Bioresource Technology 102 (2011) 8022–8026

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Bioresource Technology

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Influence of humic substances on bioavailability of Cu and Zn duringsewage sludge composting

Jun Kang a, Zengqiang Zhang a,⇑, Jim J. Wang b

a College of Resources and Environment, Northwest A&F University, Yangling, Shaanxi Province 712100, PR Chinab School of Plant, Environmental and Soil Sciences, Louisiana State University Agricultural Center, 104 Sturgis Hall, Baton Rouge, LA 70803, USA

a r t i c l e i n f o a b s t r a c t

Article history:Received 26 April 2011Received in revised form 14 June 2011Accepted 16 June 2011Available online 23 June 2011

Keywords:Sewage sludgeCompostingHeavy metalsHumic substancesBioavailability

0960-8524/$ - see front matter � 2011 Elsevier Ltd. Adoi:10.1016/j.biortech.2011.06.060

⇑ Corresponding author. Tel.: +86 13609254113.E-mail address: zhangzq58@126.com (Z. Zhang).

Influence of humic substances (HS) on bioavailability of Cu and Zn was characterized during 120 days co-composting of sewage sludge and maize straw. At the initial stage of composting, Cu and Zn in sewagesludge were released as organic matter was degraded, and water soluble Cu and Zn increased markedly.Water soluble Cu and FA content decreased after 21 days whereas water soluble Zn increased during thewhole process. Both HA–Cu and HA–Zn were significantly and positively correlated with HA and H/F,respectively. At the end of composting, the distribution coefficients of HA–Cu and HA–Zn reached27.50% and 3.33% respectively with HA–Cu/HA–Zn ratio increased from 1.29 to 2.73. The results suggestthat Cu combined with HA more strongly than Zn, and composting treatment could decrease bioavailabil-ity of Cu markedly.

� 2011 Elsevier Ltd. All rights reserved.

1. Introduction

Sewage sludge is a by-product of the sewage treatment pro-cesses. It contains high levels of the major plant nutrients, suchas N and P, and is rich in organic matter (Singh and Agrawal,2008; Cheng et al., 2007). Land-application of sewage sludge hasbeen regarded as an effective way of recycling this kind of organicsolid waste (Gao et al., 2008; Wong et al., 2001; Roca-Pérez et al.,2009). On the other hand, some heavy metals, such as Cu and Zn,in sewage sludge could pose a serious environmental risk to theagricultural ecosystem, and consequently threaten human healththrough the food chain (Wei and Liu, 2005; Walter et al., 2006).In general, heavy metals associated with biosolids can have differ-ent impacts on the environment due to the fact that the behaviorand bioavailability of heavy metals are more often dependent oftheir chemical forms rather than total concentrations (Nomedaet al., 2008; He et al., 2009a,b). Therefore, it is important to reducethe bioavailability of toxic metals in order for safely recycling sew-age sludge.

Various methods such as acid treatment, electrodialytic remedi-ation and bioleaching, which result in the dissolution and removalof a significant fraction of heavy metals, have been used prior toland application of sewage sludge (Veeken and Hamelers, 1999;Solisio et al., 2002; Chen et al., 2005). These procedures are gener-ally expensive and potentially risky due to the possibility of

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by-product generation. On the other hand, composting is a stabil-ization process of aerobic decomposition, which has been widelyused for different types of wastes. Research has demonstratedthe reduced bioavailability and crop uptake of heavy metals fromcomposted biosolids as compared to other treated types of sewagesludge (Singh and Agrawal, 2008; Cai et al., 2007). The bioavailabil-ity decreased over the period of composting and maturity (Amiret al., 2005; Haroun et al., 2007, 2009; Liu et al., 2007). This behav-ior has been attributed to the formation of stable metal–humuscomplexes during the composting process (Tandy et al., 2009;Zheng et al., 2007). Therefore, composting processes overall arelikely to contribute to lowering the availability of metals inamended soil compared to other waste biostabilisation techniques(Singh and Agrawal, 2008).

Humic substances (HS), especially humic acids (HA) and fulvicacids (FA), are known for their significant influence on the mobilityand bioavailability of heavy metals in soils (Laborda et al., 2008). Dueto their higher molecular weight and low content of acidic functionalgroups, metal complexes of HA are less soluble, mobile and bioavail-able than those of FA (Xiong et al., 2010). A speciation approach hasbeen developed to differentiate the role of HS (HA and FA) on themobilization of metals from compost (Wang et al., 2010). Mobiliza-tion behaviors of metals have been established according to theirbinding pattern to the mobilized humic substances (Antoniadisand Alloway, 2002). Therefore, investigations about the binding ofheavy metals by HA and FA can help us understand the mechanismsinvolved in reducing the availability of metals during the humifica-tion process.

J. Kang et al. / Bioresource Technology 102 (2011) 8022–8026 8023

In this study, a co-composting experiment of sewage sludge andmaize straw was conducted to evaluate the influence of HS on themobility of Cu and Zn during aerobic composting in order to assessif composting can reduce or enhance the bioavailability of themetals.

2. Methods

2.1. Composting process

Sewage sludge was collected from Yangling Wastewater Treat-ment Plant (Shaanxi Province, China) and mixed with maize straw(d < 5 mm). The mixture contained 57.5% moisture and was charac-terized with a C/N ratio of 25:1. The composting reactor was aforced-aeration static pile system with its inner dimension of0.8 � 0.5 � 0.6 m (length �width � height). The compostingprocess was controlled by a time/temperature-based aeration con-trol system with following settings: aeration rate 0.05 m3/(m3 min)at low temperature (pile temperature <35 �C), aeration rate 0.1m3/(m3 min) at temperature 35–60 �C, and aeration rate 0.2 m3/(m3 min) at high temperature (pile temperature >60 �C). The cool-ing and ventilation interval was 20 min. With the aim of maintain-ing good aerobic conditions during the composting process, themixture was turned manually every week. Temperature was mea-sured daily at ten positions inside the pile. The primary fermenta-tion lasted for 35 days, and the secondary fermentation was85 days. On 0, 21, 35, 63 and 120 days, approximately 2.0 kg com-posite samples were taken from eight positions in the compostingreactor. All samples were homogenized, air-dried, crushed andsieved through a 1 mm sieve for analysis.

2.2. Chemical analysis

Humic acids (HA) and fulvic acids (FA) are two of main fractionsof humic substances (HS) and they are distinguished by solubilityproperties. HA is soluble in base but insoluble in acid, whereasFA is soluble in both base and acid (Laborda et al., 2008). Thehomogenized compost samples as described previously were ana-lyzed for heavy metals and humic fractions based on a sequentialextraction. Water soluble metals and humic substances were ex-tracted using deionized water and a solution of 0.1 MNa4P2O7 + 0.1 M NaOH (pH 13.0) for 24 h at room temperaturewith sample extractant ratio of 1:10 (W/V) respectively. The super-natant solution was then separated from the residues by centrifu-gation at 10,000 rpm for 20 min, and filtered through 0.45-lm

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nt/

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Fig. 1. Changes of HAs content during sewage sludge composting.

filter membranes. The extraction procedure was repeated threetimes. The extracted HA and FA were further separated by precip-itating HA using 5.0 M HCl (24 h at 25 �C, pH 1.5) while FA re-mained in solution. The precipitated fraction contained HA, HA–complexed copper (HA–Cu), and HA–complexed zinc (HA–Zn). Itwas digested with a mixture of HNO3 and HClO4 (1:4, V/V), andanalyzed for HA–Cu and HA–Zn. The supernatant fraction includingFA, FA–complexed copper (FA–Cu), FA–complexed zinc (FA–Zn),Cu2+ and Zn2+. HA and FA were determined by oxidation withpotassium bichromate. The unextracted compost samples were di-gested with a mixture of HNO3 and HClO4 (1:4, V/V), and analyzedfor total Cu and Zn. The concentrations of Cu and Zn in the extractsand digests were determined by a flame atom absorption spectro-photometer (Hitachi Z–5000). All measurements were made intriplicate for each sample and results were presented as the meanof the triplicate. Correlation analysis was conducted with Statisti-cal Analysis System software.

3. Results and discussion

3.1. Evolution of HA and FA

Fig. 1 shows the evolution of HA and FA during the compostingprocess. In general, FA content decreased whereas HA contentunderwent a very significant increase during the primary fermen-tation. Consequently, this resulted in an increase in HA/FA ratio(H/F). The increased HA represented the humification process, indi-cating the maturity of compost (Huang et al., 2006). Furthermore,the increase in the ratio of H/F could be due to either the formationof complex molecules (HA) as a result of polymerization of simplemolecules (FA), or the biodegradation of non-humic or easilydecomposable components of the FA fraction followed by the for-mation of more polycondensed humic structures (Jouraiphy et al.,2005).

3.2. Influence of humic substances on bioavailability of Cu

Compared with the corresponding HA fractions, FA is soluble atall pH values, and has smaller organic free radical contents andsmaller degrees of aromatic ring polycondensation, polymerizationand lower molecular weight (Huang et al., 2006; Plaza et al., 2007;Jouraiphy et al., 2008). Consequently, the bioavailability andmobility of heavy metals may be enhanced when associated withFA. Water soluble Cu enhanced during the first 21 days and thendecreased. (Fig. 2A). The results showed that the concentration ofwater soluble Cu (FA–Cu and Cu2+) was not correlated to FA con-tent (Fig. 2B). Since FA was decreasing during the composting pro-cess (Fig. 1) and there was no metal loss through leaching duringthe course of composting, the increased water soluble Cu waslikely due to the Cu release from initially decomposed organic mat-ter of sewage sludge and the decreased water soluble Cu was thendue to the transformation of FA–Cu and Cu2+ to the solid phase(HA–Cu). After 60 days of composting, water soluble Cu and FAcontent changed only slightly, and the compost was gradually sta-bilized. The hazards of Cu in compost were reduced by decreasingFA concentration.

It has been well documented that high molecular weight com-pounds increased with composting, by increased condensationand aromatization processes which produced more polycondensedhumic acid during composting, a greater degree of condensed, aro-matic character in humic acid (Huang et al., 2006). Therefore, theheavy metals associated with HA, as a solid phase, are insolubleand stable. In this study, HA–Cu increased to 60 days and thenremained stable and was significantly positively correlated withHA content (Fig. 2C). The affinity of HA to Cu, which contributed

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Fig. 2. Changes of water soluble Cu content (A); relationship between water soluble Cu and FA (B), HA–Cu and HA (C), HA–Cu and H/F (D) during sewage sludge composting.

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to the stabilization of Cu, became higher during composting as evi-dent by the significant correlation between HA–Cu and H/F(Fig. 2D). The results were consistent with the known affinity ofCu to organic acids which contributed to the formation of humicsubstances and supported the high affinity of Cu for functionalgroups –OH or –COO of humic substances (Haroun et al., 2009;Chien et al., 2006). These results confirmed that humification pro-cess of organic matter played an important role in reduction inavailability of heavy metals in the compost.

3.3. Influence of humic substances on bioavailability of Zn

Zn is the most mobile and bioavailable heavy metal in sewagesludge and mainly in the easily mobile class at any time of com-posting (Cai et al., 2007; Fuentes et al., 2004). The mobile fractionsof heavy metals tended to decrease through leaching in the courseof composting (Haroun et al., 2007). In this study, there was no Znloss through leaching during composting. Water soluble Zn (FA–Znand Zn2+) increased to 60 days and then tended to remain constant(Fig. 3A), and was significantly negatively correlated with FA con-tent (Fig. 3B). This also suggested that Zn associated with the or-ganic fraction transferred to the mobile fraction and mainlyexisted as free ions. This indicated that the mobility and bioavail-ability of Zn in sludge compost was higher compared to Cu. Onthe other hand, HA–Zn increased throughout the compostingprocess and was significantly positively correlated with HA content(Fig. 3C) and H/F (Fig. 3D). Water soluble Zn was significantly high-er than HA–Zn, and this showed that the affinity of Zn to HA was

weak. Considering the amphoteric characteristics of Zn oxide andits relatively high solubility, Zn was correspondingly more mobileand available for plant uptake after the decomposition process(Haroun et al., 2009). This indicated that the humification processof organic matter could not stabilize Zn.

3.4. Effect of HA on Cu and Zn availability

To follow up the metal distribution during composting, the dis-tribution coefficients of HA–Cu and HA–Zn as the percentage of to-tal metal in the HA form respectively were calculated and used toillustrate the stabilization of Cu and Zn during the composting. Asharp increase in the distribution coefficient of HA–Cu was ob-served during the first two months and it reached 27.50% overthe 120 days period (Fig. 4). On the other hand, the distributioncoefficient of HA–Zn increased gradually and only reached 3.33%during the same period (Fig. 4). Compared with Cu, less Zn wascomplexed with HA and Zn had a lower affinity to humic acids(Fig. 5). The ratio between HA–Cu and HA–Zn increased from1.29 to 2.73 with majority of the increase within 30 days of com-posting process. The result further showed that most of the Znwas not associated with humic acids and Cu had higher affinityto HA than Zn.

4. Conclusions

Both water-soluble Cu and Zn increased initially, suggestingthat these metals were generally released from decomposed

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Fig. 3. Changes of water soluble Zn content (A); relationship between water soluble Zn and FA (B), HA–Zn and HA (C), HA–Zn and H/F (D) during sewage sludge composting.

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Fig. 4. Changes of distribution coefficients of HA–Cu and HA–Zn during sewagesludge composting.

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-Cu/

HA

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Fig. 5. Changes of HA–Cu/HA–Zn during sewage sludge composting.

J. Kang et al. / Bioresource Technology 102 (2011) 8022–8026 8025

organic matter of sewage sludge. Water soluble Cu and FA contentdecreased after 21 days whereas water soluble Zn increased duringthe entire process. The distribution coefficient of HA–Cu reached27.50%, suggesting that the mobility and bioavailability of Cu re-

duced. The HA–Cu/HA–Zn ratio increased from 1.29 to 2.73 overthe composting period. While both HA–Cu and HA–Zn were signif-icantly positively correlated with HA and H/F, the results indicatedthat Cu had higher affinity for HA and was less labile in sludgecompost than Zn.

8026 J. Kang et al. / Bioresource Technology 102 (2011) 8022–8026

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