Journal of Integrative Agriculture 2016, 15(6): 1395–1406

RESEARCH ARTICLE

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Comparative short-term effects of sewage sludge and its biochar on soil properties, maize growth and uptake of nutrients on a tropical clay soil in Zimbabwe

Willis Gwenzi1, Moreblessing Muzava1, Farai Mapanda1, Tonny P Tauro2

1 Department of Soil Science and Agricultural Engineering, Faculty of Agriculture, University of Zimbabwe, Harare, Zimbabwe2 Marondera College of Agricultural Science and Technology, University of Zimbabwe, Marondera, Zimbabwe

AbstractSoil application of biochar from sewage could potentially enhance carbon sequestration and close urban nutrient balances. In sub-Saharan Africa, comparative studies investigating plant growth effect and nutrients uptake on tropical soils amended with sewage sludge and its biochar are very limited. A pot experiment was conducted to investigate the effects of sewage sludge and its biochar on soil chemical properties, maize nutrient and heavy metal uptake, growth and biomass partitioning on a tropical clayey soil. The study compared three organic amendments; sewage sludge (SS), sludge biochar (SB) and their combination (SS+SB) to the unamended control and inorganic fertilizers. Organic amendments were applied at a rate of 15 t ha–1 for SS and SB, and 7.5 t ha–1 each for SS and SB. Maize growth, biomass production and nutrient uptake were significantly improved in biochar and sewage sludge amendments compared to the unamended control. Comparable results were observed with F, SS and SS+SB on maize growth at 49 d of sowing. Maize growth for SB, SS, SS+SB and F increased by 42, 53, 47, and 49%, respectively compared to the unamended control. Total biomass for SB, SS, SS+SB, and F increased by 270, 428, 329, and 429%, respectively compared with the unamended control. Biochar amendments reduced Pb, Cu and Zn uptakes by about 22% compared with sludge alone treatment in maize plants. However, there is need for future research based on the current pot experiment to determine whether the same results can be produced under field conditions.

Keywords: maize growth, nutrient uptake, sludge biochar, soil chemical properties

1. Introduction

Low and declining soil fertility coupled unreliable rainfall constrain crop yields in smallholder cropping systems in sub-Saharan Africa (SSA), resulting in low yields (<1.5 t ha–1) compared to 12 t ha–1 attained in commercial sector (Mtambanengwe and Mapfumo 2009). Research on soil fertility in smallholder cropping systems in SSA focussed on three options: (1) harnessing biological nitrogen fixation by incorporating leguminous crop and agroforestry species

Received 21 May, 2015 Accepted 24 July, 2015Correspondence to Willis Gwenzi, Mobile: +263-771585936, Tel: +263-4-303211, Fax: +263-4-307034, E-mail: wgwenzi@yahoo.co.uk

© 2016, CAAS. Published by Elsevier Ltd. This is an open access art ic le under the CC BY-NC-ND l icense (http:/ /creativecommons.org/licenses/by-nc-nd/4.0/).doi: 10.1016/S2095-3119(15)61154-6

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(Mapfumo et al. 1999), (2) use of local available resources such as animal manure, leaf litter, termitaria, and crop residues, and (3) use of inorganic fertilizers, and their com-bination with organic fertilizers. Although yield increases have been reported in most cases, their adoption remains low due to several constraints including availability, quantity and quality (Mapfumo and Giller 2001).

Earlier efforts to improve soil fertility were limited to rural farmers, thus excluded urban and peri-urban agroecosys-tems, an emerging source of livelihoods and food security in Africa. Sewage sludge has become an important nutrient resource for urban and peri-urban farmers in Zimbabwe (Katanda et al. 2007), largely because, compared to in-organic fertilizers which are expensive, sewage sludge is readily and freely available from wastewater treatment systems. However, high levels of pathogens and heavy metals in sewage sludge pose significant environmental and public health risks. Pyrolysis of sludge into biochar, and subsequent application to soils could potentially reduce the risks (Fytili and Zabaniotou 2008) while simultaneously sequestering soil carbon and enhancing soil quality (Gwenzi et al. 2015). Biochar, a carbon rich, fine-grained, porous substance has shown to have several properties that could enhance plant growth and heavy metal adsorption. Biochar feedstocks include crop residues, wood waste, yard trashes, manures and sewage sludge (Duku et al. 2011; Gwenzi et al. 2015).

Pyrolysis of sludge into biochar can form part of sus-tainable integrated fertility management for improved crop productivity and food security, while minimizing potential public health risks associated with the use of raw sludge in urban and peri-urban areas of sub-Saharan Africa. Available studies on the effects of biochar were predominantly con-ducted in other continents such as Australia, South America, Europe, North America, and Asia (Glaser et al. 2002; van Zwieten et al. 2010; Haefele et al. 2011), while limited data are available in Africa. Most of the studies focused on the effects of biochar on agronomic performance, carbon sequestration, soil fertility, and greenhouse gas emissions. Comparative studies investigating the effects of biochar to its raw feedstocks are still limited especially in Africa. Moreover, little research has been conducted on the effects of sludge biochar on soil properties, plant growth and nutrient uptake on typical tropical soils as those in sub-Saharan Africa. Few available studies on sludge biochar conducted in China and Australia focussed on effects of pyrolysis temperature on nutrient content (Hossain et al. 2011), and garlic yield and heavy metal accumulation (Song et al. 2014), respectively. Given that urban and peri-urban farmers in SSA are using sewage sludge as a fertilizer amendment, there is need to find ways to reduce the health risks from pathogen and heavy metals while at the same time increasing food

security at the household level. The main objective was to compare the short-term effect of sludge and its biochar derivative on maize growth, heavy metal uptake and soil chemical properties.

2. Results

2.1. Chemical characteristics of soil, sewage sludge and biochar

The soil used for this study had inherently low nutrient content compared to both the sludge and biochar. The soil had a near-neutral pH coupled with an electrical conductivity value of 0.35. In addition, the soil had the least total N, P and Ca which were consistent with the least cation exchange capacity (CEC) compared to biochar and sludge. However, the soil had a considerable amount of K and Mg (Table 1). Organic amendments used had appreciable levels of Mg and Ca but contained low potassium. Sewage sludge had higher total N and %C (C percent) than biochar while the total P and K of the two amendments were similar. A lower electrical conductivity (EC) value was observed in biochar (1.1 dS m–1) than in sewage sludge (2.85 dS m–1) (Table 1). Biochar had about a unit higher pH than that of sludge. The concentrations of Pb, Cu, Ni, and Zn in the biochar were similar to those of the sludge.

2.2. Maize growth and biomass partitioning

The final plant height and total number of leaves for biochar and biochar+sludge were comparable to those of inorganic fertilizer (compound D (7% N:14% P2O5:7% K2O)+ammoni-um nitrate (AN, 34.5% N)) and sewage sludge (Fig. 1). For both height and number of leaves, biochar alone showed no significant differences with the unamended control during the early stages of plant growth until around day 21. Thereafter, a sudden increase in growth is observed. As expected, the unamended control had significantly lower growth response in terms of both height and leaves productivity than the other treatments (Fig. 1).

Inorganic fertilizer (compound D+AN) and sludge+AN treatments attained the highest (P<0.05) total biomass (shoot+root) while the unamended control had the least. Sludge+biochar and biochar had similar total biomass (Fig. 2-A). Raw sludge had the highest shoot biomass (>70 g pot–1) while unamended control attained the least shoot biomass (~10 g pot–1). Shoot dry biomass for treat-ments involving biochar (sludge+biochar, biochar) were comparable to those of inorganic fertilizer (compound D+AN) but lower than raw sludge (Fig. 2). However, there are contradictions between the trend for total biomass and those for biomass partitioning into roots and shoots across

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Table 1 Chemical properties of soil, sewage sludge and sewage sludge biochar used in the experiment

Parameter Soil Raw sludge Sludge biochar European Community maximum limit2)

Soil:H2O extract 7.2±0.05 7.55±0.03 a 8.54±0.08 bEC (dS m–1) 0.35±0.01 2.85±0.02 a 1.1±0.00 bCEC (cmol(+) kg–1) 85.0±0.1 220±0.7 a 140±0.4 bTotal P (%) 0.09±0.03 0.13±0.01 a 0.11±0.00 aTotal organic C (%) 1.87±0.13 32.8±0.02 a 5.62±0.00 bTotal N (%) 0.06±0.00 2.6±0.02 a 0.69±0.02 bC/N ratio 32.4±1.36 12.6±0.10 a 8.2±0.25 bCa (g kg–1) 0.11±0.03 25.1±2.4 a 19.9±0.7 bMg (g kg–1) 12.0±1.2 32.9±1.4 a 35.9±3.9 aK (g kg–1) 8.6±0.9 2.6±0.3 a 3.0±0.4 aNa (g kg–1) 0.64±0.05 1.8±0.1 a 2.0±0.10 aPb (mg kg–1) 25.8±3.7 106.0±5.6 a 112.7±3.7 a 750Cu (mg kg–1) 342.8±43.4 343.8±53.4 a 307.8±12.6 a 1 000Zn (mg kg–1) 135.5±8.7 563.7±0.2 a 548.8±10.7 a 2 500Ni (mg kg–1) 39.3±2.9 37.7±4.0 a 41.67±2.7 a 3001) EC, electrical conductivity; CEC, cation exchange capacity.2) European Community, the maximum allowable concentrations for heavy metals in sludge for land application are also shown for

comparison.Data are means±standard error of the means for three replicates. Mean data within a row with different letters denote significant differences between sewage sludge and sludge biochar at probability level P=0.05 based on t-test. The same as below.

Fig. 1 Effects of different soil amendments on mean number of leaves (A) and plant height (B). Control, unamended control; SB+AN, sludge biochar+AN; SS+AN, sewage sludge+AN; SS+SB+AN, sewage sludge+sludge biochar+AN; D+AN, compound D+ammonium nitrate (AN). Error bars denote the standard error of the mean. The same as below.

treatments. Inorganic fertilizer accumulated significantly (P<0.05) higher shoot biomass (>65 g pot–1) than those of sewage sludge, biochar and sludge+biochar (Fig. 2). Biochar alone and the unamended control had significantly (P<0.05) lower root biomass than the other treatments. Consequently, root:shoot ratios varied significantly among soil amendments. Treatments without organic amendments (control and inorganic fertilizer alone) significantly enhanced biomass partitioning into roots than those with sewage sludge and biochar (Fig. 2-B).

2.3. Nitrogen (N) and phosphorus (P) uptake

Nitrogen uptake was higher than P uptake across all treat-ments (Fig. 3). Nutrient uptake followed a similar pattern across all treatments with inorganic fertilizer (compound D+AN) and raw sewage sludge having the highest values while unamended control had the least uptake. Biochar applications had lower nutrient uptake than sewage sludge which was comparable to inorganic fertilizer. SB+AN and SS+SB+AN treatment had similar uptake for both nitrogen and phosphorus (Fig. 3).

2.4. Potassium (K), magnesium (Mg) and calcium (Ca) uptakes

Across all treatments uptake of cations followed the general trend: K>Mg>Ca (Fig. 4). Similar to N and P uptakes, basic cations uptake followed the same pattern, with inorganic fertilizer (compound D+AN) and raw sewage sludge having the highest values (P<0.05) while the unamended control had

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Fig. 2 Total, root and shoot dry biomass values (A) and root:shoot ratios (B) for different soil amendments at 49 days after mergence. Means with different letters are significantly different at P=0.05.

the least uptakes. The application of organic amendments reduced the amount of basic cations taken up by the crop with addition of biochar significantly (P<0.05) causing the reduction.

2.5. Zinc (Zn), nickel (Ni), copper (Cu), and lead (Pb) uptakes

A significant (P<0.05) reduction in Zn, Cu and Pb uptakes was noted following application of 15 t ha–1 biochar com-pared to sludge, sludge-biochar mixture and inorganic fertilizers (Fig. 5). Cu uptake varied significantly (P≤0.001) among all treatments. Zn uptake for sewage sludge and sludge-biochar mixture were similar to that of inorganic fertilizer. The unamended control had the least heavy met-al uptake except for Ni, which showed no clear trend. As expected, uptakes of Zn and Cu, which are essential plant nutrients was an about an order of magnitude higher than that of the non-essential Ni and Pb.

2.6. Post-harvest soil chemical properties

The concentrations of Ca, Mg, Zn, Cu, Pb, pH, EC, and CEC

varied significantly (P<0.05) among treatments (Table 2). Biochar treatments significantly (P<0.05) increased soil pH relative to inorganic fertilizer, but both were similar to that of sludge and unamended control. Biochar-amended soils had generally higher concentrations of Pb and Zn than the other treatments. Treatments incorporating sludge, biochar and inorganic fertilizer significantly increased salinity compared to the unamended control. Soil P, N, C, C/N ratio, K, and Na were comparable among all treatments. CEC values for sludge and sludge-biochar mixture were similar or high-er than that of biochar combined with ammonium nitrate. Except for Pb and CEC, the effects of biochar application on soil properties were most evident when compared to inorganic fertilizer and the unamended control, but were almost negligible when compared to sludge.

3. Discussion

3.1. Initial characterization

The soil used for this study was inherently infertile (low N, P, Ca, and CEC) and typical of most tropical clay soils in sub-Saharan Africa. Low fertilizer applications and nutrient mining could also contribute to the observed low fertility.

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Biochar used in current study had a basic pH consistent with other studies that attributed this fact to the formation of carbonates and polymerization/condensation reactions during pyrolysis (Méndez et al. 2005). Several authors also observed an increase in soil pH when biochar was applied to soil (Laird 2008; van Zwieten et al. 2010). In cases where the soil pH is below optimal for maize production, a rise in pH can provide a wide range of benefits in terms of soil quality, notably by chemically improving availability of plant nutrients, and in some cases by decreasing the availability of detrimental elements such as Al and heavy metals (Laird 2008).

Earlier studies have shown that metal concentrations are often higher in biochar than in raw sludge (Hossain et al. 2011; Song et al. 2014). Contrary to this trend, our results generally showed no statistical differences in metal concentrations between raw sludge and sludge biochar, although Ni, Pb, Na, K, and Mg were marginally higher in

biochar than raw sludge. Note that the effects of increasing pyrolysis temperature on heavy metal concentrations in sludge biochar are inconsistent and seem to vary among studies. For example, Song et al. (2014) observed that heavy metal concentrations peaked at 450°C, and then de-creased at 500 and 550°C. Hossain and co-authors (2011) showed that heavy metal concentrations in sludge biochars produced at pyrolysis temperature ranges of 300–700°C tended to decrease at 700°C except for Cd. Although the reasons for the contradictions between our findings and those of earlier studies (e.g., Hossain et al. 2011; Song et al. 2014) are unclear, this could reflect differences in feedstock quality and pyrolysis conditions such as heating rates, peak temperatures and pyrolysis duration.

Although Zimbabwe lacks maximum guideline limits for concentration of heavy metals in sludge for land application, the concentrations of Zn, Cu, Ni, and Pb were below the European Community maximum allowable concentrations of 2 500, 1 000, 300, and 750 mg kg–1 dry weight (Change et al. 2002), implying limited risk for soil and groundwater contamination. Moreover, the concentrations of Ni and Zn were generally lower than those reported in earlier studies conducted in Zimbabwe (Nyamangara and Mzezewa 2001; Mapanda et al. 2005), where industrial effluents have been implicated as the main source of heavy metal on sewage and sludge amended soils.

3.2. Maize growth and biomass production

Biochar combined with sewage sludge (SS+SB) and sewage sludge alone (SS) had plant growth and number of leaves similar to inorganic fertilizer, suggesting that they can effec-tively be used as soil fertility amendment in combination with inorganic fertilizer without adverse impacts of plant growth. Before top dressing (from germination to 21 d), biochar alone showed no significant difference with the unamended control in terms of plant height and number of leaves at (P<0.05) confirming earlier studies that biochar is not a fertiliser. Generally, reduced growth is regularly reported with biochar without fertilizer (Novak et al. 2009). Blackwell et al. (2010) also reported neutral and negative plant growth responses with biochar only. The nutrient content of biochar was generally comparable to that of sludge, except of N which tends to volatilize during pyrolysis (Laird 2008). In a sepa-rate study investigating the effects of organic amendments and biochar on nitrogen mineralisation and immobilisation potential of soil release patterns, immobilization during the first 21 d, followed by a flush of N release (Mupunga 2014). This might also be another possible explanation to slow growth with biochar during the early stages of maize growth.

The high total biomass attained from sewage sludge which was similar to that of inorganic fertilizer indicates

Fig. 4 Mean values of K (A), Mg (B) and Ca (C) uptakes at 49 d after crop emergence.

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the high nutrient supply power of sewage sludge. Low total biomass attained from biochar and sludge+biochar further confirms the notion that biochar is not a fertilizer. In consistence with previous studies, sewage sludge was reported to have high levels of nutrients and can be used as a substitute for inorganic fertilizers (Toory et al. 2003). However, the major drawback in utilisation of sewage sludge might be health related and the issue of bioaccumulation of heavy metals (Tandi et al. 2004; Mapanda et al. 2005).

The inorganic fertiliser treatment had higher nutrient uptake than organic amendments probably due to high solubility of mineral fertilizer. A significant increase in the dry matter production of wheat was observed when N fertiliser was combined with biochar in an experiment carried out by Blackwell et al. (2010). The low total biomass attained in the control further confirms that the soil used for this study was inherently infertile. Application of organics and fertilizer subsequently increased biomass accumulation amongst

Table 2 Effects of different treatments on post-harvest soil chemical properties

Parameter Biochar+AN1) Compound D+AN Control Sludge+AN Sludge+Biochar+ANSoil:H2O extract 6.6±0.0 a 5.4±0.3 b 6.7±0.1 a 6.2±0.3 a 6.4±0.2 aEC (µS cm–1) 306.7±19.1 ab 350.7±60.9 a 108.4±2.3 c 274.3±5.0 ab 221.3±30.4 bcCEC (cmol(+) kg–1 66.2±2.0 b 80.7±6.8 a 63.7±0.6 b 78.8±0.73 a 71.5±1.4 abTotal P (g kg–1) 0.67±0.02 a 0.74±0.09 a 0.68±0.02 a 0.76±0.10 a 0.75±0.04 aTotal C (%) 2.04±0.13 a 2.00±0.18 a 1.56±0.45 a 2.43±0.40 a 1.93±0.11 aTotal N (%) 0.16±0.02 a 0.18±0.01 a 0.18±0.02 a 0.21±0.01 a 0.21±0.02 aC/N ratio 13.2±2.8 a 11.4±1.0 a 9.0±3.0 a 11.5±2.4 a 9.64±1.51 aCa (g kg–1) 4.76±0.22 a 3.7±0.9 a 5.02±0.19 a 2.75±0.79 a 3.00±0.98 aMg (g kg–1) 7.25±0.96 ab 5.76±0.88 b 8.17±0.68 ab 7.07±1.60 ab 10.2±1.58 aK (g kg–1) 16.4±0.7 a 16.1±1.8 a 17.2±0.7 a 17.3±2.6 a 15.9±0.9 aNa (g kg–1) 0.42±0.18 a 0.57±0.27 a 0.91±0.65 a 1.64±0.50 a 0.77±0.45 aPb (mg kg–1) 28.4±0.8 a 22.3±0.3 b 21.2±0.1 b 23.1±0.4 b 26.7±0.2 aCu (mg kg–1) 544.7±2.5 a 467.2±4.2 b 546.0±3.0 a 536.8±5.7 a 531.8±3.92 aZn (mg kg–1) 781.5±79.7 a 561.0±54.5 b 634.5±5.2 ab 633.0±41.4 ab 721.5±33.0 aNi (mg kg–1) 65.8±1.5 a 61.33±5.8 a 68.5±1.8 a 66.3±5.9 a 66.8±1.86 a1) AN, ammonium nitrate.

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different treatments. The results revealed that in the presence of N fertilizer,

there was an increase in yield for soils with biochar additions, in comparison to those with N fertilizer alone. Improved fer-tilizer-use efficiency was thus shown as a major positive fea-ture of the use of biochar. This means that sludge+biochar can be as good as compound D basal fertilizer but sludge biochar alone can give poor result except in cases where an inorganic fertilizer is added. The improved biomass pro-ductivity and fertilizer use efficiency obtained by combining biochar and inorganic fertilizer is particularly important in urban and peri-urban areas in sub-Saharan Africa, where low and declining soil fertility is one of the major constraints to improve crop yields. This finding corroborates an earlier results showing that combining biochar and inorganic fertil-izer enhanced soil fertility on a degraded soil, and more than doubled crop yields compared to the unamended control (Kimetu et al. 2008). Resource-constrained poor farmers often apply organic and inorganic fertilizer rates lower than the recommended optimum amounts. In this regard, our results suggest that combining biochar with lower fertilizer rates could potentially give higher yields than fertilizer alone possibly due to the synergistic effects of combining biochar and fertilizer. The multiple beneficial effects of biochar ap-plication to soil physical, chemical and biological properties have been documented in several studies (Glaser et al. 2002; Kimetu et al. 2008; Gwenzi et al. 2015)

Although results of short-term experiment should be interpreted with cautions, insights from this study suggest that biochar has beneficial effects on soil chemical proper-ties, biomass productivity and nutrient uptake compared to the unamended control. The findings suggest that resource-poor smallholder famers can use sludge biochar or sludge combined with sludge biochar as a substitute for basal inorganic fertilizer and attain biomass yield more than double that of the unamended control. In smallholder cropping systems, organic amendments serve multiple purposes including carbon sequestration, improvement of physical and chemical properties and supply of essential plant nutrients. Considering that biochar alone tends to have low N due to volatilization, combining sludge and its biochar provides a compromise to simultaneously improve soil properties and supply essential plant nutrients especially N. Unlike inorganic compound basal fertilizers which are expensive, sludge biochar is likely to be available for free or cheaper, thereby potentially offsetting the marginal yield benefit associated with basal inorganic fertilizer. Compared to the current practice of using raw sludge in urban and peri-urban agriculture, pyrolysis into biochar could also reduce the public health risks associated with handling raw sludge. Due to the recalcitrant nature of biochar, the effects could persist longer than that of inorganic fertilizers and raw

sludge. However, several factors still constrain the large-scale application of biochar in smallholder cropping systems in Africa, including: (1) lack of appropriate pyrolysis systems for producing large quantities of biochar at affordable costs; (2) lack of long-term data on optimum application rates and frequencies, and persistence of biochar affects following one-off applications.

Partitioning of biomass for maize is expected to be in the ratio of 2:1 (shoot:root biomass). The current study revealed that the organic amendment (biochar, sludge+biochar and sludge) encourages the expected partitioning in favour of the shoot biomass. This is in consistence with previous studies which demonstrates a beneficial effect of the organic matter on the soil biological and physical properties, plus the improvement of soil fertility. The improved plant biomass on biochar amended soils was attributed to the fact that biochar contains significant amounts of plant nutrients such as K, Ca and Mg, increases soil pH of acidic soils and reduces exchangeable acidity (Uzoma et al. 2011; Mutezo 2013). The availability of resources such as water and nutrients is a key determinant of biomass production and its partitioning between roots and shoots (Bonifas et al. 2005; Benjamin et al. 2014). Plants that encounter limited nutrient or water supply are expected to partition more biomass to their roots and less to their stems and leaves (Bonifas et al. 2005). Therefore, the significant differences in root:shoot ratio among the treatments could reflect resource availability under the different treatments. However, it is unclear from the pot experiments whether this translates into more grain yield in sludge and biochar amended soils than the control and inorganic fertilizer. Since grain yield was not measured in this pot experiment, this therefore warrants further inves-tigation through field evaluation.

3.3. Nutrients uptake and residual soil status

Maize has high demand for N as indicated by the high N up-take compared to P across all treatments. The high uptake of N is linked to the high demand for protein production being utilised in crop development (vegetative and reproductive stages) while P is mostly required to boost early root devel-opment resulting in uptake of other soil nutrients for plant development. The uptake trend for K>Mg>Ca in this study confirms that maize has higher requirement for K than Ca. Nutrients levels in biochar amendments were significantly lower than those of inorganic fertilizer and sewage sludge. Comparing sewage sludge and biochar to inorganic fertiliser, previous studies also showed that organic amendments need to undergo the mineralization process first for nutrients to be available for plant uptake (Lehmann 2003). The high uptakes of K, Mg and Ca under inorganic fertilizer indicate that fertilizer supply readily available nutrient to the crop.

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Micronutrients are necessary for crop production, but in much smaller quantities than major elements. The most commonly needed micronutrient in maize production is Zn and Mn. Although sludge biochar and sewage sludge have shown to have high concentrations of Zn, the use of biochar treatments together with sewage sludge has shown to decrease the uptake of the heavy metal even to levels that do not cause phytotoxicity. This is in consistence with previous studies which reported that biochar had the ability to reduce the mobilities of Cu, Ni and Cd in the soil making them unavailable for plant uptake (Beesley et al. 2010). Other studies also reported that biochar was more efficient than compost in decreasing the bioavailabilities of Zn and Cd, because biochar can raise the soil pH above compost (van Zwieten et al. 2010; Uzoma et al. 2011; Cornellisen et al. 2013). Similarly, our biochar had the same liming effect on the soil due to the high ash content. This can result in a decrease in the bioavailability of heavy metals (Beesley et al. 2010). In contrast to the expected decrease in heavy metal uptake, biochar effect on Ni uptake showed no consistent trend. The reason for this was unclear but could be due to high variability inherent in the data.

The CEC of biochar-amended soils was similar to that of the unamended control and lower than that of inorganic fertilizer, indicating no obvious short-term effect. Previous findings are also inconsistent; some studies showed an increase in CEC after biochar application (Chan et al. 2008; Uzoma et al. 2011) while others reported a decrease in CEC or no effect (Novak et al. 2009; Schulz and Glaser 2012). Although the mechanisms accounting for the inconsisten-cies are unclear, this could reflect differences in biochar properties and soil types. Application of biochar generally enhanced the retention of heavy metals especially Pb and Zn in the soil, probably due to high surface area associat-ed with biochar and reduced solubility and bioavailability caused by a rise in soil pH.

The concentrations of Zn, Cu, Pb, and Ni in the post- harvest soils were generally higher than that of the soil, bio-char and sludge, partly because post-harvest samples were collected from the amended top 15-cm layer rather than the entire experimental pot. The high clayey content (60–64%) of the experimental soil (Mapanda et al. 2012) coupled with the high heavy metal retention of biochar in the top layers could account for the heavy metal enrichment in the top 20 cm. In addition, although the concentrations of heavy metals compound D and ammonium nitrate were not measured in the current study, there is a possibility that inorganic fertilizers may contain heavy metals in various concentrations, largely derived from raw materials such as rock phosphate for P fertilizers. Indeed, high concentra-tion of heavy metals in the rock phosphate used to make P fertilizers in Zimbabwe is a key factor undermining the

use of rock phosphate as a fertilizer (Dhliwayo 1999), and similar results have been reported elsewhere (Hellums 1995; Iretskaya et al. 1998). Zhang et al. (2010) reported that high- and low-ash biochar have the ability to decrease the mobility of Cd, Cu and Ni in the soil. Other studies also showed that biochar can adsorb a variety of heavy metals, including Pb, As and Cd (Cao et al. 2009). Overall, the concentrations of Zn, Cu, Ni, and Pb were lower than the maximum permissible concentrations of 450, 200, 100, and 300 mg kg–1 recommended for sludge-amended soils (FAO 1992). Biochar application had no effect on soil N, P and K suggesting no short-term nutrient benefit compared to the other treatments.

4. Conclusion

Overall, the results showed that short-term application of sew-age sludge and its biochar significantly improves soil chemical properties and enhances maize growth, biomass productiv-ity, elemental uptake and reduces heavy metal uptake. In particular, combining sewage sludge and its biochar could act as a substitute for compound D basal fertilizer, which is expensive for resource-poor farmers in urban and peri-urban areas. The observed increase in pH on soils amended with biochar demonstrates its liming capacity, which is essential for overcoming Al toxicity on acid tropical soils prevalent in sub-Saharan Africa. Biochar also enhanced the retention of heavy metals especially Pb and Zn, which could preclude their mobility and leaching into groundwater, which is a key source of water for potable supply. However, the high C:N ratio of biochar could induce short-term immobilization of N, which in turn suppresses initial plant growth. Moreover, a significant quantity of feedstock N is lost through the process of volatilization during sludge pyrolysis. Further research should investigate the effects of different biochar types and application rates on crop productivity, soil quality and green-house gas emissions across different soils and cropping systems in sub-Saharan Africa.

5. Materials and methods

5.1. Sludge and biochar production and characterization

The study involved use of sewage sludge, sludge biochar and their combination in a 1:1 ratio. Sewage sludge was obtained from a sewage treatment plant in Harare that uses conventional biological trickling filtration system and the biological nutrient removal system. The sludge was air-dried and sieved through a 10-mm sieve to produce about 100 kg of thoroughly mixed sludge. The sludge was divided into two equal proportions. One of the proportions was fed into a 0.2-m3 drum pyrolysis reactor and subjected

1403Willis Gwenzi et al. Journal of Integrative Agriculture 2016, 15(6): 1395–1406

to slow pyrolysis to produce biochar (Gwenzi et al. 2015). The reactor was fired using coal and operated at 300–500°C for 6 h following results of preliminary work.

Air-dried sewage sludge and biochar were separately crushed and sieved through a 2-mm sieve for laboratory analysis and use in the pot experiment. The pH, electrical conductivity (EC), total organic C, total N, total P, Zn, Ni, Pb, Cu, exchangeable Na, K, Ca, and Mg and cation exchange capacity (CEC) were determined on triplicate samples of sludge and biochar using standard methods (Okalebo et al. 2002). EC and pH were measured using an EC meter (Thermo Orion 920A) and digital pH meter (Model: Philips W409), respectively in distilled water at 5% (w/v) after shaking at 100 r min–1 for 1 h. Total C was determined by the modified Walkley-Black method using dichromate solution in the presence of concentrated H2SO4 following procedures in Okalebo et al. (2002). For total P, heavy metals and basic cations, sludge and biochar samples were digested using the aqua regia method (Kenkel 1988). Total P was determined colorimetrically from the soil extract using ammonium-paramolybdate reagent for colour development followed by determination of absorbance using a UV-visible spectrophotometer at 660 nm. Total N was determined us-ing the Kjeldahl method (Bremner 1996). Other elements such as Zn, Ni, Pb, Cu, Ca, and Mg in the digests were determined using the atomic absorption spectrophotometer (Model: Varian 220), while Na and K were determined by flame emission (Okalebo et al. 2002).

5.2. Experimental set up

The pot experiment was conducted under ambient condi-tions at University of Zimbabwe, Harare. A red fersiallitic clay soil classified as Harare 5E.2 according to the Zimbabwe soil classification, and very fine kaolinitic, thermic rhodic Paleustalf according to United States Department of Agri-culture (USDA) classification (Nyamapfene 1991) was used. Surface (0–20 cm) soil was collected, air-dried and passed through a 10-mm sieve to remove plant debris and stones.

Five treatments were tested in the pot experiment: Unamended soil (control), representing low-input urban

and peri-urban cropping systems; sewage sludge (SS) at 15 t ha–1+ammonium nitrate (AN, 34.5% N) at 350 kg ha–1 (SS+AN); sewage sludge biochar (SB) at15 t ha–1+AN at 350 kg ha–1 (SB+AN); sewage sludge (SS) at 7.5 t ha–1+sew-age sludge biochar (SB) at 7.5 t ha–1+AN at 350 kg ha–1 (SS+SB+AN); and inorganic fertilizers only, compound D (7% N:14% P2O5:7% K2O) at 300 kg ha–1+AN 350 kg ha–1 (D+AN), representing recommended fertilizer practice for commercial maize.

The amendments and soil were thoroughly mixed and

packed in 0.02 m3 plastic pots (height: 0.3 m) with holes at the bottom to facilitate free drainage. The lower 15-cm of the pots was packed with unamended soil, underlying a 15-cm layer of the amended soil. To ensure uniform packing for each layer, the pots were swivelled manually in a circular motion during pot filling. More soil was added until a no volume change occurred. A head space of approximately 5 cm was left on top of the 15-cm amended soil to avoid water running off during irrigation. This yielded to approxi-mately 0.016 m3 of soil in each pot, with an initial estimated maximum bulk density of 1.3 g cm–3. 300 kg ha–1 of com-pound D was broadcasted on the soil surface and turned in manually to a depth of 5 cm. The pots were arranged in a completely randomized design (CRD) with four replicates for each treatment.

Four seeds of maize (variety: SC513) were sown in each pot and then thinned to two plants per pot 5 days after emergence. Pots were kept weed-free by hand pulling. Pots were watered weekly during the course of the experiment except after main rainfall events (Fig. 6). Top dressing fertilizer was applied as a single application in each pot at 4 wk after emergence except for the un-amended control.

5.3. Plant measurements

Plant height and number of leaves per plant were determined weekly for five consecutive weeks using a tape measure and counting respectively. This was done from 14 d after emergence to capture plant growth dynamics to 49 d after crop emergence. At the end of the 49 d, maize plants from each pot were cut at the first internode just above soil surface using knives. The root system was also carefully removed from the pots. Both above and below biomass samples were washed with distilled water and left under shade for 4 d to air dry. After 4 d the plants (shoot and roots) were oven-dried at 65°C until a constant weight was reached. Total dry shoot and dry root biomass were determined.

5.4. Plant and soil sampling and laboratory analyses

Dry shoot and root biomasses were ground to pass through a 2-mm sieve using a grinder (model: Thomas Willy mill grinder, model 4). 1 g of the sample was weighed into 30 mL silica crucibles. The crucibles were placed in a muffle fur-nace (model: Wildbarfield M1354) housed in a fume hood. The samples were ashed at 450°C for 24 h (Hanlon 1992). 5 mL of aqua regia was added to ash in the crucibles and the mixture was covered with watch glasses and digested on a hot plate (model: Philips 492–11) at 105°C and 50 cycles min–1 for 30 min. The sample was then made to 50 mL with

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distilled water and filtered through a Whatman No. 54 filter paper. Total P, total N, Zn, Ni, Pb, Cu, Na, K, Ca, and Mg in the digests were determined following procedures described for biochar and sewage sludge.

Post-harvest soil samples were collected from the top 15-cm layer, corresponding to the amended portion for treatments incorporating raw sludge or sludge biochar. Soil samples were dried and passed through a 2-mm sieve. The soil samples were analysed for parameters as described for initial characterization.

5.5. Data analysis

Data were first tested for homogeneity of variances and normality using Levene’s and Kolmogorov Smirnov tests, respectively. A two-sample t-test was used to compare chemical properties of raw sewage sludge to that of sludge biochar. One-way analysis of variance was used to test the effects of the soil amendments on plant growth, uptake of nutrients, heavy metals and post-harvest soil chemical properties. The Fisher’s test was used for the separation of treatment means. Kruskal-Wallis test was used for testing effects of soil amendments on non-normal data that could not be transformed. Minitab® 16 statistical software (Minitab Inc. 2010) was used for all statistical analysis at probability level P=0.05.

Acknowledgements

The authors are grateful to the Swedish International Foundation for Science (IFS) (C-5266-1) awarded to Willis Gwenzi for funding the research. We also thank the anony-mous reviewers and editorial team for comments that greatly

improved the manuscript.

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