Agriculture, Ecosystems and Environment 232 (2016) 302–311
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Response of paddy soil organic carbon accumulation to changes in long-term yield-driven carbon inputs in subtropical China Anlei Chena , Xiaoli Xiea,* , Maxim Dorodnikovb , Wei Wanga , Tida Gea , Olga Shibistovac,d, Wenxue Weia , Georg Guggenbergera,c a
Key Laboratory of Agro-ecological Processes in Subtropical Region, Institute of Subtropical Agriculture, Chinese Academy of Sciences, Hunan, 410125, China Department of Soil Science of Temperate Ecosystems, Department of Agricultural Soil Science, University of Göttingen, 37077 Göttingen, Germany Institute of Soil Science, Leibniz Universität Hannover, 30419 Hannover, Germany d VN Sukachev Institute of Forest, SB-RAS, 660036 Krasnoyarsk, Russian Federation b c
A R T I C L E I N F O
Article history: Received 17 February 2016 Received in revised form 25 June 2016 Accepted 11 August 2016 Available online xxx Keywords: Soil organic carbon Carbon sequestration Carbon inputs Yield decline Paddy field Long-term experiment
A B S T R A C T
A decrease in C inputs from the return of crop residues to soil has occurred in many regions worldwide in recent years. The effects of this decline in C inputs could provide valuable information for assessing the long-term impact of litter C inputs on soil organic C (SOC) in rice paddy soils. The present study aimed to evaluate the response of rice paddy SOC accumulation to changes in actual C inputs in subtropical China, with emphasis on the response of C accumulation to declining C inputs. For this, we used a long-term field experiment on paddy soil in a rice-rice (Oryza sativa L.) cropping system running from 1990 to 2014. The four treatments were CK (control, no fertilizer), OM (organic matter application), NPK (N, P, and K fertilizer application), and NPKOM (NPK and organic matter application). Organic matter application for the OM and NPKOM treatments included rice straw and green manure that were left in the field after harvest and chopped, along with rice residues with stubbles and roots. In all treatments, C sequestration showed an increasing trend (from 0.207 to 0.880 g kg1 yr1) in the early and middle stages of the experiment (1990–2006) followed by a decreasing trend (from 0.429 to 0.064 g kg1 yr1) in the late stage (2007–2014). The trends were more pronounced for the OM and NPKOM treatments than for their CK and NPK counterparts. The changes in SOC stocks were consistent with changes in C inputs (p < 0.01). During the late stage, yield and litter inputs from crop residues and green manure decreased, quickly affecting SOC stock in paddy soils. This declining trend in annual rice yields was mainly caused by the decline in first rice yields, accounting for 42.3–91.5% of the decrease in annual C inputs. Insufficient P or N and K supply and unfavorable climatic factors (decreases in sunshine duration and both maximum and minimum temperatures) are possible reasons for the decline in first rice yields and green manure biomass in the late stage. Collectively, the results suggest that C stocks in high-productivity paddy soils respond very sensitively to a decline in C inputs. This raises the risk of loss of C stock in paddy soil if, in the long run, a large return of C to soil with crop residues or by other sources, e.g., green manure, cannot be achieved. ã 2016 Elsevier B.V. All rights reserved.
1. Introduction Mitigation of the continuously increasing greenhouse gas emissions to the atmosphere has become an important global issue (Paustian et al., 2000). Agricultural soils attract great attention as a potential sink for atmospheric CO2, the main greenhouse gas, by sequestrating soil organic C (SOC) (Smith et al., 2000; Pan et al., 2003). Owing to its high rate of SOC accumulation,
* Corresponding author. E-mail address:
[email protected] (X. Xie). http://dx.doi.org/10.1016/j.agee.2016.08.018 0167-8809/ã 2016 Elsevier B.V. All rights reserved.
rice cultivation may play an important role in mitigation of atmospheric CO2 (Lal, 2004; Wu, 2011). Rice (Oryza sativa L.) is the most important cereal crop in China, accounting for 32.5% of the total area harvested of cereals in 2014 (FAOSTAT, 2015), mostly in tropical and subtropical regions (Li, 1992). On the regional scale, substantial accumulations of SOC in paddy soils in subtropical China have been reported (Pan et al., 2003; Sun et al., 2009; Wu, 2011). SOC accumulation has been largely attributed to the increased use of chemical fertilizers that promote increased rice yields, higher biomass production, and more crop residues to return to soil, over the last several decades (Huang and Sun, 2006; Sun et al., 2009; Wu, 2011). A meta-analysis
A. Chen et al. / Agriculture, Ecosystems and Environment 232 (2016) 302–311
of 26 long-term paddy field experiments showed that the retention of rice residues increased SOC by 0.41 Mg ha1 yr1 in the Yangtze Delta Plain of eastern China (Rui and Zhang, 2010). Similar studies conducted in southern China showed that organic matter (OM) application had significant effects on C sequestration in paddy fields (Li et al., 2005, 2010). Field experiments conducted in the Philippines and India showed similar results (Yadav, 1998; Manna et al., 2005; Pampolino et al., 2008). However, most field experiments have been conducted using a fixed rate of organic matter input (Yadav et al., 2000; Li et al., 2005; Rui and Zhang, 2010). In contrast, the rates of rice residue inputs in rice production systems managed by farmers are quite variable, so the change of SOC in field experiments does not adequately represent the reality of C sequestration in paddy ecosystems (Wu, 2011). Therefore, it is important to know how SOC responds to fluctuation in C inputs due to changes in paddy rice production. Decline in C inputs because of yield stagnation has been reported in many regions in the world since the end of the last century, following decades of increasing C inputs due to higher rice yields (Dawe et al., 2000; Yadav et al., 2000; Bhandari et al., 2002; Ladha et al., 2003; Peng et al., 2004; Ray et al., 2012; Grassini et al., 2013; Xiong et al., 2014). Xiong et al. (2014) reported that the evidently slowing growth rate was not compensated for by benefits from improved varieties and management. Meanwhile, extreme climate events (e.g., drought, flooding, or drought immediately followed by flooding) in recent years have resulted in serious negative impacts on crop production; one example is the 2009–2010 extreme drought in southwestern China (Fauna, 2010; Zhang et al., 2012). Peng et al. (2004) provided direct evidence of decreased rice yields associated with global warming in a study at the International Rice Research Institute in Los Baños, Philippines. In other Asian countries, long-term field experiments have also shown declining or stagnating yields in rice-based cropping systems (Dawe et al., 2000; Yadav et al., 2000; Bhandari et al., 2002; Ladha et al., 2003). However, the effects of that yield decline or stagnation on C stock in paddy soils are still unclear. A few studies have demonstrated inconsistent SOC responses to rice yield decline, mainly due to the differences in soil types, initial SOC level, and magnitude and duration of the decreased C inputs (Yadav, 1998; Yadav et al., 2000; Ladha et al., 2003). In subtropical China, it is extremely important to understand the consequences of decreasing C return to paddy soils on SOC stock, because stagnation and decline in rice yields are becoming common phenomena in this region (Grassini et al., 2013; Xiong et al., 2014). To explore the actual changes in C stocks in subtropical China, the fluctuation of C inputs should be examined to determine the patterns of yield changes, from an increasing trend to a declining trend or stagnation, during recent decades. Thus, the present study evaluated the response of SOC stocks and the rate of SOC changes in a rice paddy ecosystem to the changes in actual C inputs. Using a long-term fertilization experiment in the subtropical region of China as a case study, we examined the trends in rice productivity, C inputs, and topsoil SOC contents and stocks over time under different fertilization regimes, to determine the effects of fertilization practice on rice production, green manure biomass, and SOC accumulation. We put special emphasis on clarification of the response of rice paddy SOC accumulation to the changes in C inputs in subtropical China, especially under the condition of a decreasing trend in paddy rice productivity.
303
located in a typical hilly agricultural area in Taoyuan, Hunan Province (28 550 N, 111260 E). This region belongs to the subtropical humid monsoon climate zone, with mean annual precipitation of 1448 mm, mean annual temperature of 16.5 C, and a frost-free period of 283 days. The rice-cropping regime is dominated by a double rice crop rotation. The paddy soil was developed on quaternary red clay earth. Before the experiment started, the soil had a 0.20 m plow layer, which contained 14.2 g kg1 organic C, 0.55 g kg1 total P, and 1.82 g kg1 total N. The soil bulk density (BD) was 1.25 g cm3. Weather data were provided by a weather station set up next to the experimental field. 2.2. Fertilization treatments
2. Materials and methods
The long-term paddy field experiment was established in 1990. For this trial, a randomized block design with three replicates was performed. The area of each plot was 33.2 m2. Four treatments were selected in this study: no fertilizer application as a control (CK treatment; but there was C input from crop residues, i.e., stubble and roots), organic matter addition (OM treatment; i.e., with C input of straw and of green manure in addition to the crop residues), chemical N, P, and K fertilizer (NPK treatment; added N, P, and K fertilizer, C input as for CK treatment), and chemical N, P, and K fertilizer plus organic matter (NPKOM treatment; added fertilizer as for NPK treatment, C input as for OM treatment). The four fertilizer treatments represented traditional organic matter management, chemical fertilizer, and combined organic and chemical fertilizer regimes that are used locally. The additional organic matter input of the OM and NPKOM treatments included rice straw returned to the field and Chinese milk vetch (Astragalus sinicus) as green manure, and the input amount depended on the yield of rice straw and green manure per year. Chemical N, P, and K were applied as urea for N, calcium superphosphate for P, and potassium chloride for K. The annual fertilizer application rates were 262.5 kg N ha1 (1990– 1996) or 182.3 kg N ha1 (1997–2014), 39.3 kg P ha1 (1990–2014), and 137.0 kg K ha1 (1990–1996) or 197.2 kg K ha1 (1997–2014), according to the treatment design above. Urea (N fertilizer) was applied in two splits for the first rice season (40% as basal fertilizer and 60% as tillering fertilizer), and three splits for the second rice season (40% as basal fertilizer, 50% as tillering fertilizer, and 10% as panicle fertilizer). The P and K fertilizers were applied as basal fertilizers before rice transplantation. The combined rice-growing period was from the end of April to the end of October. The rice and green manure were local varieties. For CK and NPK treatments, all rice straws were harvested and removed from the plots, thus only stubble remained in the field. The plots were left fallow until the next rice was transplanted. For OM and NPKOM treatments, all harvested rice straw was cut into 5–10 cm pieces then incorporated back into the field. The residues of the first rice crop were plowed into the soil before the second rice was transplanted, and those of the second crop covered the soil surface during the fallow period and were plowed into the soil in the middle of the following April. For the OM and NPKOM treatments, the green manure was sown in October before harvesting the second rice and grown during the non-growing season for rice, then harvested and plowed into the soil with the spring plowing in the middle of April. During the trials, 3–5 cm of water was maintained above the soil surface throughout the rice growing period, although occasional drainage was also performed from the end of rice tillering to the panicle primordium differentiation stage. Field management and rice cultivation were performed according to local farming practices.
2.1. Experimental site
2.3. Sampling and analyses
The experiment was carried out in the Taoyuan Agro-ecology Experimental Station of the Chinese Academy of Sciences; it is
Upon harvest, crops were cut approximately 5–10 cm above the soil surface. Rice grains from each plot were sun-dried and
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2.4.1. Estimation of C inputs C inputs consisted of rice residues (roots and stubble) for CK and NPK treatments, and rice residues, rice straw, and green manure for OM and NPKOM treatments. Because the variability between rice yield and crop residue production was negligible (Evans and Fischer, 1999), rice yields were used as the basis of calculation of the C inputs. For estimation of proportions of rice grain, straw, stubble, and roots, the biomasses of the different parts of the rice plants were determined after harvesting in 2000 and 2012. The average proportion of whole biomass was 44.6%, 32.7%, 12.3%, and 10.4% for rice grain, straw, stubble, and roots, respectively. The C content in rice roots, straw, and green manure was 36.8%, 43.0%, and 43.5%, respectively. 2.4.2. SOC sequestration rate The SOC sequestration rate was calculated according to the SOC dynamic model (Li et al., 2010): Y = a + bt
(1) 1
where Y is content of SOC (g kg ), t is the duration of the experiment (years), a is initial SOC content (at t = 0), and b is the annual SOC sequestration rate (g kg1 yr1). Changes in rice yields, green manure biomass, and C inputs over time were calculated similarly, using the same model, with the difference that b became the annual rate of increase or decrease of rice yields, biomass of green manure, or C inputs (kg ha1 yr1), and a is the corresponding initial value (at t = 0) of rice yields, biomass of green manure, or
2.4.3. Calculation of C stocks At our experimental site, soil BD significantly decreased with time (Fig. 1), so the mass of soil at a given depth changed. This change was considered in calculating C stocks. Thus, based on the equivalent soil mass (ESM) corrections to the fixed depth (FD) method of Lee et al. (2009), we made a simple modification to calculate the C stock from a single sampling of a fixed-depth surface layer (0–20 cm). Briefly, when the soil BD decreased (e.g., in 1998), the depth of surface soil increased (depth >20 cm) relative to the initial value (i.e., 20 cm in 1990), and this added depth we define as the expanded layer. We assumed that SOC content for the expanded layer (in 1998, 2006, and 2014) was the same as the SOC content of surface layer (0–20 cm) measured at the previous measurement year (1990, 1998, and 2006 respectively). Soil mass (M) and C stock (CS) values were calculated as follows: Mi = BDi 0.20 104
(2)
Mi,e = M0,equiv Mi
(3) 1
where Mi is dry soil mass (Mg ha ) of the ith year, BD is bulk density (Mg m3) of the ith year, 0.20 is the fixed depth of profile layer (m), and 104 is a unit conversion factor (m2 ha1). Mi,e is expanded layer soil mass and M0,equiv is the initial dry soil mass in 1990. The fixed depth (FD) and ESM of C stock is calculated as: Ci,
fixed = conci Mi
Ci,equiv = Ci,
(4)
fixed + conclast Mi,e
(5)
where Ci, fixed is the C stock to a fixed depth (t C ha1) and conci is the SOC content (kg C Mg1). Ci, equiv is the equivalent C mass (t C ha1), and conclast is the SOC content in the last measured year. Specifically, conclast is the SOC content of 1990 when C1998, equiv is calculated, SOC content of 1998 for the C2006, equiv calculation, and SOC content of 2006 for the C2014, equiv calculation. 2.4.4. Rate of C stock change The rate of change in C stock was calculated as the change in C stock under a given treatment between the measured years,
1.5
1.2
-3
2.4. Calculations
C inputs, respectively. The rate of decrease in BD was calculated similarly, using the same model but where b was the rate of decrease in BD with time.
Soil bulk density (g cm )
weighed, and subsamples of the sun-dried rice grains were heated in an oven at 70 C before calculating the mass water content; the water content was constantly 14% by weight. The green manure was harvested from a 3 m2 area for determination of fresh biomass in the middle of April, and subsamples were dried in an oven at 70 C to calculate water content, as above. Initial soil samples were taken in 1990 before the spring plow (early April). Thereafter, soil samples from the surface layer (0– 20 cm) were collected once every two years until 2014, always in early April. Each sample was a composite of nine or twelve random subsamples within each plot, collected with a stainless steel tube (diameter 2–3 cm, length 80–100 cm). Root detritus was removed and the soil was air dried to constant weight and ground to pass a 2 mm sieve prior to physical analysis. A portion of soil was further ground to pass a 0.15 mm sieve for chemical analysis. In 2014, plant samples (rice straw, rice grain, and green manure) were collected for N, P, and K content analyses. To ensure the minimum amount of visible organic residue for all soil samples, we removed visible pieces of organic material during soil sample preparation: root detritus was removed during soil collection before the spring plow; visible pieces of organic material were removed from air dried samples when they were ground to pass a 2 mm sieve; and any remaining visible pieces of organic material were carefully removed from the portion of soil before it was further ground to pass a 0.15 mm sieves for SOC measurements. Soil BD was measured in six random replicates once every four years in early April from 1990 to 2014 using a soil core of 100 cm3. Organic C content of soil and plant residues was determined by the wet digestion method with potassium dichromate (Nelson and Sommer, 1975). N, P, and K contents of the plant material were determined after digestion with H2SO4 and H2O2 by colorimetric analysis using an automated spectrophotometric flow injection analyzer, the molybdate colorimetric method, flame atomic absorption spectrometry, respectively (Institute of Soil Sciences, Chinese Academy of Sciences, 1978).
0.9
0.6
CK OM NPK NPKOM
0.3
Decrease rate = -0.0133, p < 0.01 Decrease rate = -0.0146, p < 0.01 Decrease rate = -0.0123, p < 0.01 Decrease rate = -0.0151, p < 0.01
0.0 1990
1995
2000
2005
2010
2015
Year Fig. 1. Temporal variation of soil bulk density (BD) from 1990 to 2014. Results are averages (n = 3) SE. The decrease in the rate of BD was calculated according to the model Y = a + bt, where Y is BD (t m3), t is the duration of the experiment (years), a is initial BD (t = 0), and b is the decrease in the rate of BD with time.
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305
divided by the duration in years. Rate of C stock change was calculated as follows:
3. Results
DCrate = DCsto/(i2–i1)
3.1. Dynamics of rice yields and green manure
(6)
where DCrate is the rate of C stock change (t C ha1 yr1) and i is the date of measurement (years). DCsto is the change in C stock from i1 to i2.
Rice yields had similar fluctuations in all treatments during the study period of 1990–2014 (Fig. 2a, b, c) and followed three general trends: the early stage, 1990–1998, representing a stable or slightly decreasing trend in annual rice yields; the middle stage, 1999– 2006, representing a significant increasing trend (p < 0.05 or p < 0.01); and the late stage, 2007–2014, representing a significant decreasing trend (p < 0.05 or p < 0.01 for the OM, NPK, and NPKOM treatments, Table 1). The average yields of first, second, and total annual rice harvests from 1990 to 2014 are listed in Table 1. For the annual rice yields, NPKOM treatment resulted in a significantly larger harvest than did NPK or OM treatment, and there were significantly larger yields under NPK than under OM. For CK and NPK, the annual rice yield tended to increase with time, and for NPKOM, this increase was significant (p < 0.01, Table 1). For the OM treatment, the annual rate of change in rice yield was 10 kg ha1 yr1 (Table 1). The first rice yield fluctuated dramatically between years, and the coefficients of variation of first rice yields among years were higher than those of second rice yields by an average of 14.9%. The declining trend in annual rice yields in the late stage was mainly caused by the decrease in first rice yields, which accounted for 65.9–91.5% of the fluctuation in annual yield decrease. The rest of the fluctuation was accounted for by second rice yields, with a significant rate of change for NPK and NPKOM (p < 0.05, Table 1). The average biomass of green manure was significantly higher with NPKOM than that with OM treatments (p < 0.05) over the entire experiment. The trend of green manure biomass over time also showed fluctuation, from an increasing trend in the early stage
2.4.5. C stabilization efficiency C stabilization efficiency was calculated as the change in SOC stock under a given treatment between measured years, divided by the quantity of C input in the duration between measurement years. The formula is as follows: Ceffic (%) = 100 DCsto/Cinp
(7)
where Cinp is the total C input from year i1 to year i2, Ceffic is the stabilization efficiency (C stock increase per unit C input added) of added C, and DCsto is the change in C stock from i1 to i2. 2.5. Statistical analysis One-way analyses of variance (ANOVA) were applied using SAS 6.1 (SAS institute Inc., Cary, USA). The difference between mean values was evaluated at the 95% confidence interval using the Duncan method (considered significant at p < 0.05). Graphical material was prepared using Origin 7.5 (Originlab, Northampton, USA). The significance of the effect of time on changes (slopes) in rice yields, biomass of green manure, C inputs, and SOC was determined at the p < 0.05 probability level according to the Student’s t-test. The relationships between yield and climatic parameters were evaluated using correlation analysis.
a
10000
-1
Second-rice yields (kg ha )
-1
First-rice yields (kg ha )
10000 8000 6000 4000 2000
-1
1995
2000
2005
2010
6000 4000 2000
1990
2015
Biomass of green manure (kg ha )
1990
Annual rice yields (kg ha )
8000
0
0
c
-1
16000
b
14000 12000 10000 8000 6000
10000
1995
2000
2005
d
2010
2015
CK OM NPK NPKOM
8000 6000 4000 2000 0
4000 1990
1995
2000
2005
Year
2010
2015
1990
1995
2000
2005
2010
2015
Year
Fig. 2. Temporal dynamics of rice yields and biomass of green manure: (a) first rice yields, (b) second rice yields, (c) annual rice yields from 1990 to 2014, and (d) biomass of green manure (Astragalus sinicus) from 1992 to 2014. CK: control (no fertilizers); OM: organic matter left in the field after harvest and chopped; NPK: N, P, and K fertilizers; NPKOM: N, P, and K fertilizers and organic matter left in the field after harvest and chopped.
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Table 1 Average rice yields (SE) from 1990 to 2014. CK: control (no fertilizers); OM: organic matter left in the field after harvest and chopped; NPK: N, P, and K fertilizers; NPKOM: N, P, and K fertilizers and organic matter left in the field after harvest and chopped. Early stage: 1990–1998; middle stage: 1999–2006; late stage: 2007–2014; whole study period: 1990–2014. Average yield (kg ha1)
Yield change (kg ha1 yr1)
Season
Tre.
Early stage
Middle stage
Late stage
Whole study period
Early stage
Middle stage
Late stage
Whole study period
First rice
CK OM NPK NPKOM
2386 175h 4370 225ef 4187 195f 4999 282bcd
2559 175h 4636 236de 4903 278 cd 5326 360b
2533 279h 3680 569g 5183 503bc 6233 556a
2488 119D 4235 219C 4735 207B 5498 249A
19 91 58 86
142 206* 306** 339*
252* 504* 502** 471*
4 41 51 65
Second rice
CK OM NPK NPKOM
2969 244h 4102 297f 4577 429e 4782 458de
3909 72fg 5155 94 cd 5373 236bc 5850 318ab
3748 240g 4785 274de 5373 306bc 5850 281a
3520 142C 4658 163B 5108 207A 5438 228A
95 64 184 83
10 9 60 16
23 170 254* 244*
38* 30 29 47
Annual rice
CK OM NPK NPKOM
5355 257g 8473 278e 8764 416e 9781 436d
6469 154f 9792 227d 10343 403 cd 11089 408b
6281 389f 8465 766e 10556 769bc 12083 709a
6008 186D 8892 291C 9843 345B 10936 351A
114 27 126 3
152** 215* 366* 355*
275 674* 757** 715**
43 10 80 113*
Green manure
OM NPKOM
3484 389b 4198 311a
2507 454c 4093 747a
1752 424d 2960 573c
2542 278B 3731 247A
268 147
325 445
383* 477*
121** 107*
Note: Different lowercase letters indicate a significant difference at p < 0.05 in the same growth period among the three stages. Different capital letters in the same column indicate a significant difference at p < 0.05. Rates of yield were calculated according to the model: Y = a + bt, where b is the slope of annual rates of rice yield change or biomass of green manure. * and ** indicate a level of significance at p < 0.05 and p < 0.01, respectively.
to a decreasing trend in the middle and late stages (Fig. 2d); the rate of decrease of green manure biomass was significant in the late stage (p < 0.05). In general, the green manure biomass in OM and NPKOM treatments decreased significantly with time (Table 1). 3.2. Plant-derived C inputs For CK and NPK treatments, the annual C inputs to fields derived primarily from rice roots (i.e., rhizodeposition) and stubble. For OM and NPKOM treatments C inputs included straw and green manure in addition to rhizodeposition. Annual C inputs in CK and NPK treatments ranged from 765 to 2362 kg ha1 yr1, which was much lower than that in OM and NPKOM treatment, which had 3771 to 9988 kg ha1 yr1 (Fig. 3). For the latter treatments, rice provided 78.3–81.4% of the total C inputs, while the remaining 18.6–21.7% was derived from green manure (data not shown). Thus, the dynamics of C inputs were similar to the dynamics of rice yields, with a significant correlation (p < 0.01) for OM and NPKOM treatments. Generally, over the whole experiment, the annual C inputs tended to increase in the CK, NPK, and NPKOM treatments, and to
CK OM NPK NPKOM
-1
Amount of C inputs (kg ha )
12000
9000
6000
3000
1990
1995
2000
2005
2010
2015
Year Fig. 3. Temporal variation of C inputs from 1990 to 2014. CK: control (no fertilizers); OM: organic matter left in the field after harvest and chopped; NPK: N, P, and K fertilizers; NPKOM: N, P, and K fertilizers and organic matter left in the field after harvest and chopped.
decrease in the OM treatment, but the rates of change were not significant (p > 0.05) for any treatment (Fig. 3). The rate of change in C inputs in the early and middle stages were not significant (p > 0.05), except for OM treatment in the early stage and for CK and NPK treatments in the middle stage. In the late stage, C inputs for all treatments decreased, and the rates of decrease for OM, NPK, and NPKOM were significant (p < 0.01), ranging from 133.1 to 578.3 kg ha1 yr1. There were no significant differences for average C inputs between the late and middle stages for NPK and NPKOM treatments (p > 0.05, data not shown). The average C inputs in the middle stage were significantly higher than those in the early stage for OM, NPK, and NPKOM. In general, the changes in C inputs in the OM and NPKOM treatments were faster than those in the CK and NPK treatments (Fig. 3). 3.3. Soil organic carbon contents After 25 years of the double rice cropping system, the SOC content in the surface layer significantly increased from an initial 13.3–15.6 g kg1 in 1990 to 16.2–22.5 g kg1 in 2014 (Fig. 4). NPK fertilizer increased the SOC content by 14.0%, and application of organic matter, alone and combined with NPK fertilizer, enhanced the SOC content by 28.2% and 39.0%, respectively, compared with CK. For all treatments, the largest SOC content appeared in 2006– 2008, then decreased over time. The SOC losses from 2006 to 2014 were less for CK and NPK treatments (0.3% and 0.6%, respectively) than for the OM treatment (10.4%) and the NPKOM treatment (11.8%). For all treatments, there were significant correlations between carbon inputs in the three stages and SOC stock (i.e., 1998, 2006, and 2014; Table 2), thus indicating that the average C inputs best explained the SOC. The trend in SOC accumulation from 1990 to 2014 was significant (p < 0.01) for all treatments, and ranged from 0.19 to 0.46 g kg1 yr1 (not shown). Of the individual stages of the experiment, a significant trend was observed for the middle stage only. During the late stage, SOC decreased at a rate of 0.080– 0.429 g kg1 yr1, though this was not significant (p > 0.05). Generally, the magnitudes of changes in rates of SOC accumulation were larger for OM and NPKOM treatments than for CK or NPK
A. Chen et al. / Agriculture, Ecosystems and Environment 232 (2016) 302–311
-1
SOC content (g kg )
treatments. Therefore, the trend of SOC over time was significantly positively correlated to the rate of change in C inputs (Table 2).
CK OM NPK NPKOM
25
3.4. Soil organic carbon stocks
20 15 10 5 0 1990
1995
307
2000
2005
2010
2015
Year Fig. 4. Temporal variation of SOC contents from 1990 to 2014. CK: control (no fertilizers); OM: organic matter left in the field after harvest and chopped; NPK: N, P, and K fertilizers; NPKOM: N, P, and K fertilizers and organic matter left in the field after harvest and chopped.
We used the ESM method (Lee et al., 2009) to calculate SOC stocks based on BD (formulas 2–5). In all treatments, long-term rice cropping resulted in an increase of C stocks in the surface soil. As compared with the initial value, in 2014 SOC stocks were 19.0% and 24.6% larger for CK and NPK treatments, respectively, and 39.6% and 45.0% for OM and NPKOM treatments, respectively (calculated from Fig. 5a). SOC stocks varied across the three stages (Fig. 5a). The largest SOC stocks were found in 2006–2008 then stocks decreased, reflecting the decreasing SOC contents. SOC stocks in 2014 were smaller than those in 2006 for CK and NPK treatments, but decreased more strongly, by 8.7% and 10.1% for OM and NPKOM treatments respectively (significant for NPKOM treatments, p < 0.05, Fig. 5a). There were no significant differences for rates of SOC stock change between the early and middle stages, whereas in the late stage the rates of SOC stock change significantly decreased
Table 2 Correlation coefficients between C inputs, rice yields, SOC contents, SOC stocks, rate of rice yield change, C input change, SOC change, and SOC stocks change over the three stages of the experiment. Item
C inputs
SOC contents
C stocks
Rate of rice yields change
Rate of C inputs change
Rate of SOC content change
Rate of SOC stocks change
Rice Yields C inputs SOC contents C stocks Rate of rice yields change Rate of C inputs change Rate of SOC content change
0.658*
0.749** 0.869**
0.641* 0.844** 0.986**
0.098 0.026 0.086 0.108
0.351 0.242 0.33 0.311 0.709**
0.086 0.236 0.245 0.238 0.882** 0.772**
0.048 0.189 0.144 0.128 0.856** 0.833** 0.988**
Note: * and ** indicate significance at p < 0.05 and p < 0.01, respectively.
1998 2006 2014
a
60
a
ab
2
b
1
ab abc
b
a
e
de
c
-1
de
e
-1
SOC stock (t ha )
40
20
0 CK
-1
cd cd
c
Change rate of SOC stock (t ha yr )
bc
C
NPK
Treatment
NPKC
abc
bcd cd
bc cd
0
-1
de def ef
CK C NPK NPKC
f
-2 1990-1998
1999-2006
2007-2014
Year
Fig. 5. SOC stocks in 1998, 2006, and 2014 (a), and rates of SOC stock change for the early stage: 1990–1998, middle stage: 1999–2006, and late stage: 2007–2014 (b). In Fig. 5b, SOC stocks in 1998 and 2006 were used instead of in 1999 and 2007 (data for SOC and BD were not collected in 1999 and 2007). Different lowercase letters indicate significant differences at p < 0.05 among the three stages. The initial SOC stock in 1990 was 34.5 t ha1.
A. Chen et al. / Agriculture, Ecosystems and Environment 232 (2016) 302–311
for the OM, NPK, and NPKOM treatments (p < 0.05) and had negative values for OM and NPKOM (Fig. 5b). In general, SOC stocks and rates of SOC stock change were strongly affected by C inputs, for which the rice yield was a powerful proxy (Table 2). 4. Discussion 4.1. Response of SOC to the changes in C inputs Incorporation of plant residues and green manure to paddy soils was effective in improving SOC accumulation. Therefore, SOC accumulation in the NPKOM treatment was higher than that in the other three treatments because this treatment had the highest quantity of C inputs (rice residue, rice straw, and green manure). Generally, SOC accumulations and C inputs were closely related (Table 2). This echoes the results obtained by many studies showing that C input is one of the major factors controlling the C stocks (Manna et al., 2005; Huang and Sun, 2006; Li et al., 2010; Rui and Zhang, 2010). However, other reports have shown that there were significant increases in SOC in the first 30–40 years of rice cropping, followed by a lower accumulation rate or a relatively stable level (Zhang and He, 2004; Li et al., 2005). This emphasizes the ability of paddy soils to respond quickly to increasing C input rates. Through the dependency of crop residue production and rice yield, SOC contents and SOC stocks fluctuated with the variation in rice yields (Figs. 2, 3, and 4). The rates of SOC change were closely related to the rates of C input changes in all three stages of the experiment (Table 2). In the studied double-cropping system, the C inputs consisted of rice residues, which accounted for 78.3–81.4% of the total C inputs under OM and NPKOM treatments, and nearly 100% (C input via autotrophic microorganisms, e.g., Wu et al., 2015, were not accounted for) for CK and NPK treatments. Therefore, the fluctuations in rice yields directly affected the SOC dynamics. Previous reports showed that the SOC increase on a regional scale was consistent with the prolonged increase (since the 1950s) in rice productivity (Wu, 2011) and the quantity of organic C inputs enhanced the SOC accumulation rate in subtropical regions (Li et al., 2010). A decline or stagnation in yields has also been observed in other long-term experiments in Asia (Yadav et al., 2000; Bhandari et al., 2002; Ladha et al., 2003; Peng et al., 2004). However, a few studies (Yadav et al., 2000; Ladha et al., 2003) have reported an SOC decline or stagnation with decreasing crop yields. Those studies examined constant C inputs, which do not reflect the fluctuation of C inputs with crop residues and thus the effects of these fluctuation on SOC. The response of SOC to the decline in C inputs was also affected by the level of accumulated SOC. The larger SOC accumulations at the commencement of the late stage (in 2006) in OM and NPKOM decreased significantly more strongly than those of CK and NPK with the decline in C inputs (Fig. 4). This indicates that paddy soils with a high initial SOC responded particularly sensitively to the declines in C inputs. Similar results were found in a long-term experiment in a rice-wheat system (Yadav et al., 2000), where SOC decreased over time with declining yields at locations where the SOC content was greater than 6.5 g kg1 at the start of the longterm experiment, but increased at locations with initially low (<5.0 g kg1) SOC content. Therefore, the response of SOC to decreasing C inputs was more sensitive for high levels of SOC than for lower levels. The sensitivity of high levels of SOC to declining C inputs might be related to a steady state equilibrium of SOC contents (Yadav, 1998; Yadav et al., 2000; Stewart et al., 2008). Yadav et al. (2000) found that SOC decreased with decline in yields in an experiment where the initial SOC content was greater than a threshold SOC level of 6.0–6.5 g kg1 (Yadav, 1998). In the present study, the SOC
C stabilization efficiency (%)
308
40
y = 434.1 exp(-0.1524x) -18.2 2 R = 0.658, P < 0.01
20
0
-20 12
15
18
21
24
27
-1
SOC (g kg ) Fig. 6. C stabilization efficiency versus SOC content in the initial year of the three stages (i.e., 1990, 1998, and 2006). The C stabilization efficiency (Ceffic, C stock increase per unit C input added) was calculated according to the model Ceffic (%) = 100 DCsto/Cinp, where Cinp is the total C input from year i1 to year i2, and DCsto is the change in C stock from i1 to i2.
showed a slower rate of increase between 2004 and 2008 (Fig. 4), and lower C stabilization efficiency at larger SOC levels (Fig. 6). These indicate that SOC may have reached a relatively stable level during this period for OM and NPKOM treatments at about 25 g kg1, if there was a high C return to soil. Therefore, a decrease in C inputs to the soil with a high SOC level leads to a decrease in the C stocks until a new and lower steady state equilibrium is reached. Whether a certain C input will increase the SOC stock or not depends on how far a soil is from its saturation level (Stewart et al., 2008); keeping SOC at the saturation level needs sufficiently large C inputs. Stewart et al. (2008) reported that soils with greater OC content should have a decreased SOC stabilization efficiency. In contrast, soils with smaller C contents may store the added C with greater efficiency. Similar studies showed that SOC decomposition rates were positively correlated with OM inputs or SOC content (Cai and Qin, 2006; Li et al., 2010). This suggests that the higher decomposition rate of SOC and lower SOC stabilization efficiency of added C inputs could explain the sensitivity of high levels of SOC to declining C inputs. In contrast, for lower SOC levels, e.g., CK and NPK in the early and late stage, declining C inputs did not cause a significant decline in SOC accumulation (Figs. 3, 4, and 5 a). This could be due to a lower decomposition rate of SOC and higher stabilization efficiency of the organic residues in soil with lower SOC levels. The decline in C stabilization efficiency also indicates that the C inputs in the late stage were not enough to maintain the relatively stable level of SOC for the OM and NPKOM treatments (Fig. 6). Additionally, the high sensitivity of SOC to fluctuation in rice yields was partly explained by the interaction between yields and SOC contents. Increased SOC contents lead to a positive feedback on plant growth and thus increase the C input of the crop (Brock et al., 2011). In contrast, the yield-driven decline of SOC might lead to a negative feedback on plant growth. Therefore, the high rate of C accumulation or loss for OM and NPKOM treatments could be due to the more pronounced interaction between SOC and rice yields than for the CK and NPK treatments. In the late stage, the interactions result in the observed differences responses of SOC to decreasing yield between the OM and NPKOM treatments on the one hand and the CK and NPK treatments on the other (Fig. 3). 4.2. Why do yields decline? Variations in SOC stocks are the result of the imbalance between C inputs and outputs. In the present study, C inputs
A. Chen et al. / Agriculture, Ecosystems and Environment 232 (2016) 302–311
showed a decreasing trend in the late stage, which is closely related to the decline of yield and crop residue production of the paddy ecosystem. The declining trends in annual rice yields were mainly caused by the decline in the first rice yields, which explained 42.3– 91.5% of the fluctuation in the annual decrease of the C input (Figs. 2 and 3). Fluctuation in the first rice, second rice, and total annual rice yields was similar for all treatments, and the relationships between yields among all treatments were significant (p < 0.01). This indicates that there were common factors that affected the rice yields. For this region, Yang et al. (2015) reported low temperature and insufficient sunshine duration to be the limiting factors for first rice yields. In fact, daily maximum and mean temperatures as well as sunshine duration were significantly correlated with first rice yields in all treatments from 1990 to 2014 (p < 0.05 or 0.01, Table 3). In the late stage, the first rice yields decreased significantly, concurrent with a decrease of maximum temperature by 0.35 C yr1, mean temperature by 0.17 C yr1, and sunshine duration by 0.23 h yr1 during this period (Table 3). There was a significant relationship between the rate of first rice yield change and these three climatic factors (p < 0.01, Fig. 7), indicating the pronounced effect of climatic factors on plant growth and yield decline of the first rice crop. The effects of climate change on rice yields have been reported in field experiments using optimal management at the International Rice Research Institute, Los Baños, Philippines from 1992 to 2003. In contrast to our study, Peng et al. (2004) found that an increasing annual mean minimum temperature caused rice yields in the tropical region to decline. The authors conjectured that a greater rate of maintenance respiration with increasing minimum temperature may reduce the quantity of assimilates available for growth and yield. Other mechanisms, such as differential effects of night versus day temperature on the above factors, also may contribute to the observed yield reduction. Peng et al. (2004) reported a tight negative linear relationship between spikelets per m2 and minimum temperature (p < 0.05). In our subtropical region, in contrast to the tropical region, there was a significant negative climate effect on yields of early rice with the decline in temperature (maximum temperature and mean temperature) and sunshine duration. Table 3 shows that the increase in rain, reduced solar radiation, and temperature in the late stage, was different from the early stage (increase in rain did not decline with temperature and sunshine duration). We hypothesized that the decline in sunshine duration and temperature in the late stage weakened the photosynthesis of rice leaves,
309
which caused the quantity of assimilates available for growth and yield to decline. Likewise, the biomass of green manure was affected by climatic factors. The reduction of green manure biomass in the late stage, at rates of 383–477 kg ha1 yr1, was due to a decrease in the daily maximum, minimum, and average temperatures at the rate of 0.32 C yr1, 0.19 C yr1, and 0.26 C yr1, respectively, during the key growth stages of green manure (February and March) (data not shown). In the second rice season, rice yields were not related to climatic factors (p > 0.05, Table 3). Occasional cold-air outbreaks at the end of the second rice season may have weakened the relationship between yields and climatic factors. Inadequate nutrient supply may be another major cause of yield decline. Stagnation or decline in yields has been observed in many rice-based cropping systems in Asia. Yield decline has been due to changes in both quality and quantity of SOC and its impact on nutrient supply; current fertilizer management practice may not be adequate to sustain yields in long-term crop cultivation (Dawe et al., 2000; Bhandari et al., 2002; Ladha et al., 2003). The P contents of rice grain, straw, and green manure in the OM and CK treatments were significantly lower than those in the NPKOM and NPK treatments (Table 4). This suggests P as the possible limiting nutrient for rice yields and biomass production by green manure. Additionally, the N content of both rice straw and rice grain in the NPK treatment was obviously lower than in other treatments; K content of rice straw was significantly lower in the NPK treatment than in the NPKOM treatment (Table 4). This finding indicates that the decline of first rice yields with NPK treatment may be partly due to insufficient supplies of N and K. Regmi et al. (2002) also cited depletion of soil K and inadequate K fertilization as possible causes for a declining yield of rice crops in the first rotation. The mean N application rates for rice were 226 kg N ha1 in 2004 in China (Ma et al., 2009), which was higher than in the present study by 24% (182.3 kg N ha1 for double rice). This means that the recommended fertilizer may not be adequate to maintain N and K at sufficient levels for rice farming. The differences in first rice yields among treatments gradually increased from the early and middle stages to the late stage, e.g., for OM and NPKOM treatments (Fig. 2 and Table 1). This suggests that the differences in responses to limiting factors increased with the duration of the experiment. It could be due to the increasing difference in C inputs (Fig. 3), which affects nutrient input and soil nutrient availability; the faster decline of organic matter inputs then enhances the negative feedback on plant growth and biomass.
Table 3 Correlation coefficients between rice yields, green manure, and sunshine duration (SD), maximum temperature (Max-T), minimum temperature (Min-T), mean temperature (MT), and rain. Climate factor
SD Max-T Min-T MT Rain
Rate of climate factors change during first rice season Correlation between first rice yields Correlation between second rice Correlation and climate factors in whole study yields and climate factors in whole between GM and period study period climate factors in whole study period CK
OM
NPK
NPKOM
CK
OM
NPK
NPKOM OM
0.471* 0.534** 0.163 0.555** 0.143
0.402* 0.482* 0.437* 0.596** 0.075
0.331 0.611** 0.104 0.574** 0.366
0.492* 0.629** 0.053 0.713** 0.427*
0.061 0.117 0.226 0.074 0.042
0.015 0.169 0.195 0.126 0.07
0.089 0.361 0.343 0.113 0.228
0.000 0.389 0.392 0.198 0.249
0.038 0.065 0.347 0.226 0.054
NPKOM Early stage
Middle stage
Late stage
Whole study period
0.063 0.414* 0.554** 0.481* 0.085
0.077 0.273 0.065 0.095 0.479
0.234 0.353 0.076 0.165 0.260
0.013 0.040 0.043 0.005 0.268
0.025 0.340 0.066 0.035 0.508
Note: CK: control (no fertilizers); OM: organic matter left in the field after harvest and chopped; NPK: N, P, and K fertilizers; NPKOM: N, P, and K fertilizers and organic matter left in the field after harvest and chopped. Early stage: 1990–1998; middle stage: 1999–2006; late stage: 2007–2014; whole study period: 1990–2014. * and ** indicate significance at p < 0.05 and p < 0.01, respectively. GM: green manure (Astragalus sinicus). For green manure, the climate factors are data for the key growing season from February to March. The rate of climate factor change was calculated according to the model: Y = a + bt, where b is the rate of climate factor change. Unit of rate of climate factors change: h yr1for SD, C yr1 for temperature, mm yr1 for rain.
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Fig. 7. Rate of first rice yield change versus rate of change in mean temperature, sunshine duration, and maximum temperature of each of the three stages in the first rice period.
Table 4 Nutrient N, P, and K contents (average SE) of rice straw, grain, and green manure in 2014. Class
Tre.
Content of nutrient 1
N (g kg
)
Content of nutrient 1
P (g kg
)
1
K (g kg
)
First rice Rice straw
Rice grain
Green manure
N (g kg1)
P (g kg1)
K (g kg1)
0.3 0.0b 0.3 0.0b 1.0 0.2a 1.2 0.1a 2.2 0.0b 2.1 0.0b 3.2 0.2a 3.1 0.0a
22.5 1.3c 27.8 2.5b 25.5 1.1bc 33.8 0.3a 2.2 0.1b 2.3 0.1b 3.0 0.1a 3.1 0.1a
Second rice
CK OM NPK NPKOM CK OM NPK NPKOM
7.1 0.5a 6.9 0.5a 5.0 0.5b 5.8 0.5ab 13.0 1.0ab 14.5 0.7a 11.8 0.9b 14.1 0.5ab
0.9 0.1c 0.8 0.1c 1.4 0.2a 1.2 0.1b 2.5 0.1b 2.4 0.1b 3.3 0.0a 3.3 0.1a
28.1 2.9c 35.2 0.3ab 34.3 2.3b 40.8 0.8a 2.1 0.0b 2.1 0.1b 2.7 0.0a 2.8 0.1a
OM NPKOM
24.4 1.2a 27.3 1.3a
1.3 0.1b 2.2 0.2a
2.8 0.2a 2.6 0.5a
3.9 0.4c 4.3 0.4bc 5.9 0.5b 8.2 0.4a 11.6 0.6a 10.9 0.7a 10.5 0.9a 12.0 0.2a
Note: CK: control (no fertilizers); OM: organic matter left in the field after harvest and chopped; NPK: N, P, and K fertilizers; NPKOM: N, P, and K fertilizers and organic matter left in the field after harvest and chopped. Different lowercase letters represent significant differences among treatments at p < 0.05.
Hence, we can conclude that the interaction between yields and nutrient inputs could further affect the decline in rice yields. Even though we could not delineate the driving factors of the yield decrease in the last decade, it appears that an interrelationship between insufficient P or N and K supply and changes in the climatic parameters are possible reasons for the decline of rice yields and green manure in the late stage and, hence, SOC contents and stocks. 4.3. Possible consequences of reduction in C inputs On the regional scale, the sequestration of OC by paddy soils in subtropical China has usually been attributed to the increased use of chemical fertilizers. Fertilizers have provided an increased organic matter input through the stimulation of biomass production and rice yield over the last several decades (Huang and Sun, 2006; Sun et al., 2009; Wu, 2011). Many long-term experiments have found a sustained increase of OC in paddy soil with fixed amounts of organic matter application, alone or combined with fertilizer, over recent decades (Pan et al., 2003). Those data suggest that the SOC accumulation was due to the larger C inputs. Therefore, the first management method to increase SOC stock should be to increase C inputs. In contrast to previous studies, we demonstrated that recent C inputs face a high risk of reduction, especially in subtropical regions.
The major risk stems from the stagnation or decline in biomass production and rice yields since the end of the last century (Grassini et al., 2013; Xiong et al., 2014). The yields now face the challenge of global warming or extreme climate events. Reports showed that rice yields in China had increased from 4324 kg ha1 in 1981 to 6553 kg ha1 in 2010 with an evidently slowing growth rate since the end of the 20th century, which was not compensated for by relative benefits from improved varieties and management (Xiong et al., 2014). Paddy soil OC accumulation also faces new challenges of changes in crop rotation (from a double rice cropping system to a single rice cropping system), soil fertility decline, and even conversion from paddy fields to upland (Wang et al., 2014). High-quality paddy land is increasingly replaced by marginal and low-quality alternatives due to the Chinese policy of “keeping quantity balance” within an administrative territory. These changes not only decrease rice production and C inputs to the paddy fields over time, but also change the flooding condition of paddy fields, which probably increase the decomposition of soil organic carbon. 4.4. Conclusions Decreases in rice yields and SOC content were noted during the late stage of a long-term experiment. These trends were more pronounced for the OM and NPKOM treatments than for their CK
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and NPK counterparts. The declining trends in annual rice yields were mainly caused by declining first rice yields. The insufficient P or N and K supply and adverse changes in climatic factors are possible reasons for the yield declines. Decline of C inputs with crop residues and green manure quickly affected the SOC stock in paddy soils. Intensively managed paddy soils with high SOC levels responded more sensitively to reductions of C inputs than those with lower levels. Hence, the reversion from C sink to C source is likely to occur in SOC-enriched paddy fields after continued reduction of C inputs. Therefore, the protection of existing high-quality paddy fields is very important for maintenance of SOC stocks. Decreasing ricederived C inputs should be compensated for with additional inputs of similar quality. Non-natural factors that cause the reduction of C inputs, such as land use change and change from a double-to a single-rice cropping system, should be avoided though policy regulations in high-quality rice cultivation regions. Acknowledgements We thank Prof. Ron McLaren of Lincoln University for providing input on an earlier draft of this manuscript. This study was jointly supported by the National Natural Science Foundation of China (31200339), the Special Fund for Agro-scientific Research in the Public Interest of China (201203030), the Open Foundation of Key Laboratory of Agro-ecological Processes in Subtropical Region, Institute of Subtropical Agriculture, Chinese Academy of Sciences (ISA2015101), the Recruitment Program of High-end Foreign Experts of the State Administration of Foreign Experts Affairs awarded to Prof. Georg Guggenberger (GDT20154300073), and Public Service Technology Center, Institute of Subtropical Agriculture, Chinese Academy of Sciences. References Bhandari, A.L., Ladha, J.K., Pathak, H., Padre, A.T., Dawe, D., Gupta, P.K., 2002. Yield and soil nutrient changes in a long-term rice-wheat rotation in India. Soil Sci. Soc. Am. J. 66, 162–170. Brock, C., Fließbach, A., Oberholzer, H.R., Schulz, F., Wiesinger, K., Reiniche, F., Koch, W., Pallutt, B., Dittman, B., Zimmer, J., Hülsbergen, K.J., 2011. Relation between soil organic matter and yield levels of nonlegume crops in organic and conventional farming systems. J. Plant Nutr. Soil Sci. 174, 568–575. Cai, Z.C., Qin, S.W., 2006. Dynamics of crop yields and soil organic carbon in a longterm fertilization experiment in the Huang-Huai-Hai Plain of China. Geoderma 136, 708–715. Dawe, D., Dobermann, A., Moya, P., Abdulrachman, S., Singh, B., Lal, P., Li, S.Y., Lin, B., Panaullah, G., Sariam, O., Singh, Y., Swarup, A., Tan, P.S., Zhen, Q.-X., 2000. How widespread are yield declines in long-term experiments in Asia? Field Crops Res. 66, 175–193. Evans, L.T., Fischer, R.A., 1999. Yield potential: its definition, measurement, and significance. Crop Sci. 39, 1544–1551. FAOSTAT, 2015. Available at http://faostat3.fao.org/compare/E. Fauna, 2010. Available at http://chinasmack.com/2010/pictures/battling-floodsdroughts-2010-chinese-news-photos.html. Grassini, P., Eskridge, K.M., Cassman, K.G., 2013. Distinguishing between yield advances and yield plateaus in historical crop production trends. Nat. Commun. 4, 2918. Huang, Y., Sun, W.J., 2006. Changes in topsoil organic carbon of croplands in mainland China over the last two decades. Chin. Sci. Bull. 51, 1785–1803. Institute of Soil Sciences, Chinese Academy of Sciences, 1978. Soil Physical and Chemical Analysis. Shanghai Science and Technology Press, Shanghai (in Chinese). Lal, R., 2004. Offsetting China’s CO2 emissions by soil carbon sequestration. Clim. Change 65, 263–275.
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