Soil organic carbon content affects the stability of biochar in paddy soil

Agriculture, Ecosystems and Environment 223 (2016) 59–66

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Soil organic carbon content affects the stability of biochar in paddy soil Mengxiong Wua,b , Xingguo Hana,b , Ting Zhonga,b , Mengdong Yuana,b , Weixiang Wua,b,* a b

Institute of Environmental Science and Technology, Zhejiang University, 866 Yuhangtang Road, Hangzhou 310058, China Zhejiang Provincial Key Laboratory for Water Pollution Control and Environmental Safety, China

A R T I C L E I N F O

A B S T R A C T

Article history: Received 29 August 2015 Received in revised form 25 February 2016 Accepted 29 February 2016 Available online xxx

Recalcitrant biochar application appears to be a promising method to decelerate global warming through increasing long-term carbon sequestration in soil. Stability of biochar carbon (C), which is the major determining factor of C sequestration effect, depends mainly on biochar physiochemical characteristics and soil properties. However, little is known about biochar C stability in paddy soil. In this study, 13C labeled rice straw (RS) biochar produced at 500
C was incubated with five types of paddy soils to determine the key soil characteristics involved in biochar-C stability. Results showed that cumulative mineralization rates of RS biochar-C incubated with different paddy soils were relatively low (0.17–0.28%) during 390 days of incubation. The cumulative mineralization rates of RS biochar-C increased with the increasing native soil total organic carbon (TOC) content. The estimated mean residence time (MRT) of stable C components of RS biochar in paddy soil, varying from 617 to 2829 years, decreased with the increase of soil TOC content. In addition, greater atomic O/C ratio and oxygen-containing functional groups were observed in biochar samples incubated in paddy soils with higher TOC content. These results suggest that RS biochar application could be an effective method for C sequestration in paddy soil. However, the stability of RS biochar in paddy soil would be significantly impacted by soil TOC content. From the perspective of long-term C sequestration, RS biochar is more suitable for applying in paddy soils with lower TOC content. ã 2016 Elsevier B.V. All rights reserved.

Keywords: Biochar Stability Total organic carbon Carbon sequestration Paddy soils

1. Introduction Biochar is a solid material obtained from the pyrolysis of plant biomass (e.g., rice straw, grass, wood) or agricultural waste (e.g., manure) in an oxygen-limited environment. In recent years, biochar application into soil ecosystems has received great attention as it provides multiple environmental benefits, such as improving soil fertility, reducing greenhouse gas (GHG) emissions from agricultural soil and increasing long-term sequestration of carbon (C) in soils (Kuhlbusch and Crutzen, 1995; Woolf et al., 2010; Liu et al., 2011). Due to its predominantly aromatic structure (McBeath and Smernik, 2009), biochar is widely recognized as a relatively stable form of C with long mean residence time (MRT) ranging from hundreds to thousands of years (Zimmerman, 2010; Singh et al., 2012). Moreover, the recalcitrant C of biochar was considered as one of the largest contributor to GHG mitigation

* Corresponding author at: Institute of Environmental Science and Technology, Zhejiang University, 866 Yuhangtang Road, Hangzhou 310058, China. Fax: +86 571 88982020. E-mail address: [email protected] (W. Wu). http://dx.doi.org/10.1016/j.agee.2016.02.033 0167-8809/ ã 2016 Elsevier B.V. All rights reserved.

using sustainable biochar technology (Woolf et al., 2010). However, it was also reported that the MRT of some natural and laboratoryproduced char or biochar was only in the range of a few decades (Bird et al., 1999; Steinbeiss et al., 2009; Hilscher and Knicker, 2011). Thus, stability of biochar-C in soil ecosystems requires further understanding. Recently, uncertainties of biochar-C stability in soils have been observed due to the differences in feedstock types and pyrolysis conditions. For example, Zimmerman (2010) reported that the degradation rates of grass derived biochar were higher than that of wood derived biochar. Similarly, Nguyen and Lehmann (2009) found that the changes in quantity and quality of biochar derived from corn residue were greater than that from wood after one year incubation. Higher production temperature has been generally reported to increase the aromaticity of biochar and thus decrease biochar mineralization rates in soil (Zimmerman, 2010; McBeath et al., 2011; Pereira et al., 2011). In addition to feedstock types and production conditions, which significantly impact on the intrinsically chemical recalcitrance of biochar, soil physicochemical characteristics, such as clay and organic matter contents, may also have considerable effects on biochar-C stability in soil. For instance, Bolan reported that the

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M. Wu et al. / Agriculture, Ecosystems and Environment 223 (2016) 59–66

decomposition rates of biochar-C in biochar-soil mixtures increased from that incubated with clay soils to sandy soils (Bolan et al., 2012). Keith et al. (2011) observed increasing mineralization of wood biochar-C with the increasing application rate of sugarcane residues at the early stages of incubation in a smectite-rich soil. In contrast, it was found that the added sugarcane residues were incorporated into aggregate and organo-mineral fractions, and thus did not increase the decomposition of aged black C in Anthrosols of the Central Amazon (Brazil) (Liang et al., 2010). Therefore, in order to properly assess the potential of biochar technology as a long-term C sequestration method in different soil ecosystems, the influence of soil properties on biochar-C stability still remains further concerns. It was suggested that stability of biochar-C could be decreased due to the oxidation of biochar themselves and the adsorption of non-BC following its application to dry land soils (Liang et al., 2006). However, as paddy soils are generally kept under waterlogged conditions and have lower oxygen availability compared with dry land soils, the oxidation of biochar is assumed to decrease after its application to paddy soils. For example, Nguyen and Lehmann (2009) suggested that biochar O/C and carbon loss were significantly higher when incubated under unsaturated condition compared with saturated condition. As a result, biochar-C stability in paddy soils will be largely different from that in dry land soils. Nevertheless, few studies have examined the stability of biochar-C in paddy soils. Considering the potential advantages of rice-straw (RS) derived biochar applications in paddy soils instead of direct rice straw incorporation in effectively reducing GHG emissions and increasing crop yields (Liu et al., 2011; Dong et al., 2013; Zhao et al., 2014), stability of RS biochar-C should be attached great importance so that the carbon sequestration and the GHG mitigation effects of RS biochar technology in paddy soils could be estimated precisely. The objective of this study was, therefore, to evaluate the RS biochar-C stability and its potential carbon sequestration effect in paddy soils. In order to elucidate the key soil characteristics involved in biochar-C stability, paddy soils with different clay and organic carbon contents were collected from five sites located from northern to southern parts of China.

introduced into the furnace at the speed of 1 L/min. Here biochar produced at 500
C was regarded as an typical biochar because, according to our previous studies, this is the most suitable biochar for large applications in paddy soils considering the carbon stability and nutritional value (Wu et al., 2012). Soils were collected at the same period of time from the plowing layers (0–20 cm) of five paddy fields across northern to southern parts of China and then immediately transported to laboratory. The soil sampling sites were located in Benxi City, Liaoning Province (LN, 123.7E, 41.3N), Linyi City, Shandong Province (SD, 118.4E, 35.1N), Nanjing City, Jiangsu Province (JS, 118.8E, 32.1N), Hangzhou City, Zhejiang Province (ZJ, 119.9E, 30.4N) and Xuwen City, Guangdong Province (GD, 110.2E, 20.3N). LN, SD, JS, ZJ, and GD were the abbreviations for the experimental soils, which included three loamy soils (LN, SD and ZJ), a clay loam soil (JS) and a sand clay soil (GD) (USDA, Soil Texture Calculator). After being transported to laboratory, the soil samples were immediately air-dried. Roots and visible plant debris in the soils were removed. Soil samples were then ground and sieved through a 2mm mesh screen for the incubation study. Detailed physiochemical characteristics of the biochar and the soils are summarized in Table 1. For the d13C signature analysis, the soil and biochar samples were finely ground, sieved through a 150 mm sieve, and then determined by an isotope ratio mass spectrometer (GV ISO prime 100, UK). 2.2. Incubation experiment Equivalent to 50 g air-dried paddy soils were mixed with 2.5% (w/w) biochar and the corresponding control soils without biochar amendment were also included. The soil-biochar mixtures and the control soils were placed in separate 150 mL jars and then incubated in sealed buckets (D = 11 cm, H = 13 cm) with a CO2 trap containing 20 mL of 2 M NaOH for absorbing CO2 produced by C mineralization. The soils were kept under continuous flood condition without nutrient solution supply during the whole incubation period. The sealed buckets were incubated in the dark at 25  1
C. Each treatment was set in triplicate. A new CO2 trap was introduced at 1, 6, 13, 28, 42, 58, 90, 150, 225, 300, 390 days. The CO2 traps were then used for total CO2-C and d13C analysis.

2. Materials and methods 2.3. Mineralization of native SOC and biochar-C 2.1. Biochar and soils 13

C labeled rice straw that had been grown under enriched 13 CO2 environment (Lu et al., 2005) were used to produce biochar. The biochar was produced through slow pyrolysis in a GDL-1500X tubular furnace (Kejin, Hefei, China) using a previously described method (Wu et al., 2012). Briefly, the 13C labeled rice straw was heated at a rate of 5–10
C/min, followed by a residence time of 3 h at 500
C. To ensure an oxygen-free atmosphere, N2 gas flow was

The total soil C mineralization (mg kg1 soil) at each sampling time was determined by titrating 1 mL aliquots of the trap solution against 0.1 M HCl using phenolphthalein as the indicator (Rengel and Bowden, 2006). To determine the d13C signature of trapped CO2-C, a 10 mL aliquot of the CO2 trap solution was mixed with 10 mL of 1 M SrCl2 to precipitate SrCO3. The 13C signature of the precipitates was then determined by an isotope ratio mass spectrometer (GV ISO prime 100, UK).

Table 1 Some relevant characteristics of the soils and biochar used in the incubation experiment. Soil type

LN

SD

JS

ZJ

GD

Biochar

Clay (%) Silt (%) Sand (%) pH (1:5 H2O) N (mg/g) Organic carbon (mg/g) d13C (m)

24.40 (0.49) 39.90 (1.15) 35.80 (0.66) 5.39 2.43 (0.29) 19.64 (0.10) 24.51 (0.89)

19.60 (2.52) 48.30 (4.08) 32.10 (1.66) 5.70 2.69 (0.18) 14.59 (0.47) 23.87 (0.41)

27.10 (0.65) 36.50 (3.24) 36.40 (2.59) 4.64 2.46 (0.09) 12.97 (0.05) 25.58 (0.29)

26.00 (0.09) 40.30 (1.55) 33.70 (1.46) 5.60 2.59 (0.06) 15.14 (0.72) 28.18 (1.18)

35.40 (2.76) 16.10 (0.41) 48.50 (3.17) 5.25 2.93 (0.04) 19.82 (1.92) 24.95 (0.12)

– – – 10.04a 22.9 (2.1) 610.2 (0.6) 570.68 (6.51)

The number in the parentheses are the standard error of the mean (n = 3). “–” means it was not applicable or measured. LN: Liaoning soil; SD: Shandong soil; JS: Jiangsu soil; ZJ: Zhejiang soil; GD: Guangdong soil. a pH was determined under 1:20 H2O condition.

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To determine the proportion of biochar derived CO2-C in total CO2-C evolved (CB%), Eq. (1) was used (Keith et al., 2011). 13

CB % ¼

13

ðdT CO2  dC CO2 Þ ðd

13 B CO2

13

 dC CO2 Þ

 100

ð1Þ

where dT13CO2 is the d13C value of the total CO2-C evolved from soil–biochar mixtures, dC13CO2 is the d13C value of the CO2-C evolved from the corresponding control (non-amended) soil, and dB13C is the initial d13C value of biochar. The proportion of soil derived CO2-C in the soil–biochar mixture treatments was determined by subtracting CB% from 100. The amounts of biochar-C mineralized (%) were then calculated and normalized to per gram of added biochar-C. The cumulative biochar C mineralized over the 390 days incubation resulted from the treatments was all fitted to a two pool exponential model to estimate MRT of the biochars in different soils. Mt ¼ M1 ð1  ek1 t Þ þ M2 ð1  ek2 t Þ

ð2Þ

where Mt (%) is the cumulative % of biochar C mineralized and t is the incubation time (days). M1 and M2 are the proportion (%) of the labile (easily-mineralizable) and recalcitrant (slowly-mineralizable) pools in biochar-C, respectively; k1 and k2 are the mineralization rate constants for the labile and recalcitrant pools, respectively; a nonlinear least-squares curve fitting in OriginPro 8.0 (Originlab corporation, USA) was used to estimate the model parameters (M1,M2, k1 and k2) by minimizing the sum of the squared errors between the modeled and measured values of the cumulative (%) C mineralized over the 390 days period. The parameters were estimated separately for each replication, and standard deviations were calculated from the derived values of three replicates. The MRT is the inverse of the mineralization rate constant (1/k1 or 1/k2). 2.4. Biochar characterization by FTIR and XPS FTIR adsorption spectra was recorded from wavelengths 4000 to 400 cm1 at the resolution of 2 cm1 on a AVA TAR370 spectrometer (USA, Nicolet). One microgram of biochar samples was finely ground, sieved through a 150 mm sieve, and then mixed with 200 mg KBr for FTIR analysis. Carbon chemical functional groups were assigned to wave numbers according to (Wu et al., 2012). For XPS analysis, dry biochar particles (diameters from 150 mm to 300 mm) were randomly picked from each biochar amended treatment after 390 days incubation using tweezers and an anatomical lens (45, SZ61, Olympus) (Liang et al., 2006). The biochar particles and finely-ground powders (sieved through

61

150 mm sieve) from 3 replicates were pooled into 2 composite samples for each treatment and then tested using a VG ESCALAB MARK II (England) with a focused monochromatic Mg Ka X-ray (1253.6 eV) source and a spot size approximately 1 mm in diameter. The spectra of the biochar particles were assumed to represent the characteristics of biochar surface while the spectra of biochar powder represent both exterior and interior properties of the biochar. Binding energies for the high-resolution spectra of C1s and O1s were calibrated by setting C to 1s at 284.6 eV. The C1S and O1S spectra were deconvoluted using a non-linear least squares curve fitting program, with a Gaussian–Lorentzian mix function and Shirley background subtraction. 2.5. Statistical analyses All data were reported as means and standard deviation (SD) of the means. Analysis of variance and the least significant difference (LSD) tests were performed using SPSS 21.0 software to determine the significant differences between different soils with biochar amendment at confidence level of P < 0.05. Correlation analyses between soil physicochemical characteristics and biochar-C cumulative mineralization rates were performed using SPSS 21.0 software. 3. Results 3.1. Total carbon mineralization Total C mineralization rate (expressed as mg CO2 per gram total organic carbon per day, mg CO2 g1 TOC day1) was initially high and then decreased with the incubation time (Fig. 1). In comparison, the total C mineralization rate in all biochar-amended paddy soils was consistently less than the corresponding soils without biochar amendment. Over the 390 days incubation time, the cumulative mineralization amounts of total C ranged between 398.6 and 1161.7 mg CO2 g1 TOC across all biochar-amended and non-amended treatments (Fig. 2). The cumulative C mineralization amounts followed the order SD > JS > ZJ > GD > LN for the biochar-amended soils, but GD > ZJ > JS > SD > LN for the non-amended soils. Apparently, the cumulative mineralization amounts of total C from the biocharamended soils were significantly less than the corresponding nonamended soils. 3.2. Biochar-C mineralization Biochar-C mineralization rates across all treatments decreased very rapidly to 0.014–0.018% d1 within 90 days incubation and then stabilized between 150 and 390 days (Fig. 3). The proportions

Fig. 1. Total carbon (C) mineralization rate (mg CO2 per gram total organic carbon per day, mg CO2 g1 TOC day1) from control (square symbols), and biochar-amended soils (circle symbols) over 390 days incubation period. Error bars represent  standard error of the mean (n = 3).

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Fig. 2. Total carbon (C) mineralized (mg CO2 emission per gram of total organic C, mg CO2 g1 TOC dw soil) from the control (CK, white histograms) and the biochar-amended soils (BC, black histograms) after 390 days incubation. Error bars represent  standard error of the mean (n = 3).

of biochar-C mineralized over 390 days incubation varied between 0.17 and 0.28% in all biochar-amended soils (Fig. 4). Overall, the cumulative biochar-C mineralization (%) over 390 days incubation increased with the increasing native soil TOC content. There were no significant differences in the cumulative biochar-C mineralization (%) within 150 days incubation (early stage) among the soil treatments (Fig. 4 and Fig. S1). However, the proportion of biocharC mineralized in GD soil was significantly higher than that in JS soil after 390 days incubation (Fig. 4). In addition, the cumulative biochar-C mineralization across the soil treatments after 225, 300 and 390 days incubation (late stage) were all significantly positively correlated with the native soil TOC content (Table 2). 3.3. Mean residence time of biochar-C The model-predicted MRT of recalcitrant C in the biochars incubated with different paddy soils varied from 617 to 2829 years. Apparently, it increased with the decreasing native soil TOC content with the exception of the biochar in SD soil (Table 3). The recalcitrant biochar-C contents ranged between 99.84 and 99.89% of the total biochar-C across the soil treatments. The MRT of labile C

in the biochars ranged between 18 and 37 days and did not show any significant correlation with the native soil physiochemical characteristics. 3.4. FTIR analysis After 390 days incubation in paddy soils, functional groups of the origin biochar samples such as alphatic CH stretching (2950 cm1), aromatic C¼C skeletal vibrations (1440 cm1) and C H deformation modes in alkenes (1375 cm1) lose their intensities. However, bonds arising from C¼C and C¼O stretching (1630–1600 cm1) and COC skeletal vibrations (1080 cm1) became more apparent (Fig. 5). Discrepancies in the intensities of some functional groups in biochar samples collected from the paddy soils were also observed. Specifically, aromatic CH out of plane vibrations (700–900 cm1) were almost completely eliminated in the biochar samples from GD soil while still preserved in the other samples. Intensities of aromatic C¼C skeletal vibrations (1440 cm1) and C H deformation modes in alkenes (1440 cm1) declined more evidently in the biochar samples incubated with GD soil compared with the other

Fig. 3. Biochar carbon (C) mineralization rate (% of total biochar C d1) in different paddy soils during 390 days incubation. Error bars represent  standard error of the mean (n = 3) (LN: Liaoning soil amended with biochar; SD: Shandong soil amended with biochar; JS: Jiangsu soil amended with biochar; ZJ: Zhejiang soil amended with biochar; GD: Guangdong soil amended with biochar).

M. Wu et al. / Agriculture, Ecosystems and Environment 223 (2016) 59–66

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Fig. 4. Cumulative biochar carbon (C) mineralized (% of total biochar C) from different soils with biochar amendment after 150 days (white histograms) and 390 days incubation (black histograms). Error bars represent  standard error of the mean (n = 3). Different letters indicate significant differences between different soil treatments with biochar amendment (LN-BC: Liaoning soil amended with biochar; SD-BC: Shandong soil amended with biochar; JS-BC: Jiangsu soil amended with biochar; ZJ-BC: Zhejiang soil amended with biochar; GD-BC: Guangdong soil amended with biochar).

soils. Besides, C O C skeletal vibrations (1080 cm1) became more apparent in the biochar samples collected from LN and GD soils than SD, JS and ZJ soils. 3.5. XPS analysis In contrast to the original biochar, significantly less C and more O atoms in the biochar powder and particles collected from the paddy soils after 390 days incubation were observed (Table 4). As a result, O/C ratio of the biochar powder and particles was significantly increased after being incubated with paddy soils. In comparison with biochar powder, biochar particles after incubation contained more O and less C atoms with the exception of that collected from SD soil. In addition, O/C ratio of the biochar powder after 390 days incubation showed the similar trend with the biochar-C cumulative mineralization rates with the sequence of GD > LN > ZJ > JS (Table 4). However, the O/C ratio of biochar particles after incubation was not identical, following the sequence of GD > ZJ > LN > JS > SD. In respect to the carbon bonding states of biochar powder and particles, CC/C H/C¼C was the major C1s component in the original biochar and biochar incubated in different paddy soils, but its relative content was significantly decreased in the biochars after incubation (Table 5). In contrast, the amount of C oxidized states (C O, C¼O and O C¼O) increased sharply, suggesting that C C/ C H in biochar powder and particles both changed into C in oxidation states (CO, C¼O and O C¼O). However, it was only

Table 2 Correlation coefficients between biochar cumulative mineralization rates (%) at various incubation time and the soil characteristics (n = 5).

150 d 225 d 300 d 390 d 150–390 d

Clay

Silt

sand

Soil pH

Soil N

Soil TOC

Soil MBC

0.438 0.414 0.584 0.567 0.542

0.542 0.489 0.654 0.635 0.558

0.619 0.546 0.701 0.681 0.562

0.456 0.208 0.224 0.247 0.019

0.369 0.273 0.292 0.269 0.103

0.774 0.968** 0.970** 0.976** 0.914*

0.005 0.048 0.009 0.014 0.017

TOC: total organic carbon. MBC: microbial biomass carbon. * Significant correlated at P < 0.05. ** Significant correlation at P < 0.01.

found in biochar powder that the relative contents of C C/C H/ C¼C in the biochar samples incubated with LN and GD soils were lower compared with other soils while C in oxidation states were higher. In addition, C O was the major component of C oxidized states in the biochar powder incubated with LN and GD soils. 4. Discussion 4.1. Biochar carbon stability in paddy soil Total C mineralization in paddy soils (expressed as mg CO2 per gram TOC) decreased after the application of RS biochar (Figs. 1 and 2). Such pattern has also been observed by Fang et al. (2014). This is mainly attributed to the relatively higher stability and lower mineralization rates of RS biochar-C than native organic C in paddy soils. In respect to biochar-C mineralization, the progressively slower and then stabilized biochar-C mineralization rate over time (Fig. 3) was consistent with other observations reported in the literature (Singh et al., 2012; Fang et al., 2014). This pattern suggests that labile C components in RS biochar could be mineralized rapidly at the initial stage and then biochar-C mineralization rates would be largely decreased due to slower decomposition of relatively stable C components in biochar. In addition, the proportions of RS biochar-C mineralized in paddy soils (0.17–0.28%) are similarly as low as woody biochar reported by Singh et al. (2012). However, it is not in accordance with some other previous studies which suggested that grass-derived biochars mineralized faster than wood-derived biochars (Zimmerman, 2010). This inconsistency can possibly be attributed to the intrinsic recalcitrance of RS biochar and the lower oxygen availability in paddy soils than upland soils which were not waterlogged. Previous studies have suggested that predominant aromatic structure was the main reason that biochar was considered as a recalcitrant form of C with long MRTs (Brewer et al., 2009; Mao et al., 2012). The quantitative 13 C NMR results showed that aromatic C contents in RS biochar were comparatively high (94.4%) (Table S1). Recently, it has been reported that aromatic C components still dominated in the rice straw-derived charcoal in 3700 years old ancient paddy soil (Wu et al., 2015a). Therefore, RS biochar was chemically highly recalcitrant due to its highly aromatic structure. Additionally, it

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Table 3 Mean residence time (MRT) of labile and recalcitrant pools of biochar carbon (C), and the proportion of labile and recalcitrant C in biochar in the five soils. The parameters were estimated using the Two-Pool Exponential Model Fitted to the cumulative (%) biochar C mineralized over the 390 days period. Treatments

LN SD JS ZJ GD

Mean residence time Labile C (days)

Recalcitrant C (years)

19 37 18 21 26

857 2829 1896 971 617

Adjusted R2

Labile C (%) in biochar

Recalcitrant C (%) in biochar

0.979 0.982 0.994 0.996 0.982

0.14  0.01 0.16  0.01 0.11  0.00 0.13  0.00 0.12  0.01

99.86  0.01 99.84  0.01 99.89  0.00 99.87  0.00 99.88  0.01

LN: Liaoning soil amended with biochar; SD: Shandong soil amended with biochar; JS: Jiangsu soil amended with biochar; ZJ: Zhejiang soil amended with biochar; GD: Guangdong soil amended with biochar.

is also reported that silica-encapsulation protection could enhance the stabilities of RS biochar and this protection only occurred for RS biochar produced at 500
C, not for 300
C and 700
C (Guo and Chen, 2014). The RS biochar used in this study was produced at 500
C and thus its stability might be increased by the silicaencapsulation protection. Moreover, it has been suggested that C loss and O/C ratio of all tested biochar types were significantly higher under unsaturated conditions than saturated conditions, as the availability of oxygen for biotic and abiotic decomposition was increased under unsaturated conditions (Nguyen and Lehmann, 2009). In this study, paddy soils were kept under saturated conditions over the whole incubation period and thus C stability of RS biochar in paddy soils could be increased through the decreasing of oxygen availability. Due to a relatively low biochar-C mineralization rates, the estimated MRTs (617–2829 years) of stable carbon components in RS biochar in paddy soils are much longer than those reported in previous studies (Bird et al., 1999; Fang et al., 2014). Furthermore, the estimated MRT of biochars may increase further with the extension of incubation time due to the depletion of labile components and the interaction with soils minerals. For example, the estimated MRTs of leaf derived biochar-C produced at 550
C increased from 518 to 736 years with the incubation time extending from 1 year to 3 years (Singh et al., 2012). Therefore, the estimated MRTs of RS biochar-C in paddy soils of this study are expected to be increased in a longer incubation period. 4.2. Influence of native soil C on biochar carbon stability in paddy soil Among the soil physicochemical properties (Table 1), native soil organic carbon content can significantly influence RS biochar-C

cumulative mineralization rate at the late incubation stage, but clay content or pH value shows no significant impact (Table 2). This clearly reflects the importance of native soil TOC content in stabilizing biochar-C mineralization in paddy soils. Multiple studies showed that the mineralization of biochar-C could be increased with the increasing organic matter content in soil. For example, Hamer et al. (2004) reported that the addition of glucose accelerated the mineralization of biocha-C via microbial cometabolism. Luo et al. (2011) found that the C mineralization of Miscanthus giganteus straw biochar incubated under 40% water holding capacity condition significantly increased with soil total carbon content increasing from 0.87% to 0.98%. However, our results are the first to demonstrate the significant impact by native soil TOC content on biochar-C stability under waterlogged conditions. Some studies have shown that the co-metabolic effect of added labile C increases biochar-C mineralization rates in a short term incubation (Kuzyakov et al., 2009; Keith et al., 2011). Therefore, it can be proposed in our study that native soil organic carbon provides substrates for microbial co-metabolism and thus the RS biochar-C mineralization via co-metabolic effect could be increased with increasing native soil TOC content at the late incubation stage (225, 300 and 390 days). However, at the early incubation stage (before 150 days) the biochar-C was mainly decomposed by microorganisms through directly utilizing the labile C components in biochar (Table 3). As a result, native soil TOC content that significantly impacted on biochar-C stability via microbial co-metabolism at the late incubation stage, showed no significant influence on biochar-C mineralization at the early incubation stage. In addition, the input of plant-derived C (such as root exudates, plant litter), which generally occurs under field conditions and may significantly impact on biochar-C stability in

Fig. 5. Fourier-transform infrared spectra (FTIR) of the biochar samples collected from different paddy soils with biochar amendment (Origin: original biochar; LN: Liaoning soil amended with biochar; SD: Shandong soil amended with biochar; JS: Jiangsu soil amended with biochar; ZJ: Zhejiang soil amended with biochar; GD: Guangdong soil amended with biochar).

M. Wu et al. / Agriculture, Ecosystems and Environment 223 (2016) 59–66 Table 4 Atomic elemental contents of C, O, and atomic O/C ratios for biochar particles and finely ground powder after 390 days incubation as determined by X-ray Photoelectron Spectroscopy (XPS) spectra (pooled samples from N = 3). LN

SD

JS

ZJ

GD

Biochar powder C (%) 85.3 O (%) 14.7 O/C (%) 0.17

Original biochar

73.0 27.0 0.37

68.2 31.8 0.47

78.4 21.6 0.28

74.0 26.0 0.35

71.0 29.0 0.41

Biochar particles C (%) 80.5 O (%) 19.5 O/C (%) 0.24

68.7 31.3 0.46

75.7 24.3 0.32

71.4 28.6 0.40

59.4 40.6 0.68

35.7 64.3 1.80

LN: Liaoning soil amended with biochar; SD: Shandong soil amended with biochar; JS: Jiangsu soil amended with biochar; ZJ: Zhejiang soil amended with biochar; GD: Guangdong soil amended with biochar.

paddy soils (Wu et al., 2015b), was excluded in our experiment. Therefore, the influence of native soil organic C on RS biochar-C mineralization under the input of plant-derived C still remains further research. 4.3. Biochar structural properties as indicators of biochar carbon stability in paddy soils Following application to paddy soils, RS biochar displayed significant changes in structural properties, especially carbon functional groups. Based on the results of FTIR and XPS, it suggested that C C/C H/C¼C in RS biochar was changed into oxygen-containing functional groups such as C O, C¼O and O C¼O, and thus the O/C ratio of RS biochar increased significantly following their applications to various paddy soils (Fig. 4 and Table 4). It has been reported that oxidation of BC particles themselves and adsorption of non-BC may both increase the number of oxidized groups in BC (Lehmann et al., 2005; Cheng et al., 2006). However, in paddy soils which have lower oxygen availability than dry land soils, oxidation of biochar may contribute less to the increase of oxygen-containing functional groups in biochar compared with adsorption of non-BC such as soil organic carbon. It has been suggested in FTIR and XPS results that the atomic O/C ratios and relative contents of C in oxidation states, especially COC, were greater in the biochar samples collected from paddy soils with higher TOC content such as GD and LN soils Table 5 Chemical composition of carbon (C1s) for biochar particles and finely ground powder after 390 days incubation as determined by XPS spectra. Functional groups

C1s composition (%) CC, CH or C¼C

Suma

CO

C¼O

OC¼O

Origin biochar LN SD JS ZJ GD

Biochar powder 99.5 70.1 83.0 91.5 92.2 60.4

0.5 29.9 17.0 8.4 7.8 39.6

0.5 22.4 9.5 2.0 0.1 27.2

N/D 2.2 5.3 6.4 6.9 7.8

N/D 5.3 2.2 N/D 0.8 4.6

Origin biochar LN SD JS ZJ GD

Biochar particles 63.6 58.5 42.4 34.6 32.1 47.8

36.4 41.5 57.6 65.4 67.9 52.2

26.9 36.4 32.4 23.8 9.9 9.1

1.4 4.9 5.0 23.5 27.6 28.6

8.1 0.2 20.2 18.1 30.4 14.5

N/D = not detected. LN: Liaoning soil amended with biochar; SD: Shandong soil amended with biochar; JS: Jiangsu soil amended with biochar; ZJ: Zhejiang soil amended with biochar; GD: Guangdong soil amended with biochar. a Sum of oxygen-containing functional groups (C O, C¼O, OC¼O).

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(Fig. 4 and Table 4). This may indicate that the amounts of biocharC in oxidation states were increased by the adsorption of soil organic carbon onto biochar surfaces. However, soil minerals such as Si and Fe, which could be deposited on biochar surfaces and increase biochar C stability in a long term (Nguyen et al., 2009), were not taken into account in our incubation study. Therefore, long term filed research will still be needed in order to examine the influence of soil minerals on biochar C stability in paddy soils. In addition to biochar-C mineralization rates, biochar structural properties such as the composition of carbon functional groups and atomic O/C ratio were generally used as the indicators of biochar-C stability. Singh reported that the proportion of biochar-C mineralized and MRT of C in biochars were strongly and nonlinearly correlated with the initial proportions of nonaromatic C in biochars (Singh et al., 2012). It was also suggested that biocharC stability increased with the decreasing atomic O/C ratios of biochar (Spokas, 2010). In this study, atomic O/C ratio of biochar powder showed similar trend with biochar-C cumulative mineralization rates (Table 4 and Fig. 2). It inferred that atomic O/C ratio based on XPS analysis could be very good indicators of biochar-C stability following application to paddy soils. Moreover, the XPS results suggested that greater atomic O/C ratio and oxygencontaining functional groups were found in biochar samples incubated with GD and LN soil, which have higher native soil TOC content. This further support our conclusion that RS biochar-C is less stable in paddy soils with higher TOC content. 4.4. Implications for RS biochar application in paddy soil Direct return of rice straw into paddy soils has long been adopted as an effective strategy to increase soil carbon sequestration (SCS) potentials in rice paddies (Lu et al., 2009). However, the increased methane emissions due to the directly straw returning could greatly offset the mitigation benefits of SCS via straw return in paddy soils (Lu et al., 2010). Nevertheless, biochar technology is considered to have great potentials in increasing SCS and decreasing methane emissions simultaneously. It has been confirmed in previous studies that RS biochar application could significantly suppress methane emissions from paddy soils (Dong et al., 2013). In this study, our results indicated that RS biochar-C had relatively low cumulative mineralization rates and considerably long MRTs in various paddy soils. Therefore, RS biochar application could be an effective method for SCS in rice paddies. In order to maximize the GHG mitigation benefits, direct rice straw return should be replaced with RS biochar application. However, chemical interactions with soil minerals could contribute to the stabilization of biochar through limiting its accessibility to soil microorganisms (Lehmann et al., 2011). Input of available carbon and nitrogen sources may promote the degradation of biochar via stimulating microbial activities (Hamer et al., 2004; LeCroy et al., 2013). All these processes were not taken into account in our study and thus need further research when assessing biochar-C stability and its C sequestration effect in paddy soils. Moreover, with the increase of native soil TOC content, RS biochar-C cumulative mineralization rates increased and MRTs decreased in paddy soils. RS biochar-C oxidation was also more obvious in paddy soils with higher native soil TOC content such as LN and GD. Therefore, considering the benefits of greater carbon sequestration effect following RS biochar application in paddy soils, RS biochar produced at 500
C may be more effective for longterm carbon sequestration when applied in paddy soils with lower TOC content. Furthermore, it was previously known that RS biochar application could significantly increase rice yields of paddy soils (Wang et al., 2012; Dong et al., 2013). Thus, the low rice yields of paddy soils with low TOC content will also be greatly improved after RS biochar application.

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5. Conclusion RS biochar application could be an effective method for soil C sequestration in rice paddies. Cumulative mineralization rates of RS biochar-C incubated with different paddy soils were relatively low. The estimated MRT of stable C components of RS biochar were considerably long in various paddy soils. However, RS biochar-C cumulative mineralization rates increased with the increasing native soil TOC content. For long-term C sequestration, paddy soil with lower TOC content is a better option for RS biochar application. Further studies are needed to examine the influence of soil minerals and input of available carbon and nitrogen sources in RS biochar-C stability in paddy soils. Conflict of interest The authors declare no competing financial interest. Acknowledgements This research was supported by the National Key Technology R&D Program (2015BAC02B01), the National Natural Science Foundation of China (41271247, 41571241) and the Natural Science Foundation of Zhejiang Province (LZ15D030001). Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.agee.2016.02.033. References Bird, M., Moyo, C., Veenendaal, E., Lloyd, J., Frost, P., 1999. Stability of elemental carbon in a savanna soil. Glob. Biogeochem. Cycles 13, 923–932. Brewer, C.E., Schmidt-Rohr, K., Satrio, J.A., Brown, R.C., 2009. Characterization of biochar from fast pyrolysis and gasification systems. Environ. Prog. Sustain. Energy 28, 386–396. Bolan, N.S., Kunhikrishnan, A., Choppala, G., Thangarajan, R., Chung, J., 2012. Stabilization of carbon in composts and biochars in relation to carbon sequestration and soil fertility. Sci. Total Environ. 424, 264–270. Cheng, C.-H., Lehmann, J., Thies, J.E., Burton, S.D., Engelhard, M.H., 2006. Oxidation of black carbon by biotic and abiotic processes. Org. Geochem. 37, 1477–1488. Dong, D., Yang, M., Wang, C., Wang, H., Li, Y., Luo, J., Wu, W., 2013. Responses of methane emissions and rice yield to applications of biochar and straw in a paddy field. J. Soils Sediments 13, 1450–1460. Fang, Y., Singh, B., Singh, B., Krull, E., 2014. Biochar carbon stability in four contrasting soils. Eur. J. Soil Sci. 65, 60–71. Guo, J., Chen, B., 2014. Insights on the molecular mechanism for the recalcitrance of biochars: interactive effects of carbon and silicon components. Environ. Sci. Technol. 48, 9103–9112. Hamer, U., Marschner, B., Brodowski, S., Amelung, W., 2004. Interactive priming of black carbon and glucose mineralisation. Org. Geochem. 35, 823–830. Hilscher, A., Knicker, H., 2011. Degradation of grass-derived pyrogenic organic material: transport of the residues within a soil column and distribution in soil organic matter fractions during a 28 month microcosm experiment. Org. Geochem. 42, 42–54. Keith, A., Singh, B., Singh, B.P., 2011. Interactive priming of biochar and labile organic matter mineralization in a smectite-rich soil. Environ. Sci. Technol. 45, 9611–9618. Kuhlbusch, T., Crutzen, P., 1995. Toward a global estimate of black carbon in residues of vegetation fires representing a sink of atmospheric CO2 and a source of O2. Glob. Biogeochem. Cycles 9, 491–501. Kuzyakov, Y., Subbotina, I., Chen, H., Bogomolova, I., Xu, X., 2009. Black carbon decomposition and incorporation into soil microbial biomass estimated by 14C labeling. Soil Biol. Biochem. 41, 210–219.

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