Sewage Sludge Biochar Influence upon Rice (Oryza sativa L) Yield

Article pubs.acs.org/est

Sewage Sludge Biochar Influence upon Rice (Oryza sativa L) Yield, Metal Bioaccumulation and Greenhouse Gas Emissions from Acidic Paddy Soil Sardar Khan,†,‡ Cai Chao,† Muhammad Waqas,‡ Hans Peter H. Arp,§ and Yong-Guan Zhu†,* †

Key Lab of Urban Environment and Health, Institute of Urban Environment, Chinese Academy of Sciences, Xiamen, China Department of Environmental Science, University of Peshawar, Pakistan § Department of Environmental Engineering, Norwegian Geotechnical Institute, Ullevål Stadion, Oslo, Norway ‡

S Supporting Information *

ABSTRACT: Biochar addition to soil has been proposed to improve plant growth by increasing soil fertility, minimizing bioaccumulation of toxic metal(liod)s and mitigating climate change. Sewage sludge (SS) is an attractive, though potentially problematic, feedstock of biochar. It is attractive because of its large abundance; however, it contains elevated concentrations of metal(loid)s and other contaminants. The pyrolysis of SS to biochar (SSBC) may be a way to reduce the availability of these contaminants to the soil and plants. Using rice plant pot experiments, we investigated the influence of SSBC upon biomass yield, bioaccumulation of nutrients, and metal(loid)s, and green housegas (GHG) emissions. SSBC amendments increased soil pH, total nitrogen, soil organic carbon and available nutrients and decreased bioavailable As, Cr, Co, Ni, and Pb (but not Cd, Cu, and Zn). Regarding rice plant properties, SSBC amendments significantly (P ≤ 0.01) increased shoot biomass (71.3−92.2%), grain yield (148.8−175.1%), and the bioaccumulation of phosphorus and sodium, though decreased the bioaccumulation of nitrogen (except in grain) and potassium. Amendments of SSBC significantly (P ≤ 0.05) reduced the bioaccumulation of As, Cr, Co, Cu, Ni, and Pb, but increased that of Cd and Zn, though not above limits set by Chinese regulations. Finally regarding GHG emissions, SSBC significantly (P < 0.01) reduced N2O emissions and stimulated the uptake/oxidation of CH4 enough to make both the cultivated and uncultivated paddy soil a CH4 sink. SSBC can be beneficial in rice paddy soil but the actual associated benefits will depend on site-specific conditions and source of SS; long-term effects remain a further unknown.

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INTRODUCTION Biochar application into agricultural soil has recently attracted attention due to its potential agronomic, economic, and environmental benefits. Biochar is a carbon (C) rich material produced by pyrolyzing waste biomass between 250 and 900 °C under continuous flow of nitrogen or anoxic conditions.1−6 Examples of waste biomass used for biochar include hard woods, corn stover, rice straw, rice husks, bamboo, wheat straw, peanut hulls, poultry litter, and animal manures.2,4−6 The prospect of converting sewage sludge (SS) to biochar (SSBC) presents a potential economic opportunity. SS is produced in massive quantities, for instance 6.2 million metric tons dry weight is estimated to be produced per year in the United States.7 Use of SS in agriculture is heavily restricted, because of associated pathogens and contaminants. However, conversion into SSBC may not only allow for a safer soil amendment but potentially a useful fertilizer and greenhouse gas (GHG) mitigator.8−10 Biochar often has an increased, negatively charged surface area compared to soil and can be enriched in nutrients. Thus, upon amendment to soil biochar may increase the cation © 2013 American Chemical Society

exchange capacity, pH, water holding capacity, and decrease bulk density.5,11 Biochar has been reported to have considerable agronomic values for enhancing crop production,9 being associated with improved soil fertility, improved ecosystem functioning and sequestration of C.12,13 Biochar can immobilize heavy metals2,4 and minimize the bioavailability of organic contaminants to earthworms, microbes, and plants, due to its high porosity, large surface area, and associated high sorptive capacity.1,6,9,10 SSBC is a promising yet problematic biochar source. SS is polluted with toxic metals compared to other raw materials used to make biochar (e.g rice straw). A critical issue is if SSBC introduces unacceptable contamination levels that would make it impermissible as a soil amendment from a regulatory, ecosystem-health or human health point-of view. However, both the pyrolysis of SS to make SSBC and the resulting Received: Revised: Accepted: Published: 8624

February 8, 2013 June 5, 2013 June 24, 2013 June 24, 2013 dx.doi.org/10.1021/es400554x | Environ. Sci. Technol. 2013, 47, 8624−8632

Environmental Science & Technology

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During harvesting at grain maturity (13 weeks after transplanting), rice straws were cut at 3 cm above soil surface and washed with deionized water. The number of tillers, panicles, and spikelets were counted; the heights of tillers and length of panicles were measured. Plants were dried at 70 °C for 72 h, then weighted and separated into leaves and stem. Unpolished grains, leaves and stem were pulverized for further chemical analyses. Chemical Analyses. Dissolved organic carbon (DOC) was extracted with a method adopted by Feng et al.20 with some modifications. Briefly, 40 mL of 0.5 M K2SO4 solution was added to 4.0 g moist soil sample and shaken for 1 h at 200 rpm and then centrifuged. The supernatant was filtered through a filter membrane (0.22 μm) and analyzed for DOC using a total carbon analyzer (TOC-VCPH Shimadzu, Japan). Available nitrate-nitrogen (NO3−N) and ammonium-nitrogen (NH4− N) were extracted with 2 M KCl and analyzed using QuikChem QC 5800 (Lachat Instruments, Loveland, CO). The procedural details are given in the SI. Available P (Colwell P) was measured using the method adopted from Rayment and Higginson,21 whereas the ammonium acetate (NH4OAc) (1M) extraction method was used for availablecations including K and Na.22 The EDTA-extractable fraction of soil was measured as an assumed proxy for the bioavailable contents of metal(loid)s.23 A mixture (20 mL) containing 0.05 M ethylene-diamine-tetra-acetic acid disodium (EDTA-Na2), 0.01 M CaCl2 and 0.1 M triethanolamine (TEA) was added to dried sample (10 g) in 50 mL polypropylene tubes, these were shaken for 3 h at 180 rpm, centrifuged and then the supernatant was filtered through a membrane filter (0.22 μm). To measure the total concentration of metal(loid)s, soil and SSBC samples (0.2 g) were digested with aqua regia,19 whereas powdered leaves, stem, and grain samples were digested with high purity HNO3/H2O2(1/1 v/v) in a microwave accelerated reaction system (CEM-Mars,V. 194A05). The suspensions were filtered and the filtrate was adjusted to 50 mL with Milli-Q water. The concentrations of the elements such as K, Na, P, Cr, Cu, Ni and Zn were determined using ICP-OES (Perkin-Elmer Optima 7000 DV, Downers Grove, IL), whereas As, Cd, Co, and Pb were measured using ICP-MS (Agilent Technologies, 7500 CX, Santa, Clara, CA). GHG Emissions. The emissions of N2O and CH4 were measured from the transplanting to harvesting stage at one week intervals for the both cultivated and uncultivated soils, with and without SSBC amendment. Transparent PVC chambers (90 cm high and 30 cm diameter) with a small electric fan on the top of the chamber and a gas sampling space tightened with butyl rubber lids at the height of the rice-pot were used to enclose the pots one hour prior to sampling (see SI Figure S1). Gas samples (120 mL) were collected immediately at 0, 30, and 60 min after enclosing for one hour by first turning on the fan for a few seconds to mix the air and then removing gas with a 60 mL syringe (taken twice) and stored in 120 mL airtight vacuumed glass vials crimped with butyl rubber lids and aluminum crowns. Changes in temperature and humidity were also monitored inside the chamber during sampling. Gas samples were analyzed using a gas chromatograph (Agilent Technologies, GC-7890A series) equipped with an autosampler with peristaltic pump, chemoluminescence NO analyzer, flame ionization detector (FID) and electron capture detector (ECD). The fluxes of N2O and CH4 were calculated on the basis of linear regression analysis of

increase in sorbtive capacity will immobilize toxic metals to some extent.9,10 Whether this immobilization is sufficient to reduce exposure in rice plants to negligible levels is a key focus of the present study, as large scale application would require this as a prerequisite. Being anoxic and anaerobic, rice paddy soil is considered one of the major anthropogenic sources of GHG nitrous oxide (N2O) and methane (CH4).5 Rice paddy soils contribute 5− 19% annually to total global CH4 emission.14In China, the annual emissions of N2O and CH4 from rice paddy soils range from 88.0 to 98.1 GgN2O-Nyear−1 and from 7.7 to 8.0 TgCH4year−1, respectively.15 Biochars derived from wheat straw and bamboo biomass are reported to reduce emission of N2O and CH4 from paddy soils.16,17 Therefore, biochar amendment to rice paddy soils is attracting increasing attention to mitigate these GHG, though, the effects of SSBC on GHG emissions remained largely unexplored. Herein a mechanistic study is presented on how SSBC in paddy soil influences the uptake of nutrients and potential toxic metal(loid)s to rice plants (Oryza sativa L) as well as emissions of N2O and CH4.

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MATERIALS AND METHODS Biochar Preparation and Characteristics. SS was obtained from Xiamen Yundang wastewater treatment plant and air-dried. SSBC was produced through pyrolysis of SS at 550 °C for 6 h under a continuous flow of nitrogen; details on biochar preparation are given in our previous paper.10 The initial characteristics of SSBC including pH, electrical conductivity (EC) and losson ignition (LOI) were measured. Porosity and surface area were determined using a surface area and porosity analyzer (Micromeritics, ASAP 2020). Total C, N, and S were measuredby dry combustion using amacro analyzer (VarioMax CNS, Germany). Procedural details are given in the Supporting Information (SI). Soil. Surface soil samples (0−10 cm) were collected from Jimei District, Xiamen, China. After transportation to the laboratory, the soil was air-dried, sieved (2 mm mesh) and homogenized to obtain a composite sample. The basic characteristics including pH, EC, LOI, C, N, S, and particle size were measured. Procedural details are provided in the SI. Experimental Design. SSBC amendments were made at application rates of 5 and 10% w/w (referred to as SSBC5 and SSBC10, respectively) and homogenously mixed. A control treatment without SSBC addition was also included. The basal fertilizers NH4NO3 (120 mgN kg−1 soil) and K2HPO4 (30 mgP kg−1 soil and 75.7 mgK kg−1 soil)18 were applied to all the treatments and mixed thoroughly. These treatments were replicated five times in cylindrical polyvinylchloridepots (24 cm high and 15 cm diameter) having 4 kg total mass of soil/ treatment. Two sets of these soil treatments were flooded with deionized water one week before the cultivation of rice seedlings. Rice seeds were disinfected according to the method mentioned in our previous study19 and then germinated on cleaned moist perlite. Two uniform pregerminated rice seedlings having two leaves were transplanted to one set of pots, whereas the other set of pots was not cultivated with rice (to investigate the influence of cultivation). The experiment was conducted in a greenhouse under 12 h natural light, with daytime temperature 31 ± 2 °C, nighttime temperature 25 ± 3 °C and relative humidity 70 ± 5%. Rice plants were flooded with deionized water and the pots randomized at regular intervals to compensate for light and temperature differences. 8625

dx.doi.org/10.1021/es400554x | Environ. Sci. Technol. 2013, 47, 8624−8632


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Figure 1. The effect of SSBC amendments (0, 5 and 10%) on rice plants, showing a) plant biomass (grain and shoot) and tiller number, and b) tiller height (TH), panicle number (PN), panicle length (PL), and spiklet number (SN). Error bars represent standard deviations (n = 5). Different letters indicate significant difference (P ≤ 0.01), whereas similar letters and parameters without letters indicate no significant difference.

Accounting for the difference in behavior across the metals is nontrivial, and dependent upon the species of the metals present. The application of other types of biochars have been reported to cause a significant decrease in the bioavailable concentrations of many metals,4,30,31 which has also been investigated using kinetic and adsorption studies.32 Soil metal availability in SSBC amended soil could be linked with the changes in soil pH, cation exchange and DOC values. In this study, soil pH (4.02) changed to 4.84−5.39, a range associated with the maximum adsorption of metals32 as well as precipitation of insoluble species. Available concentration of Cd increased in SSBC amendments (Table 2), likely owing to the high concentration in SSBC. The calculated Cd total concentration (0.33−0.48 mg/kg dw) in the SSBC amended soils lightly exceeded its permissible limit (0.3 mg/kg dw) set for acidic soil by State Environmental Protection Administration, China (SEPA).26 The large relative increase in bioavailable Zn concentrations may be of more concern than Cd. Freddo et al.33 also found a slight increase in Cd and a large increase in Zn concentrations during contextualization of metal(loid)s in biochars. Effects on Rice Plant Growth. The addition of SSBC significantly stimulated plant growth as compared to the control (Figure 1). Shoot biomass, grain yield, number of tillers, and the height of tillers all increased significantly (P < 0.01), though no significant change was observed in the length of panicles and number of spikelets (Figure 1). The average dry weights of rice grain harvested were 3.3 ± 0.8 g from the control soil, 8.3 ± 1.9 g from SSBC5 and9.2 ± 0.9 g for SSBC10 (SI Table S1). Similarly, the shoot biomass yields were greater than in the control soil by 71.3% for SSBC5 and 92.2% for SSBC10. Rice plants grown on SSBC amended soil reached the flowering stage quicker than nonamended soil (SI Figure S2). The uptake of nutrients such as N (6.5−7.5%), P (137− 166%), Na (96.8−122%) increased in the grains, whereas K did not change significantly as described in the SI. Bioaccumulation of Metal(loid)s. The bioaccumulation of As, Cd, Cr, Co, Cu, Ni, Pb, and Zn, as affected by SSBC amendments, in rice grains, leaves and stem, is presented in Figure 2. Despite the increased total concentration in the soil after amendment, the concentrations of As, Co, Cr, Cu, Ni, and Pb in the plant extracts (i.e., all except Cd and Zn) were significantly (P ≤ 0.05) reduced with the SSBC amended soil compared to the control soil. This corresponds to the

the temporal changes in these gases using an average temperature (see further detail in the SI). Quality Control. Sample blanks and standard reference materials (GBW07603-GSV-2, GBW07406-GSS-6, and GBW10010 for plant, soil and rice flour, respectively, obtained from the National Research Center for Standards in China) were included to verify the accuracy and precision of the digestion and subsequent analysis procedure. The recovery rates of selected elements were satisfactory and ranged from 91.5 ± 8.4% to103 ± 6.5%. Data Analysis. The data were analyzed using the statistical package SPSS 11.5.24 The measurements are expressed in terms of mean values, while Figures 1−3 and SI Figure S3 present the mean values and standard deviation of five replicates. Differences from the treatment methods were tested using analysis of variance (ANOVA), whereas for mean significance the Tukey’s test was used with a level of P < 0.05.

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RESULTS AND DISCUSSION SSBC. Basic characteristics of SSBC are given in Table 1. Pyrolysis of SS to produce SSBC caused an increase in the pH, BET surface area and pore volume. The total concentration of most elements (including all metals) increased after pyrolysis but the available concentrations (as defined in Table 1) all decreased substantially: from factors of >10 (for As and P) to approximately 2 (e.g., for Zn and Cd). Méndez et al.29also found that the pyrolysis process to form SSBC decreased the available concentration of metal(loid)s and their leaching risk. Soil and SSBC Amended Soil. A comparison of soil and SSBC amended soil (SSBC-5% and SSBC-10%) is presented in Table 2. The soil can be classified as acidic (pH 4.02).The addition of SSBC changed many soil characteristics such as pH, DOC, TC, TN, NH4−N, NO3−N, P, and Na (see the SI for details). Among the metal(loid)s, there was an increase in total concentration, as the concentration in the SSBC was higher than in the soil (Table 1), but this was not reflected in the more environmentally relevant bioavailable (EDTA-extractable) concentrations. Decreased bioavailable concentrations were observed for As (−30.3 to −37.7%), Co (−23.4 to −30.3%), Cr (−18.5 to −26.1%), Ni (−2.9 to −7.0%), and Pb (−47.4 to −65.0%), whereas increased bioavailable concentrations were observed for Cu (35.8 to 63.2%), Zn (10 to 17-fold), and Cd (67.2 to 115%) compared to the control soil (Table 2). 8626



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Table 1. Basic Characteristics of SS, SSBC, and Soil Used in This Study and Comparison with Maximum Permissible Limits Set for SS Application into Agricultural Soil (pH < 6.5) (The Available Concentrations of Elements in SS, SSBC and Soil Are Also Given) permissible limits properties

sludge

pH (CaCl2) EC (mS/cm) soil particle size clay(%) silt(%) sand(%) BET surface area (m2 g−1) pore volume (cm3 g−1) pore size (nm)

5.41 2.56

2.17 0.0097 17.9

C (%) S (%) N (%) P (g/kg) K (g/kg) Na (g/kg) As (mg/kg) Cd (mg/kg) Co (mg/kg) Cr (mg/kg) Cu (mg/kg) Ni (mg/kg) Pb (mg/kg) Zn (mg/kg)

32.2 3.56 3.17 51.7 13.8 86.8 8.81 2.98 2.07 54.0 163 23.7 19.9 845

Kf (g/kg) Naf (g/kg) Pg (mg/kg) Ash (mg/kg) Cdh (mg/kg) Coh (mg/kg) Crh (mg/kg) Cuh (mg/kg) Nih (mg/kg) Pbh (mg/kg) Znh (mg/kg)

1.65 5.58 240 0.45 0.59 1.05 4.13 22.8 6.62 7.89 267

bibiochar 7.22 1.73

soil

a

CEC (sludge)

USEPAb (sludge)

SEPAc(soil)

background soild

75 85

40 0.3

6.3 0.07

3000 4300 420 840 7500

150 50 40 250 200

44 22.8 18.2 41.3 86.1

4.02 0.04

0.63 22.1 77.3 5.50 NDe 0.0144 ND 10.5 ND Total Concentrations(In Dry Weight) 28.0 0.24 5.30 0.03 2.60 0.02 58.2 ND 17.8 1.82 108 2.59 9.25 1.09 16 3.69 0.16 20 3.19 0.80 74.1 6.56 1000 222 7.56 1000 34.5 2.15 300 27.0 3.58 750 1102 19.0 2500 Available Concentrations (In Dry Weight) 0.49 0.30 3.05 1.70 17.8 0.03 0.04 0.05 0.26 0.01 0.40 0.04 1.24 0.20 6.50 0.09 2.26 0.002 2.13 0.002 127 0.003

a Permissible limits set for sewage sludge by the Commission of European Communities (CEC).25 bPermissible limits set for sewage sludge by the United States Environmental Protection Agency (USEPA).28 cPermissible limits set for soil pH < 6.5 by the State Environmental Protection Administration (SEPA).26 dBV soil background values taken from Lu et al.27 for Fujian province, China. eND not determined. fNH4OAc-extractable g Colwell P. hBioavailableextracted with EDTA-Na2(0.05 M), CaCl2(0.01 M) and TEA (0.1 M).

decreased bioavailability of these compounds in soil (Table 2), with the exception of Cu which had increased bioavailability in soil. Changes in grain concentration are provided in SI Table S3. Average decreases at 5 and 10% SSBC application were: As (69.8% and 74.1%), Cr (27.2% and 34.8%), Co (73.9% and 70.4%), Cu (15.3% and 35.8%), Ni (19.2% and 25.4%), and Pb (77.8% and 88.9%). The average grain concentration increase in SSBC amended soil for Cd were 560−500%, and for Zn 167−185% (SI Table S3). No significant difference in grain bioaccumulation was found between the rice plants grown on SSBC5 and SSBC10 treatments. Similar results were found for leaf concentrations; average decreases at 5 and 10% SSBC application were As (24.4% and 27.7%), Cr (18.2% and 24.1%), Co (77.4% and 78.4%), Cu (29.8% and 36.8%), Ni (29.7% and 36.3%), and Pb (60.2% and 70.3%) (Table S3). Leaf concentrations of Cd and Zn increased

in SSBC5 and SSBC10 treatments, though somewhat less than grain: Cd (131−118%) and Zn (55−68%). Whereas, differences in leaf concentrations between the control and SSBC5 amendment are significant, the differences between the SSBC5 and SSBC10 amendments are slight, though generally change with the amendment amount. For stems, average decreases at 10% SSBC application were: As (33.9%), Cr (38.3%),Co (91.9%), Cu (28.2%), Ni (32.9%), and Pb (69.8%). Stem concentrations appear more correlated to amendment amount than do leaf or grain concentrations, though these changes are not statistically significant (except Pb) (SI Table S3). The concentrations of Cd (188.2% and 250.4%) and Zn (216.6% and 227.6%) increased in rice stem grown on SSBC5 and SSBC10 amended soil (respectively as compared to control). The concentrations of As, Cd, Co, Cr, 8627



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level of As exceeded the maximum permissible limits (0.05 mg/ kg dw) set for food by SEPA.36 It is worth noting that the addition of SSBC decreased As concentration in rice grains to permissible limits. SSBC is characteristically different from biochar derived from other feed stocks, therefore, it may be expected to influence the uptake rate of metal(loid)s in rice differently. The addition of SSBC in this study reduced As uptake, while Zheng et al.30 reported an increase in uptake of As in rice, reaching up to 327% when rice-crop derived biochar was used. Paddy rice is proficient at As accumulation because of its flooded paddy cultivation which mobilizes arsenite.37 However, S, P, and Fe interact strongly with As during plant uptake and affect its bioaccumulation.38 In the present SSBC amendments, elevated concentrations of S and P were present (see the SI) which could be a reason for lower As bioavailability being observed. Being a phosphate analog, arsenate is taken up by plants through P transporters,39 therefore, increased P can reduce As uptake and accumulation. The addition of SSBC increased soil S (13−16 fold), which could have interacted with As and reduced its uptake by the rice plants.5 Previous studies have shown that S and sulfate influence As uptake by different mechanisms such as Fe-plaque formation on rice root surfaces,40 arsenate desorption from iron plaque41 and inhibition of arsenate transport into cells by phosphate competition.42 As mentioned earlier, the uptake of P by rice plants significantly increased, whereas S decreased, upon SSBC amendment. These trends are consistent with the abovementioned mechanisms involved in low As and metal uptake. To account for why SSBC amendment increased Cu availability in soil, yet decreased uptake in rice plants, the high concentration of available Zn in SSBC could have interfered with Cu uptake, as plant roots absorb Cu and Zn through the same mechanism.43 Supporting this, a strong negative correlation between the uptake of Zn and Cu (for grain, leaves and stem, having a r2 = 0.754, 0.890, and 0.844, respectively) was found, indicating an antagonistic effect of Zn on Cu bioaccumulation in rice plants. To account for the decrease in uptake of all other metal(loids) upon SSBC amendments, many mechanisms have been proposed in the literature, some of which correspond to the trends observed in the present study. The most direct and simple mechanism would be the increase in soil pH44and CEC45 which helps to increase the sorption of metal(loid)s in soil. An increase in pore size, pore volume and surface area would increase the number of exchange sites, thereby reducing metal mobility.35,45,46 The increase in DOC concentration with SSBC (Table 2) could reduce metal(loid) availability by acting as a chelator.30 GHG Emissions. The addition of SSBC to the paddy soil significantly (P < 0.01) reduced the emissions of N2O and CH4 from both cultivated and uncultivated soils (Figure 3). For rice cultivated soil, the reduction in total cumulative N2O emissions compared to the control was 95.6% and 98.4% (5 and 10% SSBC, respectively), whereas for uncultivated treatments this reduction was 89.9% and 93.1%. Emissions of N2O from control and SSBC (5 and 10%) amended soils, both cultivated and uncultivated, increased at first and then decreased (Figure 3), though this feature is much less noticeable on SSBC amended soils (Figure 3a), and the decrease for cultivated soil was significantly greater as compared to the uncultivated soil (Figure 3b).Furthermore, N2O fluxes were not constant between the measuring periods for all treatments (SI Table

Table 2. Properties of Soil and SSBC Treatments (After Mixing) before Rice Seedling Cultivation (Note That All Concentrations Are in Dry Weight) treatments properties

control soil

SSBC-5%

pH 4.02 4.86 EC (μS/cm) 38.7 622 bulk density (g/cm3) 1.12 1.07 TN(%) 0.04 0.18 TC(%) 0.22 1.44 S(%) 0.03 0.39 NH4−N (mg/kg) 9.47 42.7 NO3−N (mg/kg) 90.8 77.2 DOC (mg/kg) 94.8 130 Ka (mg/kg) 305 315 Pb (mg/kg) 30.9 43.0 Naa (mg/kg) 1699 1788 bioavailable Asc (μg/kg) 49.1 34.2 bioavailable Cdc (μg/kg) 8.31 13.9 bioavailable Coc (μg/kg) 36.2 27.7 bioavailable Crc (μg/kg) 197 160 bioavailable Nic (μg/kg) 86.8 84.2 bioavailable Cuc (μg/kg) 1.87 2.54 bioavailable Pbc (μg/kg) 2.34 1.23 bioavailable Znc (μg/kg) 3.33 34.5 Uptake Rates (Aboveground) of Nutrientsd N (kg/ha) 56.4 105 (I) P (kg/ha) 15.2 69.3(I) K (kg/ha) 82.8 163 (I) Na (kg/ha) 9.09 64.6 (I) S (kg/ha) 26.7 41.8 (I)

SSBC-10% 5.39 992 1.01 0.26 2.02 0.49 60.1 62.0 161 374 58.5 1852 30.6 17.9 25.2 145 80.7 3.06 0.82 56.7 98.2 (II) 98.4 (II) 165 (I) 76.2 (II) 39.0 (I)

a

NH4OAc-extractable. bColwell P. cBioavailable extracted with EDTANa2(0.05 M), CaCl2(0.01 M) and TEA (0.1 M). dAboveground nutrient values in a row with the letters indicate significant difference (P < 0.01) between SSBC and the control, where both entries marked with a (I) indicate no significant difference between the SSBC amendments, and those marked with a (I) and (II) as being significantly different.

Cu, Ni, Pb, and Zn were found in the order of leaves > stems > grains. The above-mentioned findings showed that SSBC was very effective in reducing the bioaccumulation of most metal(loid)s (As, Co, Cr, Cu, Ni, and Pb) in rice plant grown on paddy soil. However, for upland conditions in the literature observed that SSBC effects were different. One study on cherry tomatoes reported a reduced bioaccumulation of Ni and Co, though increased bioaccumulation of Cd, Cu, and Zn, and no change for As.34 Furthermore, Yachigo and Sato35 observed an increase in the bioaccumulation of Cd, Cu, and Zn in spinach and bean grown on SSBC amended soil. The concentrations of Cd and Zn in rice grain significantly increased in SSBC amended soil, reaching up to 0.12−0.11 mg/ kg and 26.3−28.1 mg/kg, respectively, corresponding to the increased bioavailable concentrations in the SSBC amendments (Table 2). Although Cd and Zn concentrations increased in rice grain they did not exceed the limits set for food by SEPA (these limits being 0.2 and 100 mg/kg dw, respectively) (SI Table S3). SSBC with higher levels of Cd and Zn than in the present study may pose a risk. Grain As content was significantly (P = 0.01) elevated in rice grown on unamended soil, reaching up to 0.14 mg/kg. This 8628



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Figure 2. Potential toxic metal (loid) concentrations in rice grains, leaves and straw grown on soil amended with 0%, 5%, and 10% SSBC. Error bars represent standard deviations (n = 5). Different letters indicate significant differences between members of the same set (P ≤ 0.05), while similar letters and elements without letters indicate no significant difference.

S4). For the control treatments the peak N2O emission was 2.02 mg/m2/h (at week 5) for the rice cultivated soil and 0.84 g/m2/h for the uncultivated soil (at week 4). Expressing the total cumulative N2O emission on a per hectare basis (note these may be prone to extrapolation biases), the control soil cultivated with rice plants emitted 12.80 kg/ha over 13 weeks, much higher than 0.57 kg/ha and 0.20 kg/ha for the SSBC5 and SSBC10 soils, respectively. Similarly, the cumulative N2O emission from the uncultivated control soil was 9.94 kg/ha, much higher than the emissions of 1.00 kg/ha and 0.68 kg/ha from SSBC5 and SSBC10 amended soils, respectively (Figure 3b). Cumulative N2O fluxes were significantly higher for the cultivated control soil than the uncultivated control soil, while for SSBC treatments the uncultivated soil presented significantly higher emissions. While the rice plants grew during the first six weeks, the N2O emission from both the control and SSBC treatments increased and peaked at week six and then decreased to levels far below the uncultivated soil emissions, indicating the rice plants at a young stage facilitate the emission of N2O.47 In the rhizosphere, the living root systems of plants stimulated nitrification substantially more so than bulk soil.48 In this study, NO3−N concentrations decreased with increasing additions of SSBC, implying SSBC reduces the denitrification process responsible for N2O emission. This could be related to SSBC increasing root growth by increasing the amount of nutrients and soil aeration.49

In paddy soil, under anaerobic conditions, available C and NO3− are needed for anaerobic denitrifying bacteria to produce N2O,50 therefore, any changes in these conditions could affect the emission of N2O. Results showed that SSBC addition decreased the available NO3− and affected other relevant parameters like increasing soil pH and decreasing bulk density (Table2). SSBC amendment increased soil pH which presumably would stimulate the N2O reductase enzymatic activity of denitrifying bacteria,15 while suppressing the activity of reductase enzymes responsible for conversion of NO3 and NO2 to N2O.5,51 Furthermore, an increase in soil pH decreases N2O production by denitrification.52,53 Increased sorption surfaces for N2O may be another possibility. After adding SSBC (5 and 10%) to the cultivated and uncultivated soil, the emissions of CH4 decreased by more than 100%, meaning that the paddy soil stopped emitting CH4 and became a CH4 sink (SI Table S5). Figure 3c and d show the CH4 fluxes throughout the whole experiment. Like N2O, CH4 fluxes were not constant over the measuring periods for all treatments, and were greater for the control soil than the biochar amended soil (SI Table S5). There was no significant difference between SSBC5 and SSBC10 treatments cultivated with rice, whereas a significant (P < 0.05) difference was observed for uncultivated treatments. peak CH4 emission observed from the control soil was 164.8 mg/m2/h (week 6) for the cultivated treatment and 40.8 mg/m2/h (week 4) for the uncultivated. The peak negative CH4 fluxes (uptake rates)for the SSBC5 and SSBC10 soils ranged from 1.5 to 12.5 mg/m2/h 8629



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Figure 3. N2O and CH4 emissions from SSBC amended and unamended soils, showing (a) N2O from rice cultivation treatments, (b) N2O from uncultivated soil, (c) CH4 from rice cultivation treatments, and (d) CH4 from uncultivated soil. Error bars represent standard deviations (n = 5).

oxidation,16 having no effect on CH4 oxidation,51 or increasing CH4 oxidation,51 needs further research work to elucidate the mechanisms involved using different biochars and soil types.

and 2.4−22.0 mg/m2/h, respectively, for the cultivated treatment (Figure3c), while it ranged from 0.4 to 25.6 mg/ m2/h and 1.0−40.3 mg/m2/h, respectively for uncultivated treatment (Figure3d). The total cumulative CH4 emission from cultivated control soil (1035 kg/ha) was significantly higher than uncultivated treatment (401 kg/ha), while the total cumulative CH4 uptake rate was significantly higher (P < 0.05) in uncultivated soil amended with SSBC5 and SSBC10 (175 kg/ha and 351 kg/ha, respectively) than cultivated treatments (132 kg/ha and 197 kg/ha, respectively). Other researchers have also reported an increase in CH4 oxidation in biochar amended soil.54 It has been suggested that biochar increases soil aeration which could increase CH4 oxidation51 through stimulating the growth of methanothrops,19an aerobic proteobacterial group utilizing CH4 as the sole C source.. Comparing rice in the cultivated and noncultivated soil, the increase in CH4 emission from unamended soil and decrease in oxidation from SSBC amended soil with rice cultivation could presumably be related with labile organic C of root exudates, particularly during the young stage of rice, which can act as potential substrates for methanogens to promote CH4 production.55,56 Growth and activity of methanotrophic bacteria are not only controlled by CH4 and oxygen but also by the available N in soil.57 Thus available N could also act as a limiting factor for CH4 oxidation. However, the contradictory results reported in the literature about biochar decreasing CH4

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ENVIRONMENTAL RELEVANCE

The present study indicates a net benefit of SSBC amendment for rice paddy soils: decreased GHG emissions, increased crop yield, and mostly decreased metal(loid)s in rice grains. The biggest concern was the amount of metal(loid) contaminants contained within the SSBC, and how bioavailable they would be. With the exception of Cd and Zn, the soil availability and rice plant biouptake of other metal(loids) was reduced. Thus, sufficiently low levels of Cd and Zn may be prerequisite for the use of SSBC as soil amendment, and such limits would have to be defined conservatively based on subsequent studies. Though the results here are promising, such as the As concentration in rice grain decreasing to SEPA permissible levels, it should be emphasized that how well these results can be extrapolated for other SSBC, other biochars and other soil types is uncertain, and would require further investigation. The presence of PAHs and other organic contaminants on SSBC is another issue that should be followed up in future studies.6,8A particular concern is the long-term effects of SSBC application, in that the metals contained within may become more bioavailable with time. Because SS is an abundant feedstock to produce BC for rice 8630



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paddy soil, further research and long-term field trials are warranted.

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(12) Haefele, S. M.; Konboon, Y.; Wongboon, W.; Amarante, S.; Maarifat, A. A.; Pfeiffer, E. M.; Knoblauch, C. Effects and fate of biochar from rice residues in rice-based systems. Field Crop Res. 2011, 121, 430−440. (13) Whitman, T.; Nicholson, C. F.; Torres, D.; Lehmann, J. Climate change impact of biochar cook stoves in western Kenyanfarm households: System dynamics model Analysis. Environ. Sci. Technol. 2011, 46, 3687−3694. (14) Intergovernmental Panel on Climate Change (IPCC). Agriculture. In Climate Change 2007: Mitigation, Contribution of Working Group III to the Fourth Assessment Report of the IPCC; Metz, B., Davidson, O. R., Bosch, P. R., et al., Eds.; Cambridge University Press: Cambridge, UK/New York, 2007; pp 498−54. (15) Liu, S. W.; Qin, Y. M.; Zou, J. W.; Liu, Q. H. Effects of water regime during rice growing season on annual direct N2O emission in a paddy rice-winter wheat rotation system in southeast China. Sci. Total Environ. 2010, 408, 906−913. (16) Spokas, K. A.; Koskinen, W. C.; Baker, J. M.; Reicosky, D. C. Impacts of woodchip biochar additions on greenhouse gas production and sorption/degradation of two herbicides in a Minnesota soil. Chemosphere 2009, 77, 574−581. (17) Liu, Y.; Yang, M.; Wu, Y.; Wang, H.; Chen, Y.; Wu, W. Reducing CH4 and CO2 emissions from waterlogged paddy soil with biochar. J. Soil. Sed. 2011, 11, 930−939. (18) Li, R. Y.; Stroud, J. L.; Ma, J. F.; Mcgrath, S. P.; Zhao, F. J. Mitigation of arsenic accumulation in rice with water management and silicon fertilizers. Environ. Sci. Technol. 2009, 43, 3778−3783. (19) Khan, S.; Aijun, L.; Zhang, S.; Hu, Q.; Zhu, Y.-G. Accumulation of polycyclic aromatic hydrocarbons and heavy metals in lettuce grown in the soils contaminated with long-term wastewater irrigation. J. Hazard. Mater. 2008, 152, 506−515. (20) Feng, Y.; Xu, Y.; Yu, Y.; Xie, Z.; Lin, X. Mechanisms of biochar decreasing methane emission from Chinese paddy soils. Soil Biol. Biochem. 2012, 46, 80−88. (21) Rayment, G. E.; Higginson, F. R. Australian Laboratory Handbook of Soil and Water Chemical Methods; Inkata Press: Melbourne, Australia, 1992. (22) Helmke, P. A.; Sparks, D. L. Lithium, sodium, potassium, rubidium, and cesium In Methods of Soil Analysis: Part 3; Sparks, D. L. et al., Eds.; SSSA and ASA: Madison, WI; Suarez, D. L. 1996. Beryllium, magnesium, calcium, strontium, and barium. p 575−601. In Methods of Soil Analysis: Part 3; Sparks, D. L. et al., Eds.; SSSA and ASA: Madison, WI. (23) Zeng, F.; Ali, S.; Zhang, H.; Ouyang, Y.; Qiu, B.; Wu, F.; Zhang, G. The influence of pH and organic matter content in paddy soil on heavy metal availability and their uptake by rice plants. Environ. Pollut. 2011, 159, 84−91. (24) SPSS®base 11.5 User’S Guide; SPSS Inc., (Statistical Package for the Social Science): Chicago, IL, 2002. (25) CEC, Commission of the European Communities’ Council Directive of 12 June1986 on the Protection of the Environment, and in Particular of the Soil, When Sewage Sludge is Used in Agriculture. L 181 (86/278/EEC) Off. J. Eur. Commun. : 1986. (26) SEPA. Environmental Quality Standard for Soils, GB15618− 1995; State Environmental Protection Administration: China, 1995. (27) USEPA. Process Design Manual, Land Application of Sewage Sludge and Domestic Septage, EPA/625/R-95/001; United States Environmental Protection Agency, Office of Research and Development: Washington, DC, 1995. (28) Lu, Y.; Zhu, F.; Chen, J.; Gan, H. H.; Guo, Y. B. Chemical fractionation of heavy metals in urban soils of Guangzhou, China. Environ. Monit. Assess 2007, 134, 429−39. (29) Méndez, A.; Gómez, A.; Paz-Ferreiro, J.; Gascó, G. Effects of sewage sludge biochar on plant metal availability after applicationto a Mediterranean soil. Chemosphere 2012, 89, 1354−1359. (30) Zheng, R. L.; Cai, C.; Liang, J. H.; Huang, Q.; Chen, Z.; Huang, Y. Z.; Arp, H. P. H.; Sun, G. X. The effects of biochars from rice residue on the formation of iron plaque and the accumulation of Cd,

ASSOCIATED CONTENT

S Supporting Information *

Details on supportive methodology, results and discussion including 5 Tables and 3 Figures are given. This material is available free of charge via the Internet at http://pubs.acs.org.

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AUTHOR INFORMATION

Corresponding Author

*Phone: 00865926190560; fax: 00865926190997; e-mail: [email protected]. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This study financially supported by National High-Tech R&D Program of China (863 Program 2012AA06A204) and the International Science, Technology Cooperation Program (2011DFB91710) and the Chinese Academy of Sciences under the young international scientists fellowship program (2011Y2ZA02).

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Sewage Sludge Biochar Influence upon Rice (Oryza sativa L) Yield

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