Straw-derived biochar mitigates CO2 emission through changes in soil pore structure in a wheat-rice rotation system

Journal Pre-proof Straw-derived biochar mitigates CO2 emission through changes in soil pore structure in a wheat-rice rotation system

Ruqin Fan, Baohua Zhang, Jiangye Li, Zhenhua Zhang, Aizhen Liang PII:

S0045-6535(19)32569-X

DOI:

https://doi.org/10.1016/j.chemosphere.2019.125329

Reference:

CHEM 125329

To appear in:

Chemosphere

Received Date:

28 July 2019

Accepted Date:

05 November 2019

Please cite this article as: Ruqin Fan, Baohua Zhang, Jiangye Li, Zhenhua Zhang, Aizhen Liang, Straw-derived biochar mitigates CO2 emission through changes in soil pore structure in a wheatrice rotation system, Chemosphere (2019), https://doi.org/10.1016/j.chemosphere.2019.125329

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Journal Pre-proof Straw-derived biochar mitigates CO2 emission through changes in soil pore structure in a wheat-rice rotation system

Ruqin Fan a, b, Baohua Zhang c, Jiangye Li a, b, Zhenhua Zhang b *, Aizhen Liang d, * a

College of Environmental Science and Engineering, Zhongkai University of

Agriculture and Engineering, Guangzhou, 510225, China b

Institute of Agricultural Resources and Environment, Jiangsu Academy of

Agricultural Sciences, Nanjing, 210014, China c

School of Environment and Planning, Liaocheng University, Liaocheng, 252000,

China d

Key Laboratory of Mollisols Agroecology, Northeast Institute of Geography and

Agroecology, Chinese Academy of Sciences, Changchun, 130102, China

Abstract To better understand the relationships between soil pore structure features and soil CO2 emission and soil organic carbon (SOC) sequestration following different straw return modes, undisturbed soil cores (0-5 cm and 5-10 cm) were collected from a rice-wheat rotation system under 4 straw return treatments as (1) no straw return (CK), (2) straw direct return (DR), (3) straw biochar return (BR); (4) straw-pig manure fermentation return (FR) for six years. Pore structure parameters including pore size distribution, porosity, connectivity, anisotropy and fractal dimension (FD) were determined using X-ray computer tomography. Soil CO2 flux and concentrations of SOC, readily oxidable carbon and nutrients were also measured. The results showed that BR and FR had significantly higher SOC concentration than DR and CK. Porosity and number of >500 μm and 500-100 μm macropores, FD and connectivity

Journal Pre-proof were significantly highest under FR and was lowest under BR. FR and DR produced 28.1%-32.4% higher C-CO2 than CK and BR in wheat growing season, and 9.80%-16.9% higher in rice season. Soil CO2 emission and C concentrations were significantly related to soil pore structure parameters. The CO2 emission was most significantly related to number of > 500 μm pores and FD, indicating that poorly developed pore structure under BR hindered the production and diffusion of CO2 from soil. These results enhanced our understanding of the relationship between soil pore structure and CO2 emission following biochar application, and provided evidence for decision making process in choosing proper straw managements to promote SOC sequestration and reduce CO2 emission. Key words: Biochar, CO2 emission, Straw application, Soil organic carbon, Soil pore system, X-ray CT

1 Introduction The CO2 from soil is a major agricultural by-product which has been changing the global climate as agricultural production feed the global population (Schlesinger and Amundson, 2018). There is a > 95% probability that anthropogenic activities over the past decades have raised global temperature predominantly due to increased greenhouse gas (GHG) emission (IPCC, 2014). Reducing CO2 emission and sequestering carbon to agricultural soils are key promising strategies to slow down the increase in atmospheric GHG concentrations (Lal, 2010; Fang et al., 2018). Return of agricultural straw to soil has been recommended to be a promising practice to improve soil fertility and counteract global warming (Zang et al., 2016; Htun et al., 2017; Chen et al., 2019). However, the application of agricultural straw has often

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Journal Pre-proof drawn criticisms due to its potential issues. More CO2 emissions have been frequently reported in soils with straw return (Yan et al., 2012; Liu et al., 2014; Wang et al., 2019). The straw direct-return, which is most widely used among straw return modes at present, was reported to create unfavorable soil environment for root penetration due to limited time for straw biodegradation (Li et al., 2018). Negative effects on crop seedling development were also found following straw direct-return in the rice (Oryza sativa L.) and wheat (Triticum aestivum L.) rotation system (Wuest et al., 2000; Zuo et al., 2010; Shan et al., 2008). In this context, developing proper straw return modes that can benefit soil productivity and reduce CO2 emission has been a big challenge and research focus worldwide (Li et al., 2018; Wang et al., 2019). The rice and wheat rotation system which occupies about 4.5 million ha in China (Dawe et al., 2004) is an extremely important cropping system for food security. Large amount of rice and wheat straw is produced every year. The pyrolysis of straw into biochar has been advocated as an environment-friendly approach for straw utilization. Among the possible strategies for removing CO2 from the atmosphere, the biochar solution is regarded notable and of higher potential (Zhang et al., 2019). Incorporation of biochar in soil has also been widely recognized to have benefits in carbon sequestration and soil fertility improvement (Steinbeiss, et al., 2009; El-Naggar et al., 2015; Awad et al., 2018). However, negative or nil impacts of biochar on greenhouse gas emissions were also frequently reported (Liu et al., 2019a; van Zwieten et al., 2019). Spokas and Reicosky (2009) examined effects of 16 different biochar on GHG emission and concluded that biochar addition could increase CO2 release from soil. Castaldi et al (2011) found that biochar incorporation showed a minimal impact on GHG emissions and microbial parameters. Liu et al. (2016) found no effect of biochar on soil CO2 efflux across Chinese agricultural soils.

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Journal Pre-proof The potential mechanisms beneath the effects of biochar on soil CO2 emission have been discussed. It is generally acknowledged that soil respiration depends on many factors including soil temperature, soil air and water conditions, nutrient transportation, etc., most of which are related to soil pore system (Yuste et al., 2003; Buragiene et al., 2019). Nonetheless, the relationships between soil CO2 emission and soil pore structure following biochar application have received little attention. Soil pores play a key role in various soil functions and processes, including decomposition of organic matter by microorganisms, provision of optimal conditions for microbial activity, transportation of air, water, and nutrients, etc. (Gregory et al., 2007; Katuwal et al., 2015; Yu and Lu, 2019). The movement of gas and water in soil is influenced not only by the number of pores but also by the size distribution and other geometric characteristics of soil pore structure. Morphological features including connectivity, fractal dimension, anisotropy, porosity, etc., were effective indices for assessing soil structure (Dal Ferro et al., 2013; Zhao et al., 2017; Liang et al., 2019). Study by Amoakwah et al. (2017) showed that biochar application led to significant increase in soil water retention as a result of increased microporosity (pores < 3μm). Sun et al. (2013) found that birch wood biochar effectively improved soil macroporosity and pore tortuosity and organization. Although there are evidences showing the influence of biochar and straw in changing soil pores, most of the studies investigated soil pore structures only by conventional analytical methods, whereas the microscale information was not provided. The X-ray microtomography (CT) permits non-destructive investigations of the soil pore system and provides a direct procedure to quantify the geometrical attributes of the pore system in three dimensions (De Gryzeet al. 2006; Kravchenko et al. 2011). Dal Ferro et al. (2013) employed X-ray CT in study of soil cores and aggregates and found that the pore-size distribution was

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Journal Pre-proof strongly affected by soil organic carbon (SOC) level. Liang et al. (2019) found close relationships between soil pore structure and distribution of soil microbes and SOC using X-ray micro-CT. Yu and Lu (2019) studied soil macropore networks using X-ray CT and found reduced macroporosity following biochar application. Few studies, however, have applied X-ray CT to quantify the effects of straw return on soil pore structure. Although effort has been put into revealing the effects of straw and biochar application on soil pore structure features, the mechanisms underlying most of the observed effects still remain unclear. Pore structure-related functions of soil are not available due to poor understanding of the interactions between soil and biochar at the microscale. The objectives of this study were (1) to investigate the SOC sequestration and CO2 emission under different straw return modes in the rice-wheat rotation system, (2) to investigation of the effect of straw return modes, especially straw-derived biochar, on soil pore structures using X-ray CT technique, (3) and to analyze the correlations between CO2 emission, SOC and soil pore structure and thereby, to reveal how straw return modes affect CO2 emission through changes in soil pore system. 2 Materials and methods 2.1 Site description and experimental design The straw incorporation experiment was established on a yellow-brown soil (Alfisol) in summer of 2013 in an experimental station (118°61′ E, 32°48′ N) in Luhe County, Nanjing, Jiangsu Province, China. The site is located in subtropical monsoon humid climate zone with annual temperature and precipitation at 16.1 °C and 797 mm, respectively. The average texture in top soil layer (0-10 cm) was 260 g kg-1 sand, 528 g kg-1 silt, and 212 g kg-1 clay. The field had been cultivated for rice and wheat

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Journal Pre-proof production under chemical fertilization management for more than 30 years before the study started. The initial SOC concentration, total nitrogen (N) concentration, bulk density and pH (H2O) was 7.1 g/kg, 1.1 g/kg, 1.3 g/cm3 and 6.9, respectively, before the study. The cropping system was a rice-wheat rotation. Four straw return treatments were studied: (1) control, no straw return (CK); (2) straw direct return (DR); (3) straw biochar return (BR); (4) straw-pig manure fermentation (straw compost) return (FR). In DR, the straw was directly returned to soil surface after cutting to 5-10 cm pieces by machine during harvest. The concentrations of total C, N and phosphorus were 405 g kg-1, 6.3 g kg-1 and 1.9 kg-1, respectively, for wheat straw, and 391 g kg-1, 9.0 g kg-1 and 3.0 g kg-1, respectively, for rice straw. In BR, rice straw was processed into biochar by fast pyrolysis at 600 °C and then returned to soil surface twice a year, at a rate of 8000 kg ha-1 after wheat harvest and 8000 kg ha-1 after rice harvest with same application method. Total C and N concentrations in the biochar were 79.6 g kg-1 and 9.7 g kg-1, respectively. The pH (H2O), porosity and water-holding capacity of the biochar were 7.6, 76.3% (v/v) and 105% (w/w), respectively. In CK, DR, and BR, chemical fertilizers were pure nitrogen (N), phosphorus (P) and potassium (K) applied at 175, 95 and 210 kg ha−1, respectively, during the wheat season and 220, 114 and 260 kg ha−1, respectively, during the rice season. In FR, straw and pig manure were fermented at a local organic fertilizer factory at a 4: 6 ratio, and chemical fertilizers were supplemented to ensure the same amount of total N applied with other treatments. The experimental design was a randomized complete block with four replicates. In total 16 plots were included with the size of 12 m × 8 m each. 2.2 CO2 flux measurement and estimates of seasonal emission Three polyvinyl chloride (PVC) collars (10 cm in diameter and 5 cm in height)

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Journal Pre-proof were vertically inserted 5 cm deep into soil surface between crop rows in each plot three days before the first measurement. The soil around the outside wall of each PVC collar was tightly compacted to prevent gas leakage. The PVC collars were removed before harvest and re-inserted into soil after harvest following the same protocol as described previously. Soil CO2 emission from each PVC collar was measured biweekly at 9:00-11:00 a.m. using a LI-8100 automated soil CO2 flux system (LI-COR Inc., Lincoln, NE, USA) for a 2-year period from 20 June 2017 to 18 June 2019. Soil temperature at 5 cm depth was measured using stem thermometers near the collar during CO2 flux measurements. Cumulative CO2 emission was calculated according to a previous study (Shi et al. 2012). Estimates of soil CO2 emission for wheat and rice growing seasons were calculated using the follow equation (Sims and Bradford, 2001): n 1

TSR   SRm ,k t k

(1)

k 1

where TSR is total soil CO2 emission in each plant growing season; SRm,k is the measured averaged CO2 flux rate over the interval tk+1 to tk; Δtk is the number of days between each field measurement within the season; n is the number of soil CO2 flux measurements in each season. 2.3 Soil sampling and measurements Three intact soil cores were collected from 0-5 cm and 5-10 cm soil depth of each plot using PVC cylinders (5 cm in inner diameter and 5 cm in height) in May 2019 right before wheat harvest. Soil cores were carefully wrapped in plastic films and transported to the laboratory for CT scanning. After that, soil samples were air-dried in room temperature. Any visible residues and stones were removed and the soils were passed through a 0.154-mm sieve for SOC measurement. Total soil carbon was determined using a Flash EA 1112 elemental analyzer (Thermo-Finnigan, Milan, 7 / 35

Journal Pre-proof Italy). The studied soils were free of carbonates, and the SOC was assumed to equal the total C. Soil readily oxidable carbon (ROC) was measured using a UV–vis spectrophotometer (UV-1200, Shanghai, China) after oxidation with 333 mmol L–1 potassium permanganate (Blair et al., 1995). 2.4 X-ray computed tomography scanning and image processing Intact soil cores (5 cm in diameter and 5 cm in length) were scanned with an industrial Phoenix Nanotom X-ray µ-CT (GE, Sensing and Inspection Technologies, GmbH, Wunstorf, Germany). The scans were performed at the center of the core obtained with the PVC cylinder. A set of 2300 images for each soil core was obtained with image resolution acquisition at 25 μm (isotropic voxel). A 0.2 mm copper filter was used to alleviate the beam hardening effect. The experimental conditions were 110 kV with 110 µA X-rays and 2284 × 2304 pixels per image. Ring artifacts in some slices were removed before image segmentation (Zhou et al. 2013). Image processing, visualization, quantification and reconstruction were carried out using ImageJ software (National Institutes of Health, Bethesda, MD, USA). Segmentation of the grayscale slices was carried out using a global thresholding method (Zhou et al. 2012) and produced binary images where soil pores were represented by white pixels and solid material by black (Pires et al. 2017). After segmentation, pores smaller than 8 voxels, representing 0.001mm3, were removed to reduce noise. Pore morphology analysis was completed using the BoneJ plugin package from ImageJ software. Pore sizes are classified into four groups according to equivalent diameter, including > 500 μm, 500-100μm, 100-30 μm, and < 30 μm (micropores). Due to the resolution limit, only macropores (the first three sizes) were used in this study. The fractal dimension (FD) was determined in this study to quantify

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Journal Pre-proof self-similarity and scale-independent properties of the soil cores (Dal Ferro et al. 2013). Fractal ranges values were calculated using the box-counting method by covering the image stack with cubic boxes of side ε and recording the number of boxes (N(ε)) intersecting the pores within the stack (Kravchenko et al. 2011). Basically, the image stack was covered with various cube or box sizes and the number of boxes intersecting the pores within the stack was recorded. The soil porosity is calculated as: 𝑉𝑝

(2)

𝑃𝑜𝑟𝑜𝑠𝑖𝑡𝑦 = 𝑉𝑡

where Vp and Vt were the volume of void voxels and the total sample volume (void plus solid voxels), respectively. Connectivity was calculated using the Euler–Poincaré volumetric characteristic (Deurer et al., 2009) to provide a comparable measure of pore connectivity density (hereafter Ev). The lower the Ev value, the higher the connectivity of the soil pore system. Ev is quantified as follows: 𝐸𝑉 =

𝐼―𝐶 𝑉𝑜𝑙

(3)

where I was the number of clusters that are not interconnected; C was the number of redundant connections; V was the volume represented by the image stack. The anisotropy (ANI) is an indicator of the degree of dissimilarity in orientation of substructures within a volume. The possible range of ANI values were from 0 (totally isotropic) to 1 (totally anisotropic), with 1 indicating a high degree of ANI. It was obtained using the mean intercept length method (Harrigan and Mann, 1984): 𝐿𝑠

(4)

𝐴𝑁𝐼 = 1 ― 𝐿𝑙

where Ls and Ll represented the shortest and longest of mean intercept length ellipsoid, respectively.

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Journal Pre-proof 2.5 Statistical analysis The least significant difference (LSD) method was used to test the effect of straw return modes on dependent variables of soil nutrient and C concentrations, soil temperature, CO2 emission and pore system parameters at the P = 0.05 level of statistical significance. Analysis of variance (ANOVA) was carried out using the GLM procedure in the SAS 9.3 software (SAS Institute, Cary, NC, USA). 3 Results 3.1 Effects of straw retuning modes on SOC and nutrient concentrations The SOC concentrations were significantly higher under BR, FR and DR than under CK in the upper 5 cm soil depth. The SOC in 5-10 cm showed a similar patter among treatments, except that the SOC under DR was not significantly different compared with CK, and was significantly lower than BR (Table 1). BR had the highest SOC concentration which was 36.9%, 10.7% and 4.8% higher than CK, DR and FR, respectively, at 0-5 cm depth and 33.6%, 18.6% and 13.4% higher than CK, DR and FR, respectively, at 5-10 cm depth. The ROC concentrations under BR and CK were significantly lower than that under FR and DR in the top 5 cm layer. FR had the highest ROC concentration among all treatments in both soil depths. Total P concentration in soil was significantly higher under FR than under CK, DR and BR in both soil depths, and the value was significantly higher under BR than under CK and DR. Concentrations of total N and K were significantly higher in soil under BR than under the other 3 treatments (Table 1). Table 1 Soil organic carbon (SOC), readily oxidable carbon (ROC) and nutrient concentrations in soil under different straw returning modes (n = 4). Soil depth (cm)

Treatment

SOC kg-1)

(g

ROC kg-1)

(mg

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Total N (g kg-1)

Total P (g kg-1)

Total K (g kg-1)

Journal Pre-proof 0-5

CK DR BR FR CK DR BR FR

5-10

7.12 c 8.81 ab 9.75 a 9.30 a 7.03c 7.92 bc 9.39 a 8.28 b

2.94c 3.83b 3.05c 4.19a 2.84b 3.12ab 2.53b 3.56a

0.98 b 0.99 b 1.33 a 1.10 ab 0.96 b 0.94 b 1.34 a 1.10 ab

0.57 c 0.51 c 1.05 b 1.36 a 0.69 c 0.50 c 0.93 b 1.30 a

11.32b 12.27ab 13.95a 12.21ab 10.24c 10.52c 13.08a 11.99b

Note: CK, chemical fertilizers with no straw return; DR, straw direct return with chemical fertilizers; BR, straw biochar return with chemical fertilizers; FR, straw-pig manure fermentation return with reduced chemical fertilizers. Different lowercase letters in the same column within the same soil depth indicate significant differences at P = 0.05 level.

3.2 Structure features of soil pore system under different straw return modes Straw return significantly changed pore size distributions in 0-5 cm and 5-10 soil layer (Table 2). The 100-30 µm pores dominated in soil of CK, while in FR the >500 μm pores dominated. In both 0-5 cm and 5-10 cm layers, numbers of >500 μm and 500-100 μm macropores were significantly higher under FR than DR, CK and BR; porosity of each macropore class showed a similar pattern with the number among all 4 treatments. BR had significantly lower number and porosity of >500 μm and 500-100 μm macropores than FR and DR. The porosity and pore number of mesopores (100-30 µm) were significantly reduced after straw return. Number and porosity of the 3 studied pore class were comparatively higher in 0-5 cm than in 5-10 cm soil depth. Table 2 Structure parameters of different pore sizes for soil cores as affected by different straw returning modes in different soil depths Soil depth (cm)

Structure parameter

Pore Size

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CK

DR

BR

FR

Journal Pre-proof

Pore number 0-5 Porosity (%)

Pore number 5-10 Porosity (%)

100-30 μm 500-100 μm >500 μm 100-30 μm 500-100 μm >500 μm 100-30 μm 500-100 μm >500 μm 100-30 μm 500-100 μm >500 μm

78115a 29992c 10197b 0.10a 0.40b 10.9c 38590a 8792b 8358c 0.05a 0.32c 7.87bc

48324b 35560b 30013b 0.05b 0.55a 14.8b 30659b 21248a 14010b 0.03ab 0.55b 9.93ab

32735c 28220c 9578c 0.02c 0.19c 8.89d 20085c 9576b 8661c 0.02b 0.39c 7.14c

39711b 47579a 64956a 0.04b 0.51a 17.5a 11763b 28072a 37965a 0.02b 0.71a 11.2a

Note: CK, chemical fertilizers with no straw return; DR, straw direct return with chemical fertilizers; BR, straw biochar return with chemical fertilizers; FR, straw-pig manure fermentation return with reduced chemical fertilizers. The same index followed by different lowercase letters indicate significant differences between treatments at P = 0.05 level.

Soil pore anisotropy, connectivity and fractal dimension were effectively affected by straw return modes, and were higher in 0-5 cm than in 5-10 cm depth (Table 3). Total porosity showed no significant difference among all straw return modes in either of the studied soil depths (P > 0.05). Anisotropy was highest under BR, and was significantly higher than the other 3 treatments. The FD values among treatments followed the order of FR > DR > CK > BR. The Ev which was negatively related to pore connectivity showed the opposite trend among treatments. Table 3 Total porosity (TP), anisotropy (ANI), Ev, and fractal dimension (FD) of soil pores under different straw returning modes Soil depth (cm) 0-5

5-10

Parameters TP (%) ANI Ev (10-3 pixel-3) FD TP (%) ANI Ev (10-3 pixel-3) FD

CK 17.4a 0.33c 0.05b 2.29bc 12.7a 0.31b 0.05b 2.12b

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DR 16.9a 0.39b 0.04bc 2.38ab 12.3a 0.35ab 0.05b 2.24ab

BR 17.3a 0.45a 0.07a 2.16c 13.5a 0.43a 0.08a 2.00b

FR 18.3a 0.37bc 0.03c 2.54a 14.1a 0.37ab 0.04b 2.35a

Journal Pre-proof Note: CK, chemical fertilizers with no straw return; DR, straw direct return with chemical fertilizers; BR, straw biochar return with chemical fertilizers; FR, straw-pig manure fermentation return with reduced chemical fertilizers. The same index followed by different lowercase letters indicate significant differences between treatments at P = 0.05 level.

3.4 Variation of soil temperature under different straw return modes Soil temperature at 5 cm depth showed a seasonal variation with local air temperature and was affected by different straw return modes (Fig. 1). The 3 straw return treatments generally resulted in higher temperature compared with CK. Annual temperature of DR (16.9 °C) was notably higher than that of CK (15.5 °C). Compared with wheat growing season (November to late June), soil temperature during rice growing season (late June to late October) showed smaller variation among treatments (Fig. 1). 30 CK DR BR FR

20

。

Soil temperature ( C)

25

15 9 8 7 6 5 4 3

10 5 0

/1 18

Jun.

Oct.

Feb.

8 9 9 9 9 01 019 01 01 01 01 2/2 /1/2 5/1/2 9/1/2 2/2/2 6/2/2 1 1 2 1 2

Jun.

Oct.

Feb.

Jun.

Fig. 1 Soil temperature at 5 cm depth from 20 June 2017 to 18 June 2019. Vertical bars indicate standard error (n = 4). Measurements covered in color grey were during rice growing season. CK, 13 / 35

Journal Pre-proof chemical fertilizers with no straw return; DR, straw direct return with chemical fertilizers; BR, straw biochar return with chemical fertilizers; FR, straw-pig manure fermentation return with reduced chemical fertilizers.

3.4 Soil CO2 flux rate and total emissions in rice and wheat growing season The soil CO2 flux rate varied from 3.55 to 35.4 g CO2 m-2 d-1 during the two years of measurement, and generally followed the seasonal pattern of soil temperature in all 4 treatments (Fig. 1; Fig. 2). The flux was relatively low when soil temperature dropped to below 10 °C in winter from December to February. The highest flux occurred in early June before wheat harvest when the soil was in an aerobic state with relatively high temperature. The differences of CO2 flux rate among the straw return treatments also occurred during this period. It was worth noting that although soil temperature was relatively smooth during rice growing season, the flux varied greatly with time, which was in accordance with the alternating flooding and dry situation of the field. Among the 4 straw return modes, FR and DR generally showed higher flux rates than CK and BR, especially when the flux levels were high (Fig. 2). 40

H CK DR BR FR

-2

-1

Soil CO2 emission rate (g CO 2 m d )

H

30

R

20

R

H W

H W

10

0

Jun.

Oct.

Feb.

Jun.

Oct.

Feb.

Jun.

Fig. 2 Soil CO2 flux rate from 20 June 2017 to 18 June 2019. Rice transplantation (R), wheat 14 / 35

Journal Pre-proof plantation (W) and harvest (H) dates are marked with vertical arrows. Vertical bars indicate standard error (n = 4). CK, chemical fertilizers with no straw return; DR, straw direct return with chemical fertilizers; BR, straw biochar return with chemical fertilizers; FR, straw-pig manure fermentation return with reduced chemical fertilizers.

Averaged soil CO2 flux rates under BR, CK, FR and DR during rice growing season were 22.4%, 21.5%, 7.42% and 5.38% higher, respectively, than that during wheat growing season (Table 4). The flux under FR and DR were significantly higher than under CK and BR in both crop growing seasons. Estimated annual soil CO2 emission was also significantly greater under FR (11.58 Mg C ha-1) and DR (11.52 Mg C ha-1) than under CK (9.17 Mg C ha-1) and BR (9.53 Mg C ha-1). Total soil CO2 emission during wheat season was higher than that during rice season throughout the treatments. FR and DR produced 28.1%-32.4% higher C-CO2 than CK and BR in wheat growing season. The differences among treatments were relatively lower in rice growing season, when FR and DR produced 9.80%-16.9% higher C-CO2 than CK and BR (Fig. 2). Table 4 Soil CO2 flux rate and total emissions in rice and wheat growing season during a 2-year measurement period. Treatment

CK DR BR FR

Soil CO2 flux rate (g CO2 m-2 d-1)

Total amount of soil CO2 emission (Mg C ha-1)

Rice season (Jun. - Oct.)

Wheat season (Nov.- Jun.)

Rice season (Jun. - Oct.)

Wheat season (Nov.- Jun.)

Annual

11.26c 12.92ab 11.71bc 13.18a

9.27b 12.26a 9.57b 12.27a

4.30b 4.93a 4.49ab 5.03a

5.31b 7.02a 5.48b 7.03a

9.17b 11.52a 9.53b 11.58a

Note: CK, chemical fertilizers with no straw return; DR, straw direct return with chemical fertilizers; BR, straw biochar return with chemical fertilizers; FR, straw-pig manure fermentation

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Journal Pre-proof return with reduced chemical fertilizers. Different lowercase letters in the same column indicate significant differences at P = 0.05 level.

3.5 Relationships between soil CO2 emission, C concentrations and pore structure The SOC concentration had a significantly positive correlation with anisotropy, and a significantly negative correlation with number and porosity of 100-30 µm pores (P < 0.05). The ROC concentration was negatively correlated with anisotropy and Ev and positively correlated with total porosity and porosity of > 500 µm pores. The correlation of average CO2 flux rates in both crop growing seasons were most significant with number of > 500 µm pores and fractal dimension. The CO2 flux rates in wheat season were negatively correlated with anisotropy and Ev, and were positively correlated with soil temperature while the CO2 flux rates in rice season showed no significant correlation with these three parameters (Table 5). Table 5 Correlation coefficient matrix of average soil physical and chemical parameters in 0-10 cm soil depth Parameters Pore number porosity

100-30 μm 500-100 μm >500 μm 100-30 μm 500-100 μm >500 μm

Total porosity anisotropy Ev Fractal dimension Soil temperature

SOC

ROC

-0.536* -0.343 -0.298 -0.592* -0.149 -0.037 0.102 0.717* -0.258 -0.321 -0.053

-0.453 0.216 0.731* -0.526 0.511 0.703* 0.034 -0.702* -0.699* 0.790* 0.219

* Significant at 0.05 level. ** Significant at 0.01 level.

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CO2 flux rate in wheat season 0.333 0.571 0.876** 0.288 0.402 0.815* 0.161 -0.693* -0.680* 0.849** 0.606*

CO2 flux rate in rice season 0.213 0.447 0.821** 0.139 0.336 0.756* 0.094 -0.571 -0.592 0.795* 0.572

Journal Pre-proof 4 Discussion 4.1 Impacts of straw return on soil C and fertility Increased SOC concentrations have been wildly reported following straw return (Lou et al., 2011; Yang et al., 2013; Fang et al., 2018; Liu et al., 2019b). Li et al. (2018) concluded that proper straw return is the most promising, sustainable, economical and feasible way for carbon sequestration in China at present. Straw biochar (BR) and straw compost (FR) application significantly raised SOC levels in this study; however, straw direct return (DR) showed no significant influence on SOC concentration at 5-10 cm depth compared with CK (Table 1). This was consistent with results of Huang et al. (2018) who found that direct straw incorporation was not effective in raising SOC level compared with other treatments including straw biochar incorporation. Many long-term field observations showed that although straw was incorporated in soil every year, SOC concentration did not necessarily increase (Fontaine et al., 2004; Poeplau et al., 2015). This could be due to the inherent quality (e.g. high C/N ratio) of raw straw that hindered straw decomposition (Shahbaz et al., 2018) or the high priming effect induced (Miao et al., 2017). Other soil physical and biochemical causes such as the interactions with the mineral soil matrix and shift of microbial community after straw return could also contributed to the low SOC concentration (Cui et al., 2018). On the other hand, the C in biochar is generally acknowledged to be more stable than in straw and is largely unavailable to soil microbes, thus the biochar return was the most effective in the increase of SOC concentration. This is in line with the evidently higher SOC concentration under BR than other straw return modes in our study. Unlike SOC, the ROC concentrations were significantly higher under FR and DR than CK, while BR showed no significant influence on ROC, resulting in significantly lower ROC under BR and CK than under

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Journal Pre-proof FR and DR (Table 1). This contributed to the higher CO2 under FR and DR than under BR and CK. The higher concentrations of soil nutrients under BR were consistent with other studies (Lou et al., 2017; Lebrun et al., 2019). This was probably due to the high soil nutrient-holding capacity of biochar which reduced nutrient leaching in soil (Zhao et al., 2016; Chen et al., 2018). Soil P concentration was increased under FR compared with other treatments, which was attributed to the P input from pig manure-straw fermentation. Overall the BR showed the most promising effects on improving soil fertility and promoting SOC sequestration compared with other straw return modes after 6 years of application. 4.2 Changes in soil pore structure induced by straw return modes It has been reported that soil management practices, such as tillage and organic matter input, could largely affected the soil pore structure features (e.g. Papadopoulos et al., 2009; Ogunwole et al., 2015). Results from X-ray CT in this study showed that different straw return modes significantly changed pore number and porosity of macropores (>500 μm, 500-100 μm) and mesopores (100-30 μm) (Table 2). FR led to the highest number and porosity of macropores with DR came next. Increased porosity of these large pores was frequently reported in soil cores and aggregates with application of organic materials including straw and organic fertilizers (Pagliai et al., 2004; Dal Ferro et al., 2013). It was worth noting that in our study the porosity of macropores was significantly higher under FR while total porosity of the soil core was similar among all 4 treatments, indicating that FR induced a notable shift from small pores to large pores. This was consistent with the findings of Dal Ferro et al. (2013) who revealed that manure and straw application in soil induced pore space reallocation with a shift from small to large pores. Our results suggested that straw return after fermentation with pig manure effectively improved soil pore structure

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Journal Pre-proof which had implications for better water infiltration and drainage. Yu et al. (2019) studied macropore networks using industrial CT and found that porosities of large macropores (600-800 μm and 1800-2000 μm) were significantly reduced following biochar addition. In our study, the number and porosity of >500 μm, 500-100 μm and 100-30 μm pores under BR were also significantly lower than that under CK, DR and FR. This could be partially due to the fact that biochar particles occupied macropores with larger size than themselves, which led to lower number and porosity of these pores (Zhang et al., 2016; Blanco-Canqui, 2017). This was proved by the observation that certain macropore size class decreased significantly with the significant increase of biochar volume at the corresponding scales (Yu et al., 2019). Other studies also suggested that the effect of biochar on soil pore structure could be due to physical interactions between biochar and soil particles (Sun & Lu, 2014; Blanco-Canqui, 2017). The significantly lower porosity of macropores and mesopores and the similar total porosity in soil under BR compared with other treatments indicated that BR induced a shift from large pores to micropores. This could be due to the “occupy effect” as explained above and partly due to the porous nature of the biochar applied with numerous micropores. The FD is an indicator used to quantify self-similarity and scale-independent properties of an object. FD increased with structural complexity (Dal Ferro et al. 2013). In our study, the FD was significantly higher under FR and DR than under CK and BR, indicating that soil structure was more complex under FR. Pore connectivity can affect gas diffusion, water flow and transport of solutes. It is a sensitive indicator to differentiate effects of management practices. Schlüter et al. (2011) reported that fertilized soils had better connected pore systems. Deurer et al. (2009) found more and better connected macropores and greater simulated gas diffusion in an organically

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Journal Pre-proof managed soil. Dal Ferro et al. (2013) reported that manure application enhanced connectivity and improved the soil core structure. Similarly, results from our study showed that FR had significantly lower Ev, which meant significantly higher pore connectivity compared with CK (Table 3). Quin et al. (2014) observed significant increases in connectivity of the largest pore and mean pore radius following addition of an oil mallee biochar using X-ray CT. However, we found significantly lower connectivity under BR in our study which was consistent with the higher anisotropy under BR. The differences could be due to the different soil types and distinct properties of the two biochars with different feedstocks and pyrolysis methods. 4.3 Soil CO2 emission following straw return Soil respiration is the primary pathway by which the CO2 fixed by plants returns to the atmosphere. It is acknowledged to be affected by natural factors (e.g., soil fertility, temperature and moisture) and human activities (e.g., straw managements, tillage, cropping, fertilization and irrigation) (Shi et al., 2012; Huang et al., 2018). There are discrepancies in the literature about the effects of straw return on CO2 emission. Straw application was often observed to increase CO2 emission in different soils and cropping systems (Badía et al., 2013; Wang et al., 2018; Wang et al., 2019). Xia et al. (2014) found from a long-term filed experiment that direct straw return worsens rather than mitigates climate change. Decreased CO2 emissions or no effects of straw return were also reported (Dossouyovo et al., 2016; Bai et al., 2017). Our results showed that FR and DR significantly increased CO2 emission in both rice and wheat growing seasons (Table 4; Fig. 2). The increased CO2 emission following straw return could be due to the fact that the C from decomposition of the added straw served as a C substrate for soil microorganisms (Dendooven et al., 2012; Yang et al., 2017). The SOC and ROC levels were significantly raised under FR and DR, which

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Journal Pre-proof partly explained the higher CO2 emission under these two treatments. The soil temperature and moisture were constantly reported to increase due to straw return, which also promoted CO2 release (Ludwig et al., 2001; Shi et al., 2012; Dong et al., 2017; Wang et al., 2019). In this study, soil temperature and ROC were notably higher under DR and FR, which also contributed to the higher CO2 emission in these two treatments. Notably, the great variation of CO2 flux with the alternating flooded and dry situation of the field emphasized the important influence of soil aerobic and anaerobic condition on soil respiration. Also, although soil CO2 emission rates were generally higher in rice season than in wheat season, the total amounts of CO2 released were higher in wheat season, probably due to the fact that wheat season was more than 3 months longer than rice season, and that the flooded and anaerobic state of soil during rice season reduced CO2 emission and narrowed the difference with wheat season. Although soil temperature and SOC concentration were increased under BR, the CO2 emission was evidently reduced compared with CK. This is consistent with result of Huang et al. (2018) who found that soil CO2 flux increased following the addition of straw, but decreased following biochar application due to the lower concentrations of labile organic C fractions in soil. The CO2 emission under BR was also significantly lower than that under FR and DR. He et al. (2016) found that after an application period of 7 years, biochar application did not significantly increase soil respiration compared with direct straw return and CK. Li et al. (2013) reported 4 to 34 times higher of CO2 emissions under direct straw return compared with straw biochar return. These findings are consistent with our results. The significantly lower ROC concentration in soil with BR could be one of the reasons for the lower CO2 emissions compared with FR and DR.

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Journal Pre-proof Furthermore, the production of CO2 is a result of biochemical activities that are affected by soil aerobic and anaerobic conditions. Thus, it is affected by soil pore distribution and pore structure features. The mechanism of soil CO2 emission to the atmosphere also involves the movement of CO2 through soil pores (Dossou-Yovo et al., 2016). Therefore, CO2 emission is to some degree controlled by the soil pore system (Pires et al., 2017). Silva et al. (2019) found that higher soil CO2 emission under an intensive tillage was related to higher number of macropores, and concluded that pore class distribution is an essential physical attribute to explain variations of soil CO2 emissions. Similarly, we found significantly lower number and porosity of macropores under BR than FR and DR in this study, which contributed to the anaerobic condition and in turn led to lower soil respiration under BR. The lower pore connectivity and FD and the higher anisotropy under BR indicated poor gas diffusion in soil profile, which further led to lower CO2 emissions compared with FR and DR. 4.4 Contributions of soil pore structure to CO2 emission and C concentrations Kay (1990) pointed out that macropores and mesopores were important in soil functions, since macropores could provide space for macrofauna activity and root penetration while mesopores played an important role in soil aeration, microbe activities and water movement (Taboada et al., 1998; Yoo et al., 2006). Our results showed that macropores were significantly and negatively related to soil CO2 emission (P < 0.01), and mesopores to SOC sequestration (P < 0.01). Aside from pore size distribution, other pore morphology features including anisotropy, connectivity and fractal dimension significantly affected CO2 flux rate (particularly in wheat season) and ROC concentrations. Overall the CO2 emission was most significantly related to number of > 500 μm pores and FD, indicating that better developed pore structure contributed to the production and diffusion of CO2 from soil to the

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Journal Pre-proof atmosphere, which is consistent with findings of Silva et al. (2019). The significantly negative correlation between ROC concentration and anisotropy and Ev showed the importance of pore connectivity and dissimilarity in pore orientation to this labile C fraction. Among all studied soil pore structure features, anisotropy and mesopores (30-100 μm) were most significantly related to SOC concentration. Garbout et al. (2013) pointed out that anisotropy was significantly related to soil gas and water transport processes. Mesopores have also been found to play very important roles in soil aeration, water movement as well as activity of soil microbes (Taboada et al., 1998; Yoo et al., 2006; Liang et al., 2019). Thus, our results indicated the important impact of gas and water transportation process and related pore structure features on SOC sequestration. 5 Conclusions The SOC and nutrient concentrations were significantly higher under BR compared with DR and FR after 6 years of application in the rice-wheat rotation system. The CO2 emissions were significantly higher under FR and DR than under CK and BR in both crop growing seasons. Straw return caused relocation of soil pores, with FR inducing a shift from small pores to large pores while BR inducing a shift from large pores to micropores. The higher percentage of large pores and higher degree of pore connectivity and fractal dimension under FR indicated that straw return after fermentation with pig manure effectively improved soil pore structure, which had implications for better water infiltration and drainage. Among all studied soil pore structure features, anisotropy and mesopores (30-100 μm) were most significantly related to SOC concentration. The CO2 emission was most significantly related to number of > 500 μm pores and fractal dimension, indicating that better developed pore structure under FR and DR contributed to the production and diffusion of CO2

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Journal Pre-proof from soil to the atmosphere. In conclusion, results from our study confirmed that BR application significantly raised SOC and nutrient concentrations; at the same time, it significantly reduced number and porosity of soil macropores, pore connectivity, and soil ROC concentration. As a result, BR had the most promising effects on improving soil fertility, promoting SOC sequestration and reducing soil CO2 emission, compared with DR and FR in the rice-wheat rotation system. Acknowledgements This research was supported by the National Natural Science Foundation of China (41401259, 41877095) and the Natural Science Foundation of Jiangsu Province (BK20161379).

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Journal Pre-proof 

Soil CO2 flux and SOC were significantly related to soil pore structure parameters

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Soil CO2 flux was lower after straw biochar return than raw straw and straw compost

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Straw biochar significantly raised concentrations of soil organic C and nutrients

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Straw biochar reduced number and porosity of macropores and increased micropores

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Straw biochar reduced pore connectivity and fractal dimension and raised anisotropy