on the behavior of heavy metals contained in biosolids that tend to change due to SOC decomposition and DOC evolution.

The aims of this study were (i) to quantify SOC decomposition, and DOC dynamics in soils incubated with and without biosolids, (ii) to assess the effect of SOC and DOC on Zn solubility, and (iii) to determine some of the potential risks or benefits of biosolids application to two representative Mediterranean soils.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Soils and Biosolids
Two representative soils of Central Greece with different clay and SOC content were selected for the study. Soil A was a sandy loam alluvial soil (Typic Xerofluvent) collected near River Pineios in Larissa and soil B was clayey (Vertic Xerochrept), collected 5 km away from the river. Soils were sampled from a 0- to 20-cm depth, air-dried, and passed through a 2-mm sieve. The following properties were determined: particle size distribution (Gee and Bauder, 1982), cation exchange capacity (Rhoades, 1982a), organic carbon by wet oxidation (Nelson and Sommers, 1982), dry bulk density, pH (1:2.5 w/v soil to H2O), electrical conductivity (1:5 w/v soil to H2O), and CaCO3 (Rowell, 1994). The soils were also digested with aqua regia (Ure, 1995) and Zn concentrations were analyzed by atomic absorption spectrophotometry (Varian, SpectrAA-400 Plus, Australia) (Table 1). Biosolids were obtained from the drying beds of the sewage treatment plant of the city of Larissa, where biosolids are anaerobically digested. Biosolids were air-dried, crushed to pass through a 1-mm sieve, and analyzed for pH, electrical conductivity, water-extractable Zn (Beckett, 1989), aqua regia-digested Zn, DOC, and organic carbon (Table 2). The methods of analyses were similar to those used for the soils.


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  		Table 1. Some physical and chemical properties of soils.

 

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  		Table 2. Some physical and chemical properties of biosolids.

 
Experimental Design
Soil samples were mixed with biosolids at rates equivalent to 0 (control), 20, and 100 Mg ha–1. Mixtures were obtained at a 1:90 biosolids to soil ratio for the 20 Mg ha–1 treatment and at a 1:18 ratio for the 100 Mg ha–1 treatment on a gravimetric basis. While the 20 Mg ha–1 treatment is close to the application rate used in common agricultural practice, 100 Mg ha–1 was deliberately chosen to cause a measurable increase in Zn, SOC, and DOC concentrations.

One half kilogram of oven-dry equivalent masses of soils and soil-biosolids mixtures were placed in plastic bags. All treatments were replicated three times and this resulted in a total of nine bags for each soil (the experiment was a complete factorial design). All samples were wetted to 67% of their water holding capacity with deionized water, and were incubated for 310 d in a temperature-controlled chamber at 28°C. This temperature was selected because at 28°C the rate of SOC mineralization is nearly twice as high as that at 21°C (Rey et al., 2005), which is the mean annual air temperature of the area from which the soils were obtained. The bags were not sealed, and the mixtures were being aerated. Oxic conditions were maintained, and no signs of anaerobic conditions developed throughout the course of incubation. Every week the samples were weighed and water was added according to the recorded weight loss.

Sampling and Analysis
The soil properties measured throughout the duration of incubation were: pH, SOC, DOC, and water-soluble Zn. pH (1:2.5 soil/H2O) was measured according to Rowell (1994) on Day 0 (the start of incubation), and then on Days 16, 58, and 310 (the end of incubation). Soil organic C was measured by wet oxidation (Nelson and Sommers, 1982) on Days 0, 1, 2, 4, 8, 16, 23, 36, 58, and 310. On the same days water extracts were obtained by shaking 10 g of soil with 10 mL of deionized H2O overnight and then filtering the paste through a 0.45-µm filter to retain large colloids and leave in the solution only the dissolved matter (Antoniadis and Alloway, 2002). Dissolved organic C was then measured in these water extracts by isotope ratio mass spectrometry (IRMS, 20–20 ANCA-SL, PDZ Europa, Crewe, UK), after values were corrected for dissolved inorganic C (comprised of mainly HCO3–), which was analyzed as explained below. Inorganic C was only a minor fraction (typically approximately 5%) of the values measured by IRMS, and unchanged throughout the incubation. Isotopic composition of C ({delta}13C) in the water extracts was measured at the end of incubation period by IRMS. Two hundred µL of the water extract were oven dried in 12 by 5 mm tin capsules at 60°C for 3 h. The dried samples were then analyzed for {delta}13C using an automated combustion elemental analyzer interfaced with a triple collector. Sharpsburg silty clay loam ({delta}13C = –17.251{per thousand}) was used as the working standard. The procedure followed was the same as that used for the isotopic determination of soil samples, as outlined by Stamatiadis et al. (2006). Overall precision (machine error plus sample preparation error) for C isotopic composition was ± 0.46{per thousand}. Carbon isotopic composition, {delta}13C, was calculated according to the following equation:

Formula 1[1]
where R = 13C/12C. Values were calculated relative to the international standard Vienna-Pee Dee Belemnite for 13C (R = 0.0112372). The {delta}13C values were then used to determine the fraction FDOC of ‘new’ organic C (i.e., biosolids-borne organic C) in the dissolved C pool of the biosolids-amended soils, according to the equation given by Balesdent and Mariotti (1996):

Formula 2[2]
where {delta}t is the isotopic composition of the dissolved C fraction of the biosolids-amended soil samples measured at the end of incubation (Day 310), {delta}S is the isotopic composition of the dissolved C fraction of the control soils (Table 1), and {delta}B the isotopic composition of the dissolved C fraction of biosolids (Table 2). Although the measured isotopic composition of C referred to both organic and inorganic dissolved C in the water extracts, the current use of the {delta}13C and FDOC values is acceptable, since inorganic C fraction was small and stable over time (Midwood and Boutton, 1998). For comparison, the fraction of SOC that biosolids contribute in the amended soils, FSOC, was also measured in the beginning and at the end of incubation, according to the equation:

Formula 3[3]
where SOC100 is the SOC content in the 100 Mg ha–1 treatment and SOCcontrol is the SOC content in the unamended control treatment. Soluble Zn was extracted in the same water extracts as those used for measuring DOC and {delta}13C values, and was analyzed on an atomic absorption spectrometer (Varian, SpectrAA-400 Plus, Australia). Water extracts were also analyzed for HCO3–, Cl–, and SO42–, as well as Ca2+, Mg2+, K+, and Na+ (Rhoades, 1982b). These data along with water-extractable Zn, and dissolved organic matter content (back-calculated from DOC assuming a molecular weight of 800 g mol–1 and a carbon content of 500 g kg–1) were the input data to Visual Minteq, version 2.50 (Gustafsson, 2005), from which Zn speciation in the water extracts was calculated.

Statistical Analysis
Data were analyzed statistically using analysis of variance (ANOVA). The multiple range test was employed to determine the significance of differences between treatments and sampling times at p < 0.05. The statistical package used was SPSS 10 for Windows (Release 10.0.1) (SPSS, 1999).


   RESULTS AND DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
CONCLUSIONS
 REFERENCES
 
Changes in pH and Soil Organic Carbon
The reduction of soil pH with increasing rates of biosolids application (Fig. 1) was attributed to the lower pH of biosolids (Table 2). Biosolids application caused a slight but insignificant pH decrease in all treatments over time. Soil acidification is known to occur from nitrification of ammonium contained in sludge (Smith and Doran, 1996; Stamatiadis et al., 1999). In this study, the changes in pH over time were not significant, probably due to buffering capacity of both soils, as a result of the presence of carbonates (Table 1). Although carbonates were not present in exceptionally high concentrations, they were found in such amounts that could keep soil pH controlled during the 310-d incubation. This suggests that pH did not have a significant role in any of the temporal changes of Zn behavior in this study.


Figure 1
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  		Fig. 1. pH values during incubation of unamended and biosolids-amended soils. Error bars indicate standard deviation (n = 3).

 
On the other hand, biosolids application increased SOC content significantly in both soils (Fig. 2). On Day 0 SOC was 2.5 and 2.3 times higher at 100 Mg ha–1 than the control in soil A and B, respectively. As expected, SOC decreased significantly over time in the biosolids-amended soils, and the rate of decrease was higher at the 100 Mg ha–1 treatment. The overall decrease of SOC at the end of incubation, which is a measure of organic C mineralization, was 8% (soil A) and 12% (soil B) in the 20 Mg ha–1 treatment. The rate of decrease at 100 Mg ha–1 was 31% (soil A) and 28% (soil B). It should be noted that most of the SOC reduction at 20 Mg ha–1 occurred in the early stages of incubation, probably because in that treatment there was a smaller quantity of easily decomposable biosolids-borne organic C. The rate of decomposition in the amended soils was relatively fast compared to some field experiments. For example, Hyun et al. (1998) found that SOC in amended soils decreased by 30 to 40%, an only slightly higher percentage than that found in this study, after a 10-yr field experiment. Soil organic C did not change over time in the unamended soils (Fig. 2) as has also been reported by others (Hooda and Alloway, 1993), indicating that native SOC was more stable and resistant to decomposition than added organic C. This means that in the amended samples it was mostly the biosolids C that decomposed. Stemmer et al. (1999) similarly reported a near 40% decrease of added C, in the form of straw amendment, in their 360-d incubation. Despite its significant reduction, SOC was still elevated in the biosolids-amended soils relative to the unamended control at the end of the incubation period. This means that biosolids application increased SOC in the studied time-scale, which is a beneficial effect for Greek soils that are usually low in SOC.


Figure 2
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  		Fig. 2. Soil organic C dynamics during incubation of unamended and biosolids-amended soils. Error bars indicate standard deviation (n = 3).

 
Changes in Dissolved Organic Carbon and Zinc Solubility
Biosolids application triggered an initial and gradual increase of DOC that reached a peak on Day 23 in both soils at 100 Mg ha–1 (Fig. 3). After Day 23 DOC rapidly declined to levels similar to those of the control and did not change significantly thereafter. The initial DOC peak may have been the result of a flush in microbial activity, which was probably stimulated by wetting the air-dry mixtures to 67% of their water holding capacity at the beginning of incubation. According to Griffiths et al. (2005), wetting-drying cycles can cause this effect in DOC dynamics. They reported a peak of similar magnitude and duration to ours. There also seems to be an association between DOC increase and SOC decrease, since both occurred during the early stages of incubation in the treatments that received higher additions of biosolids-borne organic matter. This suggests that in soils where high biosolids applications are added, DOC can increase significantly especially when relatively fast organic matter decomposition occurs. The same was also observed by Antoniadis and Alloway (2001). This peak in DOC dynamics did not occur in the unamended controls, neither at 20 Mg ha–1 in soil A, probably due to the relatively low content of added biosolids-borne decomposable organic matter.


Figure 3
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  		Fig. 3. Dissolved organic C dynamics during incubation of unamended and biosolids-amended soils. Error bars indicate standard deviation (n = 3).

 
To assess the role of DOC on metal solubility in the amended soils, an analysis of the particular contribution of soil and biosolids to the DOC fraction at the end of incubation was performed. This was based on FDOC, described in Eq. [2]. Control soil {delta}13C values were in the expected range (Table 1), typical for soils that have been cultivated for years with C3 plants (Norra et al., 2005). At the end of incubation, the mean {delta}13C values of the soils amended with 100 Mg ha–1 (Table 3) were significantly lower than those of the control soils (a difference of 0.96{per thousand} in soil A and of 0.80{per thousand} in soil B). Gerzabek et al. (1997) reported similar differences in {delta}13C values between soils amended with animal manure and unamended soils. Based on the above figures, FDOC indicated that the applied biosolids contributed only 31% to the total DOC in soil A and 24% in soil B at the end of incubation (Table 3). To have an assurance over these values, FSOC (described in Eq. [3]) was also calculated, both at the beginning and at the end of incubation. On Day 0, biosolids contributed 60% of the total SOC in soil A, and 56% in soil B (Table 3). Biosolids organic C decreased significantly to approximately 39% at the end of incubation in both soils, and confirmed that this fraction of organic C in the amended soils was depleted faster than the indigenous SOC. The difference between FDOC and FSOC on Day 310 was probably a result of not taking into consideration in the calculation of FSOC the ‘priming effect’ in the amended soils, which led to an overestimation of FSOC. Assuming that the two fractions, FDOC and FSOC, were similar on Day 0, the biosolids-derived DOC decreased by 48% in soil A, and by 58% in soil B. These estimates are more conservative than those reported by Aita et al. (1997) in a soil amended with 13C-enriched straw. They estimated that straw-derived organic C decreased by 80% after 1-yr incubation.


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  		Table 3. Percentage of the contribution of biosolids to soil organic carbon (SOC) and to dissolved organic carbon (DOC) at the beginning and at the end of incubation in the 100 Mg ha–1 treatment. Mean {delta}13C values of DOC refer to Day 310.

 
Zinc solubility, measured in the same water extracts where DOC was measured, significantly increased with the application of biosolids (Fig. 4). In both soils there was a significant peak on Day 23 in the water-extractable Zn at 100 Mg ha–1, which was not observed in the controls (Fig. 4). At 100 Mg ha–1 water-extractable Zn increased on Day 23 by 156% (from 0.27 to 0.42 mg kg–1) in soil A, and by 215% (from 0.34 to 0.73 mg kg–1) in soil B, relative to their corresponding concentrations on Day 8. This increase indicates that DOC dynamics can have an effect on Zn solubility, since the peak of water-extractable Zn bears a similarity to the DOC peak obtained in the 100 Mg ha–1 treatment (Fig. 3). After that, water-extractable Zn decreased back to the unamended control. The reduction of Zn solubility in the amended soils over time may also have been assisted by the decrease of the biosolids-derived DOC. The effect of DOC on water-extractable Zn was also evidenced by the speciation calculation by Visual Minteq (Gustafsson, 2005), which suggests that the increase in soluble Zn was associated with a significant increase in the activity of Zn-dissolved organic matter species (Fig. 5). At 100 Mg ha–1 the activity of Zn-dissolved organic matter species increased from 1.42 µmol L–1 (on Day 0) to 2.98 µmol L–1 (on Day 23) in soil A. Likewise, in soil B at 100 Mg ha–1 the organo-metallic species increased their activity from 1.86 µmol L–1 (Day 0) to 4.97 µmol L–1 (Day 23), and at 20 Mg ha–1 from 1.00 µmol L–1 (Day 0) to 2.63 µmol L–1 (Day 23). Unlike what was observed at 100 Mg ha–1, water-extractable Zn at 20 Mg ha–1 had a peak only in soil B, a behavior similar to that of DOC at 20 Mg ha–1. This indicates that even at low biosolids application rates Zn solubility can increase when affected by DOC. Antoniadis and Alloway (2002) also found that Zn solubility, assessed both by soil extraction with DTPA and plant uptake, increased with DOC in soil-biosolids mixtures. Neal and Sposito (1986), studying the adsorption of Cd, which is a similarly mobile metal in the soil environment as Zn, found that adsorption decreased in the presence of DOC. The significant effect of DOC on metal solubility within the time-scale of this experiment (44 wk) was also reported by Strobel et al. (2005). In their 88-wk incubation, they found that the presence of DOC can increase the release of readily available forms of Cd in the first 40 wk of incubation. It should be noted that in the current study the peaks of DOC and water-extractable Zn had some differences in geometry (DOC increased gradually, while the increase in soluble Zn was steep). This seems to suggest that DOC affected Zn solubility and speciation only when DOC increased above a certain concentration threshold.


Figure 4
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  		Fig. 4. Water-soluble Zn dynamics during incubation of unamended and biosolids-amended soils. Error bars indicate standard deviation (n = 3).

 

Figure 5
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  		Fig. 5. Visual Minteq-calculated activities (µmol L–1) of the Zn-dissolved organic matter species on Days 0 and 23. Error bars indicate standard deviation (n = 3). Dissolved organic matter was assumed to have a molecular weight of 800 g mol–1 and a C content of 500 g kg–1.

 
Other measured variables known to affect Zn solubility did not exhibit temporal fluctuations that could explain those of water-extractable Zn. Soil pH remained unchanged over time. Additional evidence that Zn solubility was not affected by pH was the fact that neither HCO3– nor Ca2+ concentrations in the water extracts increased on Day 23 (data not shown); in fact they remained unchanged throughout the course of incubation (If the above mentioned concentrations had increased, that would have indicated CaCO3 dissolution due to the acidifying effect of CO2, produced by the pulse of microbial activity described above. That would have decreased pH, and thus it would have affected Zn solubility. However, that was not the case in this study.). Moreover, SOC decreased steadily over time in the amended soils (Fig. 2). Yuan and Lavkulich (1997) found that Zn adsorption decreases when a portion of SOC is removed. Our data suggest that the remaining portion of SOC was sufficiently effective in keeping Zn solubility low and stable over time after the initial flush (Fig. 4). This rather appears to agree with Sloan et al. (1997), who found that most of total Zn concentration, years after application of biosolids, was in relatively stable chemical forms and did not correlate with Zn uptake by crops.


   CONCLUSIONS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS
REFERENCES
 
The time-limited, but significant, flushes of DOC and soluble Zn appear to be induced by re-wetting the biosolids-amended soils in this incubation study. Wetting-drying cycles are not uncommon during the growing season in rain-fed agricultural fields of semiarid Mediterranean climates. Such repeated cycles may induce the release of available metal fractions in higher concentrations than other studies have previously predicted. Flushes of DOC may also occur after biosolids application to soils. Our data suggest that shortly after biosolids application, SOC decreases relatively fast and this may induce an increase in DOC. This effect may also occur in field environments, only over a longer time scale. Also DOC flushes in amended soils are more likely to occur at times when ambient temperatures increase. In the Mediterranean basin significant sudden temperature increases are not uncommon in spring, when crops are also commonly planted. These temperature increases can bring a flush in microbial activity, which causes SOC decomposition. This may in turn induce DOC flushes and thus an enhancement in Zn solubility, which may have significant adverse effects on recently planted crops. More research is needed on the release and plant uptake of soluble fractions of metals as a function of DOC flushes under Mediterranean field conditions when biosolids are applied to soils.


   ACKNOWLEDGMENTS
 
This work was sponsored by the State Foundation for Scholarships (IKY) in Greece under grant number 463/1-12-2003. This support is gratefully acknowledged. We also wish to thank M. Tziouvalekas from the Institute of Soil Mapping and Classification in Larissa, and C. Christofides and E. Tsantila from the Gaia Center of the Goulandris Natural History Museum in Athens for their valuable technical assistance. We are also grateful to the reviewers for their valuable comments.


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





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