Science of the Total Environment 532 (2015) 635–644
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Science of the Total Environment journal homepage: www.elsevier.com/locate/scitotenv
Long-term combined chemical and manure fertilizations increase soil organic carbon and total nitrogen in aggregate fractions at three typical cropland soils in China Y.T. He a, W.J. Zhang a, M.G. Xu a,⁎, X.G. Tong b, F.X. Sun a, J.Z. Wang a, S.M. Huang c, P. Zhu d, X.H. He a,e a Ministry of Agriculture Key Laboratory of Crop Nutrition and Fertilization, Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural Sciences, Beijing 100081, China b College of Resources and Environment, Northwest A & F University, Yangling, Shannxi 712100, China c Institute of Plant Nutrition, Resources and Environment, Henan Academy of Agricultural Sciences, Zhengzhou 450002, China d Centre of Agricultural Environment and Resources, Jilin Academy of Agricultural Sciences, Changchun 130033, China e School of Plant Biology, University of Western Australia, Crawley, WA 6009, Australia
H I G H L I G H T S • • • • •
Assessed the effects of 17 years fertilization on SOC, TN and its fractions. Manure increased all indexes but straw return had no effects on all indexes at GZL. Chemical fertilization had no effects on TN but decreased MBC in GZL and QY. cfPOC was the most sensitive indicator and MOC, MTN was the main sequestrated form. Straw return was site-dependent and manure was the best for improving soil quality.
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Article history: Received 25 January 2015 Received in revised form 26 May 2015 Accepted 2 June 2015 Available online 25 June 2015 Editor: D. Barcelo Keywords: Long-term fertilization Particulate organic carbon Mineral associated organic C Microbial biomass carbon and nitrogen Luvic Phaeozems Calcaric Cambisol Ferralic Cambisols
a b s t r a c t Soil organic carbon (SOC), total nitrogen (TN), microbial biomass carbon (MBC) and nitrogen (MBN) are important factors of soil fertility. However, effects of the combined chemical fertilizer and organic manure or straw on these factors and their relationships are less addressed under long-term fertilizations. This study addressed changes in SOC, TN, MBC and MBN at 0–20 cm soil depth under three 17 years (September 1990–September 2007) long-term fertilization croplands along a heat and water gradient in China. Four soil physical fractions (coarse free and fine free particulate organic C, cfPOC and ffPOC; intra-microaggregate POC, iPOC; and mineral associated organic C, MOC) were examined under five fertilizations: unfertilized control, chemical nitrogen (N), phosphorus (P) and potassium (K) (NPK), NPK plus straw (NPKS, hereafter straw return), and NPK plus manure (NPKM and 1.5NPKM, hereafter manure). Compared with Control, manure significantly increased all tested parameters. SOC and TN in fractions distributed as MOC N iPOC N cfPOC N ffPOC with the highest increase in cfPOC (329.3%) and cfPTN (431.1%), and the lowest in MOC (40.8%) and MTN (45.4%) under manure. SOC significantly positively correlated with MBC, cfPOC, ffPOC, iPOC and MOC (R2 = 0.51–0.84, P b 0.01), while TN with cfPTN, ffPTN, iPTN and MTN (R2 = 0.45–0.79, P b 0.01), but not with MBN, respectively. Principal component analyses explained 86.9–91.2% variance of SOC, TN, MBC, MBN, SOC and TN in each fraction. Our results demonstrated that cfPOC was a sensitive SOC indicator and manure addition was the best fertilization for improving soil fertility while straw return should take into account climate factors in Chinese croplands. © 2015 Elsevier B.V. All rights reserved.
1. Introduction In cropland soil, the preservation or improvement of soil quality and productivity is of major importance. Soil organic carbon (SOC) is closely associated with a wide range of physical, chemical and biological ⁎ Corresponding author. E-mail address: [email protected] (M.G. Xu).
http://dx.doi.org/10.1016/j.scitotenv.2015.06.011 0048-9697/© 2015 Elsevier B.V. All rights reserved.
properties, and thus has been recognized as a key component of soil quality (Reeves, 1997). Fertilizer application has been widely used as a common management practice to increase soil carbon (C) sequestration and SOC level. For instance, to increase soil fertility and obtain a satisfactory yield, manures have been used for nearly 4000 years in China, Japan and Korea (Dormaar et al., 1988). In addition, in cropland soils SOC also represents a potential sink of atmospheric CO2. As a result, understanding the impact of chemical fertilizer and manure application
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on SOC and its fractions could provide valuable information for maintaining or implementing environmentally sustainable management practices for agroecosystems. In general, the readily decomposable labile C is sensitive and responds more quickly to changes in management practices than recalcitrant C and thus is used as an early indicator of SOC changes (Campbell et al., 1997). The microbial biomass plays a critical role in regulating the C and N cycling processes in soils, and microbial biomass carbon (MBC) and nitrogen (MBN) are sensitive indicators for changes resulting from agronomic practices and other perturbations of soil ecosystems though they are only a small part of SOC and total nitrogen (TN). Numerous studies have reported the effects of fertilization on MBC or MBN, but no consistent results have been obtained (Böhme et al., 2005; Zhong and Cai, 2007). For example, organic manure tends to increase MBC by direct C input and/or the change of microbial community composition (Sun et al., 2004), while chemical fertilization have often produced contradictory effects (He et al., 2013; Sarathchandra et al., 2001). This uncertainty is partly attributed to the short-time study and to variations in soil type, climate condition, and crop system under different fertilizations. In addition, the structure composition of the different fertilizers, the changes in soil enzyme activities and abundance and function of the soil microbial community under different fertilizations also contribute to the contradictory effects (Giacometti et al., 2013, 2014). Therefore, it is important to assess the effects of different fertilizations on MBC or MBN in variable soil types at a long-time scale to better understand soil C transformation or accumulation. Meanwhile, SOC fractions are characterized by differential stabilities and turnover rate, thus also been extensively used as sensitive indicators to provide insight into the consequences of management practices that could not be gleaned from studies of total SOC. Six et al. (2002) proposed a physical fractionation procedure and the associated conceptual SOC model that separated the bulk SOC pool into four conceptual aggregate fractions according to different protection mechanisms. These four conceptual fractions are (1) coarse free and (2) fine free particulate organic C (cfPOC and ffPOC, unprotected SOC inter-aggregate), (3) intramicroaggregate particulate organic C (iPOC, physically protected SOC) and (4) mineral associated organic C (MOC, chemically and biochemically protected SOC). This conceptual model could give an opportunity to understand the effect of soil microbial activities during SOC biodegradation under different management practices (Six et al., 2002). In addition, this physical fractionation technique has been employed to separate SOC fractions that stabilize C and thus could have important implications for soil C sequestration at a long-time scale. In a 44 year field experiment, both cattle manure and crop residue treatments increased SOC and most of these increases (up to 72%) were stored in MOC fraction (Courtier-Murias et al., 2013). However, limited information still exists regarding the long-term impacts of different fertilizations on SOC physical fractions, particularly in cropland soils in China. The quality and quantity of SOC have been suggested as major factors affecting soil N dynamics, and one of the major roles of organic
matter in soil fertility is to release N and other nutrients for crop growth (Hart et al., 1994). Changes in N content in soil fractions therefore may be a good indicator of soil fertility and plant N supplying capabilities of a given soil. For instance, studies have reported changes in N contents within different density fractions under different fertilization managements (Compton and Boone, 2002). However, less is known about the responses of TN content in physical fractionations under long-term different fertilizations. Along a water and heat gradient from north to south, black soil (Luvic Phaeozems for FAO classification, Leptic Phaeozems for WRB classification), fluvo-aquic soil (Calcaric Cambisol for FAO classification and Fluvic Cambisol for WRB classification) and red soil (Ferralic Cambisols for FAO and Ferric Acrisols for WRB classification) are main soil types distributing from northwest, central and south of China, where also the important agricultural regions are located. To develop efficient soil fertility management practices, long-term experiment networks have been established since 1990 to examine the effects of continuous applications of chemical fertilizer and the combination of chemical fertilizer and manure on crop yield and soil fertility over these regions. Using soils under five 17 years long-term (September 1990–September 2007) fertilizations (chemical fertilizer with or without organic manure) from three sites (~500 km away from each site), the aims of this study were thus to address the effects of the sole chemical fertilization and the combined fertilization of chemical fertilizer and organic manure on (1) variations of MBC and MBN; (2) variations of SOC and TN accumulations in the whole soil and different physical fraction pools; (3) relationships between MBC or MBN, fraction pools and SOC or TN accumulations. Here, we paid special attention on the distribution and accumulation of SOC and TN in soil physical fractions. The expected results could identify the key fractions and the best fertilizer management practices for SOC accumulations under different fertilizer managements across different cropping systems in China. 2. Materials and methods 2.1. Site description Along a water and heat gradient from north to south of China, three selected long-term field fertilization sites (established since September 1990) are located in Gongzhuling (GZL), Jilin, northeast China; Zhengzhou (ZZ), Henan, central China; and Qiyang (QY), Hunan, southern China. Information on basic, geography, climate and soil chemical properties of these three sites in 1990 is briefly given in Table 1. 2.2. Cropping systems and plant harvest Two years before the establishment of these three long-term fertilization sites, local crops as follows were cultivated without fertilization to reduce soil fertility variability. The cropping system differed in these three sites: a mono-maize cropping (late April to late September)
Table 1 General description of geography and soil properties (0–20 cm in 1990) at the three 17 years (1990–2007) long-term experimental sites in China.
Location Climate Cropping system Precipitation (mm) Mean temperature (°C) FAO soil classification Soil texture Clay content (%) Bulk density (g cm−3) Initial SOC (g kg−1) Total N (g kg−1) pH (soil:water = 1:2.5)
Gongzhuling
Zhengzhou
Qiyang
43°30′, 124°48′ Mild-temperate, semi-humid Single-cropping, maize 525 4.5 Luvic Phaeozems Clay loam 31.0 1.24 13.5 1.42 7.2
34°47′, 113°40′ Warm-temperate, semi-humid Double-cropping, maize/wheat annually 632 14.3 Calcaric Cambisol Light loam 13.4 1.41 6.70 0.67 8.3
26°45′, 111°52′ Subtropical, humid monsoon Double-cropping, maize/wheat annually 1250 18.0 Ferralic Cambisol Light loam 35.2 1.19 7.89 1.07 5.7
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at GZL, and a wheat–maize double-cropping at both ZZ (mid-October to early June for wheat and mid-June to late September for maize) and QY (early November to early May for wheat and early April between wheat strips to July for maize). No irrigation was given to crops at GZL and QY, but two or three times of irrigations at ZZ to wheat and once to maize (about 75 mm each time) depending on precipitation. Pesticides (3 kg ha−1 carbendazim for wheat rust at a jointing stage, 3.75 kg ha−1 omethoate for aphids at wheat grain filling stage, 45 kg ha−1 carbofuran for corn borer at trumpet stage) were applied during growth when needed. Weeds were removed by hand. All above-ground biomass were manually harvested and then separated as grains and straws, which were oven dried to constant weight.
2.3. Experimental design and fertilization rates The field experiments were in a randomized block design with 3 replications in ZZ (plot size 45 m2), 2 replications in QY (plot size 196 m2) but no replication in GZL (plot size 200 m2). Five treatments were examined in this study: (1) unfertilized control; (2) chemical nitrogen (N) and phosphorus (P) plus potassium (K) (NPK); (3) NPK plus straw (NPKS); (4) NPK plus manure (NPKM); (5) 150% NPKM (1.5NPKM). The annual fertilization rates were summarized in Table 2. At each site, an equivalent total amount of N was applied to all treatments except an extra N from wheat straw under NPKS at QY. In all sites the chemical sources of N, P and K were urea, calcium triple superphosphate and potassium sulfate, respectively. The manure was horse manure from 1990 to 1998 and cattle manure from 1999 to 2007 at ZZ, whereas pig manure from 1990 to 2007 at both GZL and QY. For the two manure treatments, 30% of the total N was from the chemical fertilizer and the rest 70% from the manure. The additional added chemicals P and K in the manure and straw were not adjusted. Chemical fertilizers were applied before seeding, with 30% for wheat and 70% for maize with no topdressing at ZZ and QY, while one-third of the chemical N and the total P and K were applied at sowing, and the rest of N as top-dressing at the jointing stage at GZL. Meanwhile, the entire amount of manure and straw were once applied before wheat seeding.
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2.5. Determination of MBC and MBN The determination of MBC and MBN was in accordance with chloroform fumigation extraction method (Vance et al., 1987) and the conversion factor of 0.45 for both MBC and MBN. The amount of total organic C (TOC) in the extracts was measured using an automatic TOC analyzer (vario TOC cube, Elementar, Hanau, Germany). 2.6. Determination of SOC physical fractions Determination of soil physical fractionations was in accordance with Gale et al. (2000) and Six et al. (2000). In this study four physical fractions were adopted (Tong et al., 2014): (1) the coarse free particulate organic C (cfPOC, N 250 μm, unprotected SOC); (2) the fine free POC (ffPOC, 53–250 μm, unprotected SOC); (3) the intra-microaggregate POC (iPOC, N53 μm from the heavy fraction of ffPOC, physically protected SOC) and (4) the mineral associated organic C fraction (MOC, b 53 μm, chemically and biochemically protected SOC). 2.7. Analyses of carbon and nitrogen in soils Concentrations of SOC and TN in bulk and fraction soils were determined by the wet oxidation with K2Cr2O7 and the semi-micro Kjeldahl methods using air-dried soil samples. 2.8. Statistical analyses One-way ANOVA was performed to test different fertilization effects on soil physicochemical properties, soil microbial properties and physical fractions. Pearson linear correlations between MBC, MBN or soil physical fractions and SOC or TN were determined. Principal components analysis (PCA) was undertaken to identify soil fertility between fertilizations. Statistical significant differences were judged by LSD test at P b 0.05. Graphs were prepared using SigmaPlot 10.0. All the statistical analyses were conducted using the SPSS 17.0. 3. Results and discussion 3.1. Soil organic carbon and total nitrogen
2.4. Soil sampling Soil samples at 0–20 cm depth were collected in September 2007 using a 10 cm diameter soil auger. A total of 9 soil cores from each plot were collected with 3 cores as one composite sample, which was then divided into two subsamples. One subsample was stored at 4 °C prior to the MBC and MBN analyses; another was air-dried and ground for the determination of soil chemical and physical properties.
Generally, significantly higher both SOC and TN among the three sites patterned as GZL N QY ≈ ZZ for the same fertilization, while among five fertilizations for each site as: 1.5NPKM N NPKM N NPKS ≈ NPK ≈ Control, except a higher SOC under NPNKS at ZZ and a lower SOC under the Control at QY (Fig. 1a, b, e, f, i, j). Compared with the Control, NPK plus manure (NPKM or 1.5NPKM, hereafter manure) applications significantly increased SOC (42.6–97.5%) and TN (37.8– 109.7%) at all three sites. These trends could attribute to greater C and
Table 2 Annual fertilization rates of N, P and K (kg ha−1) at the three 17 years (1990–2007) long-term experimental sites in China. Treatmentsa
Control NPK NPKSc NPKMd 1.5NPKM
Gongzhuling
Zhengzhou
Qiyang
Inorganicb N–P–K (kg ha−1)
Organic N (kg ha−1)
Inorganic N–P–K (kg ha−1)
Organic N (kg ha−1)
Inorganic N–P–K (kg ha−1)
Organic N (kg ha−1)
0–0–0 165–36–68 112–36–68 50–36–68 75–54–103
0 0 53 115 172.5
0–0–0 353–78–146 238–78–146 238–78–146 356–117–220
0 0 115 115 173.5
0–0–0 300–53–100 300–53–100 90–53–100 135–79–149
0 0 39 210 315
a Treatment codes: NPK: inorganic nitrogen, phosphorous and potassium, the chemical sources of N, P and K were urea, calcium triple superphosphate and potassium sulfate, respectively; NPKS: NPK plus straw return; NPKM: NPK plus manure; 1.5NPKM: 1.5 times NPKM. b Inorganic N fertilizer is as urea, P as calcium superphosphate, K as potassium sulfate. c Straw rates (3.2 to 7.5 Mg ha−1 year−1) varied with N concentration and sites (1/2 wheat straw and 1/2 corn straw were returned at Qiyang while only maize straw was returned at Gongzhuling and Zhengzhou). d The manures were pig manure since 1990 at Gongzhuling (23.0 Mg ha−1 year−1) and Qiyang (42.0 Mg ha−1 year−1), but horse manure from 1990 to 1998 and cattle manure from 1999 to 2007 at Zhengzhou (12.9 Mg ha−1 year−1). All such manure amounts at these three sites were averaged in the fresh weight during 1990 to 2007.
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Fig. 1. Effects of 17 years (1990–2007) fertilizations on soil organic carbon (SOC), total nitrogen (TN), microbial biomass carbon (MBC) and nitrogen (MBN) of bulk soils at three long-term field sites in China. Data (means ± SD, n = 3) with different letters denote significant differences between fertilizations in the same site (a, b, c, d, e) and between sites for the same fertilization (x, y, z) at P b 0.05. Abbreviations: NPK: inorganic nitrogen, phosphorous and potassium; NPKS: NPK plus straw return; NPKM: NPK plus manure; 1.5NPKM: 1.5 times NPKM. GZL: Gongzhuling; ZZ: Zhengzhou; QY: Qiyang.
N inputs through the input of manure and/or root biomass due to better crop growth. Similar results have been reported from other long-term (10 to 100 years) fertilizations in cropland soils (Blair et al., 2006; Giacometti et al., 2013; Purakayastha et al., 2008). It is worth to note that a higher annual C addition with manure from NPKM to 1.5NPKM produced significant increase of sequestrated C (13.8–23.9%) and N (15.5–52.2%) at all three sites. These findings indicated that the tested soils have further potentials to sequestrate considerable C and N, suggesting the significance of more organic C input from manure could build up SOC and TN pool in our study soils. The sole chemical fertilization (NPK) generally had no effects on SOC and TN except a 22.8% increase of SOC at QY (Fig. 1). The lack of response of SOC to chemical fertilizer might be due to a lower C input, while the non-response of TN might be due to the N loss via leaching, denitrification or some other process such as ammonia volatilization in the cropland (Ju et al., 2009). Meanwhile, the return of straw had no influence on TN at the three sites, while it significantly increased SOC at ZZ (39.5%) and QY (24.8%), but not at GZL, indicating that soil C sequestration could be enhanced, but not N sequestration, when crop
residues had been incorporated into soil. The irresponsible status of SOC at GZL might be due to the low decomposition of straw added under a lower climate temperature in north China, or to an induced SOC decomposition through the straw return. 3.2. Microbial biomass carbon and microbial biomass nitrogen The highest MBC and MBN were observed at both GZL and in QY, but not at ZZ for the same fertilization (Fig. 1c, d, g, h, k, l). Meanwhile, at all three sites a significant increase and a maximum amount of MBC and MBN were under the NMKM and 1.5NPKM treatments (Fig. 1), which were similar to the pattern reported by other studies in the long-term (15–30 years) fertilization experiments in other cropland soils (Liang et al., 2012; Manna et al., 2006). Compared with the Control, MBC was 16.0%–159.6% higher, and MBN was 80.6%–119.1% higher under manure treatments at the three sites. Tu et al. (2006) found that an increase in easily decomposable organic C was likely contributed to the enhanced microbial biomass. Therefore, MBC and MBN were mostly enhanced by the regular supply of the readily metabolizable C and N under
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manure treatments. NPKS treatment had no effects on MBC and MBN at GZL, but significantly increased at ZZ, compared with the Control, which were probably due to the lower decomposition of straw in a lower climatic temperature at GZL and a suitable temperature and precipitation for microbial growth at ZZ. In contrast, QY is characterized by a higher temperature and humidity, which could lead to a faster straw decomposition, and then to a loss of straw-derived C and a release of N, thus MBC was not impacted while MBN was significantly increased under NPKS (Tong et al., 2014). Meanwhile, MBC under NPK was significantly increased at ZZ (48.2%), but significantly decreased at GZL (90.4%) and QY (24.3%), compared with the Control (Fig. 1). The stimulated effects of NPK fertilization to MBC at ZZ might mainly be because of an enhanced growth of crops. At ZZ, crop yield was 285% higher under NPK fertilization than under the control, which might result in an accumulation of MBC through increased root turnover and exudates in soils. Zhong and Cai (2007) also found that MBC was significantly increased by NPK application in a 13 year long-term fertilization in China. However, the
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decreased MBC under NPK at GZL and QY might attribute to serious soil acidity due to a long-term N fertilization. Indeed, our previous study found that NPK treatment significantly increased soil exchangeable acidity dominated by Al and elevated acidification rates at QY during the decreasing of soil pH (Cai et al., 2014). In this present study, the pH was not significantly changed at ZZ but significantly declined from 7.64 under the control to 6.19 under NPK at GZL, and from 5.70 under the control to 4.44 under NPK at QY after 17 years chemical fertilization. Therefore, the lower pH induced Al toxicity could suppress microbial activities and growth of soil microorganisms, and thus consequently lead to a reduction in microbial biomass. 3.3. Soil organic carbon and total nitrogen in physical fractions Averagely, the recoveries of soils after the fraction procedure were 97.3%, 99.3% and 97.2% under different fertilizations for GZL, ZZ and QY, respectively. The MOC fraction accounted for the largest (77.4– 87.2%) portion and ffPOC for the smallest (0.13–0.52%) portion of
Fig. 2. Effects of 17 year (1990–2007) fertilizations on soil organic carbon (means ± SD) of each soil aggregate fractions at three long-term field sites in China. Data (means ± SD, n = 3) with different letters denote significant differences between fertilizations in the same site (a, b, c, d, e), between sites for the same fertilization (x, y, z) and between fractions in the same site under the same treatment (α,β, γ, δ) at P b 0.05. Abbreviations: cfPOC: coarse free particulate organic carbon; ffPOC: fine free particulate organic carbon; iPOC: intramicroaggregate particulate organic carbon; MOC: mineral associated organic carbon; See Fig. 1 for fertilization treatments and sites abbreviations.
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Fig. 3. Effect of 17 year (1990–2007) fertilizations on total nitrogen of each soil aggregate fractions at three long-term field sites in China. Data (means ± SD, n = 3) with different letters denote significant differences between fertilizations in the same site (a, b, c, d, e),between sites for the same fertilization (x, y, z) and between fractions in the same site under the same treatment (α,β, γ, δ) at P b 0.05. Abbreviations: cfPTN: coarse free particulate total nitrogen; ffPTN: fine free particulate total nitrogen; iPTN: intra-microaggregate particulate total nitrogen; MTN: mineral associated total nitrogen; See Fig. 1 for fertilization treatments and site abbreviations.
soils. Additionally, the average recovery of SOC after the fraction procedure were 91.4%, 107.7% and 90.3% and the recovery of TN were 85.6%, 90.2%, 104.3% under different treatments in GZL, ZZ and QY, respectively. As expected, manure application (NPKM and 1.5NPKM) significantly increased SOC and TN in all four soil physical fractions compared with the Control at the three sites (Figs. 2 and 3). At GZL and QY, the SOC and TN in all four soil physical fractions under NPKM and 1.5NPKM were even significantly higher than those under NPKS and NPK treatments. Other studies also observed significant increase in SOC and TN of soil fractions under manure treatments (Purakayastha et al., 2008; Sleutel et al., 2006). Among the four soil physical fractions, the increase under manure treatments was highest in cfPOC fraction for SOC (189.2– 650.6%, averaged 329.3%) and TN (185.2–841.0%, averaged 431.1%), but lowest in MOC fraction for SOC (17.1–56.7%, averaged 40.8%) and TN (3.3–74.7%, averaged 45.4%) (Figs. 2 and 3). In a long-term 100 year experiment at Rothamsted, Blair et al. (2006) reported that the manure application had increased liable organic C by an average of 353%,
which was close to the increase rate of this study. The cfPOC was mainly derived from plant material, which might haven been subject to partial microbial decomposition. Sleutel et al. (2006) found the combined SOC in the cfPOC and ffPOC made up 10–13% of the total SOC under different fertilization treatments in a 42 year long-term cropland fertilization in Hungary. In the present study, the average proportion of these fractions varied between 9.8–22.5% and 4.7–16.7% of the bulk soil SOC and TN across the three test sites (Fig. S1), which correspond fairly with their results. In addition, there was a clear increasing trend of the proportion of the amount of SOC and TN presenting in the cfPOC and cfPTN fraction under manure, chemical fertilization or straw return treatments at the three sites, and the maximum proportion increase was under manure (from 6.9 to 13.6% at GZL, 6.0 to 12.9% at ZZ and 5.3 to 19.6% at QY) (Fig. S1). The highest increase of SOC in the cfPOC fraction in our study confirmed that cfPOC was a good indicator for the change in SOC under fertilizations, especially under manure management (Figs. 2). Due to a larger organic C input through straw, the straw return treatment also generally increased SOC and TN in each fraction at ZZ and QY
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(except for the ffPOC and ffPTN at ZZ), but not at GZL except for an increase in ffPOC and ffPTN, compared with the control (Figs. 2 and 3). Compared to NPK, however, NPKS significantly decreased SOC in each fraction at GZL (Fig. 2a, b, c, d). These results indicated that the returned straw might have stimulated the original soil old C decomposition, and such decompositions could be offset by the new straw C amendment, hence the SOC accumulation was similar under the straw return and the control at GZL. Chemical fertilizer significantly increased SOC of cfPOC (57–197%), ffPOC (95–166%) and iPOC (26–65%), but had no effects on MOC at all
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three sites and on ffPOC at ZZ (Fig. 2). Meanwhile, the TN of the four fractions was all increased under NPK except iPTN and MTN at GZL (Fig. 3). In general iPOC was thought to be stored in aggregates to prevent from the decomposition of microorganisms. Chemical fertilizer contained a large amount of available N that could stimulate the growth of crop as well as the activities of microorganism that might enhance the decomposition of iPOC fraction (Liu et al., 2010). The balanced NPK fertilization might have a stronger stimulation effect on crop growth, which could return more residues to soil than on SOC decomposition and N loss, leading to an increased SOC and TN in the cfPOC, ffPOC or
Fig. 4. Relationships between soil organic carbon (SOC) and microbial biomass carbon (MBC) of the bulk soil, cfPOC, ffPOC, iPOC or MOC of each soil physical fraction; and between total nitrogen (TN) and microbial biomass nitrogen (MBN) of the bulk soil, cfPTN, ffPTN, iPTN or MTN of each soil aggregate fraction under three 17 years (1990–2007) long-term fertilization sites in China (**P b 0.01 and ***P b 0.001). See Fig. 1 for fertilization treatments and site abbreviations, see Figs. 2 and 3 for SOC and TN fractions.
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iPOC fraction. The organic C in the iPOC fraction across these three sites ranged 7.3 to 15.7% of the total SOC (Fig. S1), which were similar to a range of 7.3 to 12.0% observed by Sleutel et al. (2006). MOC was associated with mineral and mainly sequestrated in soil in the form of humus, and the SOC and TN in the MOC and MTN fractions held the largest proportion of the total SOC (63.2–81.4%) and TN (73.1–90.0%) (Fig. S1). Meanwhile, the C input under NPK might not form enough complex organic compounds associated with mineral, which accounted for the non-response of SOC in the MOC fraction under chemical fertilization (Tong et al., 2014). The increase of TN in the MTN fraction under NPK at ZZ and QY was more likely due to the residue return through a stimulating effect on crop growth, whereas an unchanged TN in both the iPTN and MTN fractions under NPK at GZL might be attributed to a large extent on a higher TN concentration in the bulk soil at GZL than at ZZ and QY. Generally, for the same fertilization at the same site, higher TN in fractions generally ranked as MTN N iPTN N cfPTN N ffPTN at the three sites (Fig. 3), while significantly higher SOC in fractions ranked as MOC N iPOC N cfPOC N ffPOC at GZL, MOC N cfPOC ≈ iPOC ≈ ffPOC at ZZ except in ffPOC at NPKM and 1.5NPKM, and MOC N cfPOC N iPOC N ffPOC at QY except under Control and NPKS (Fig. 2). In addition, for the same fertilization among these three sites, higher cfPOC or cfPTN patterned as QY N GZL N ZZ, while in the other three fractions as GZL N QY N ZZ (Figs. 2 and 3).
3.4. Relationships between SOC and TN with MBC, MBN or fraction organic C or N The SOC significantly positively correlated with MBC, cfPOC, ffPOC, iPOC and MOC (R2 = 0.51–0.84, P = 0.01–0.001, Fig. 4a, b, c, d and e), while the TN significantly positively correlated with cfPTN, ffPTN, iPTN and MTN (R2 = 0.45–0.79, P = 0.01–0.001, Fig. 4g, h, i and j) respectively, but not with MBN (Fig. 4f). This meant that both microbial biomass and physical fractions were the components of bulk soil and they could indicate long-term changes of SOM and TN due to fertilization treatments. Chung et al. (2008) found that the SOC of the MOC fraction did not linearly relate with the C input and that the MOC fraction exhibited a C saturation behavior, namely, MOC might not have potential to further sequestrate soil C in soil. The significantly positively linear relationship between the SOC or TN of each physical fractions and the total SOC or TN of the bulk soil in the present study demonstrated that all of these fractions were not saturated. As a result, a potential is plausible for each physical fraction to sequestrate more C and N under different fertilizer managements at these three tested soils. Meanwhile, SOC also significantly positively correlated with TN (Fig. 5a), and SOC in each fraction significantly positively correlated with TN in each fraction across all three sites (R2 = 0.52–0.96, P = 0.01–0.001, Fig. 5b, c, e and f). The C:N ratio significantly decreased in the order of ffPOC (15.1) N cfPOC (14.4) ≈ iPOC (14.2) N MOC (6.6).
Fig. 5. Relationships between soil organic carbon (SOC) and total nitrogen (TN), microbial biomass carbon (MBC) with microbial biomass nitrogen (MBN) of the bulk soil, and between SOC with TN of each physical fractions under three 17 years (1990–2007) long-term fertilization sites in China (**P b 0.01 and ***p b 0.001). See Fig. 1 for fertilization treatments and site abbreviations, see Figs. 2 and 3 for SOC and TN fractions.
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the variance of soil fertility (SOC, TN, MBC, MBN, SOC and TN in each fraction) in GZL (Fig. 6a), ZZ (Fig. 6b) and QY (Fig. 6c), respectively. Soil fertility under fertilizations with the addition of manure was clearly separated with that under the chemical fertilization at all three sites, while under straw return was similar to the control at GZL, to NPKM at ZZ and to NPK at QY, which was well confirmed in all abovementioned results in this study. 4. Conclusions Our results demonstrated that continuous 17 year applications of manure significantly increased SOC and TN concentrations, MBC, MBN, and the SOC and TN in soil physical fraction of cfPOC, ffPOC, iPOC and MOC at three cropland sites of China along a heat and water gradient. Straw return might also have similar effects on SOC, TN, MBC, MBN and the SOC and TN in each soil physical fraction like the manure application, except in the low temperature and humidity site of GZL in northeast of China. Chemical fertilization had showed relatively less effects on the total SOC and TN accumulation in the whole and each soil fraction. As a general rule, cfPOC was the most sensitive indicator to C changes and MOC, MTN was the main form that C and TN sequestrated in soil under long-term fertilizations. MBC, SOC and TN in aggregate fractions were significantly linearly correlated to total SOC and TN in the bulk soil. The overall PCA showed that manure fertilization was the best fertilization management strategy while straw return should be taken into account climate factors in cropland soils in China. Supplementary data to this article can be found online at http://dx. doi.org/10.1016/j.scitotenv.2015.06.011. Acknowledgments We acknowledge our colleagues for their unremitting efforts to the long-term experiments. Financial support was from the National Natural Science Foundation of China (41371247) and National Basic Research Program of China (2011CB100501). References
Fig. 6. Principal component analyses of soil fertility under three 17 years (1990–2007) long-term fertilization sites in China. See Fig. 1 for fertilization treatments and site abbreviations.
The C:N ratio is indicative of the capacity of a soil to store and recycle nutrients. In general, soil C:N ratio decreases with increasing of degradation and humification of organic matter. As a decomposition proceeds, C is released during respiration and some of the mineralized N is lost through leaching or gaseous emissions while some other parts of mineralized N is reincorporated into the SOM pool (Chapin et al., 2002). The decrease of C:N ratio in the four fractions in this study indicates that MOC was most humified, and N was more stored than C in this fraction, which also showed the procession of SOC accumulation and sequestration in soil. Principal components analyses (PCA) showed that overall the principal components (PC1 and PC2) explained 86.9%, 89.6% and 91.2% of
Böhme, L., Langer, U., Böhme, F., 2005. Microbial biomass, enzyme activities and microbial community structure in two European long-term field experiments. Agric. Ecosyst. Environ. 109, 141–152. Blair, N., Faulkner, R., Till, A., Poulton, P., 2006. Long-term management impacts on soil C, N and physical fertility: part I: Broadbalk experiment. Soil Tillage Res. 91, 30–38. Cai, Z., Wang, B., Xu, M., Zhang, H., He, X., Zhang, L., Gao, S., 2014. Intensified soil acidification from chemical N fertilization and prevention by manure in an 18-year field experiment in the red soil of southern China. J. Soils Sediments 15, 260–270. Campbell, C., Janzen, H., Juma, N., 1997. Case studies of soil quality in the Canadian Prairies: long-term field experiments. Dev. Soil Sci. 25, 351–398. Chapin, F.S., Matson, P.A., Mooney, H.A., 2002. Principles of terrestrial ecosystem ecology. Springer, New York. Chung, H.G., Grove, J.H., Six, J., 2008. Indications for soil carbon saturation in a temperate agroecosystem. Soil Sci. Soc. Am. J. 72, 1132–1139. Compton, J.E., Boone, R.D., 2002. Soil nitrogen transformations and the role of light fraction organic matter in forest soils. Soil Biol. Biochem. 34, 933–943. Courtier-Murias, D., Simpson, A.J., Marzadori, C., Baldoni, G., Ciavatta, C., Fernandez, J.M., Lopez-De-Sa, E.G., Plaza, C., 2013. Unraveling the long-term stabilization mechanisms of organic materials in soils by physical fractionation and NMR spectroscopy. Agric. Ecosyst. Environ. 171, 9–18. Dormaar, J., Lindwall, C., Kozub, G., 1988. Effectiveness of manure and commercial fertilizer in restoring productivity of an artificially eroded Dark Brown Chernozemic soil under dryland conditions. Can. J. Soil Sci. 68, 669–679. Gale, W., Cambardella, C., Bailey, T., 2000. Surface residue- and root-derived carbon in stable and unstable aggregates. Soil Sci. Soc. Am. J. 64, 196–201. Giacometti, C., Demyan, M.S., Cavani, L., Marzadori, C., Ciavatta, C., Kandeler, E., 2013. Chemical and microbiological soil quality indicators and their potential to differentiate fertilization regimes in temperate agroecosystems. Appl. Soil Ecol. 64, 32–48. Giacometti, C., Cavani, L., Baldoni, G., Ciavatta, C., Marzadori, C., Kandeler, E., 2014. Microplate-scale fluorometric soil enzyme assays as tools to assess soil quality in a long-term agricultural field experiment. Appl. Soil Ecol. 75, 80–85. Hart, S.C., Nason, G.E., Myrold, D.D., Perry, D.A., 1994. Dynamics of gross nitrogen transformations in an old-growth forest: the carbon connection. Ecology 75, 880–891. He, Y., Qi, Y., Dong, Y., Xiao, S., Peng, Q., Liu, X., Sun, L., 2013. Effects of nitrogen fertilization on soil microbial biomass and community functional diversity in temperate grassland in Inner Mongolia, China. Clean Soil Air Water 41, 1216–1221.
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Y.T. He et al. / Science of the Total Environment 532 (2015) 635–644
Ju, X.T., Xing, G.X., Chen, X.P., Zhang, S.L., Zhang, L.J., Liu, X.J., Cui, Z.L., Yin, B., Christie, P., Zhu, Z.L., 2009. Reducing environmental risk by improving N management in intensive Chinese agricultural systems. Proc. Natl. Acad. Sci. 106, 3041–3046. Liang, Q., Chen, H., Gong, Y., Fan, M., Yang, H., Lal, R., Kuzyakov, Y., 2012. Effects of 15 years of manure and inorganic fertilizers on soil organic carbon fractions in a wheat–maize system in the North China Plain. Nutr. Cycl. Agroecosyst. 92, 21–33. Liu, H., Tong, X.G., Xu, Y.M., Ma, X.W., Wang, X.H., Zhang, W.J., Xu, M.G., 2010. Evolution characteristics of organic carbon fractions in gray desert soil under long-term fertilization. Plant Nutr. Fertil. Sci. 16, 794–800. Manna, M., Swarup, A., Wanjari, R., Singh, Y., Ghosh, P., Singh, K., Tripathi, A., Saha, M., 2006. Soil organic matter in a West Bengal Inceptisol after 30 years of multiple cropping and fertilization. Soil Sci. Soc. Am. J. 70, 121–129. Purakayastha, T., Rudrappa, L., Singh, D., Swarup, A., Bhadraray, S., 2008. Long-term impact of fertilizers on soil organic carbon pools and sequestration rates in maize– wheat–cowpea cropping system. Geoderma 144, 370–378. Reeves, D., 1997. The role of soil organic matter in maintaining soil quality in continuous cropping systems. Soil Tillage Res. 43, 131–167. Sarathchandra, S.U., Ghani, A., Yeates, G.W., Burch, G., Cox, N.R., 2001. Effect of nitrogen and phosphate fertilisers on microbial and nematode diversity in pasture soils. Soil Biol. Biochem. 33, 953–964. Six, J., Elliott, E., Paustian, K., 2000. Soil macroaggregate turnover and microaggregate formation: a mechanism for C sequestration under no-tillage agriculture. Soil Biol. Biochem. 32, 2099–2103.
Six, J., Callewaert, P., Lenders, S., De Gryze, S., Morris, S., Gregorich, E., Paul, E., Paustian, K., 2002. Measuring and understanding carbon storage in afforested soils by physical fractionation. Soil Sci. Soc. Am. J. 66, 1981–1987. Sleutel, S., De Neve, S., Nemeth, T., Toth, T., Hofman, G., 2006. Effect of manure and fertilizer application on the distribution of organic carbon in different soil fractions in long-term field experiments. Eur. J. Agron. 25, 280–288. Sun, H., Deng, S., Raun, W., 2004. Bacterial community structure and diversity in a century-old manure-treated agroecosystem. Appl. Environ. Microbiol. 70, 5868–5874. Tong, X.G., Xu, M.G., Wang, X.J., Bhattacharyya, R., Zhang, W.J., Cong, R.H., 2014. Longterm fertilization effects on organic carbon fractions in a red soil of China. Catena 113, 251–259. Tu, C., Ristaino, J.B., Hu, S., 2006. Soil microbial biomass and activity in organic tomato farming systems: effects of organic inputs and straw mulching. Soil Biol. Biochem. 38, 247–255. Vance, E.D., Brookes, P.C., Jenkinson, D.S., 1987. An extraction method for measuring soil microbial biomass C. Soil Biol. Biochem. 19, 703–707. Zhong, W.H., Cai, Z.C., 2007. Long-term effects of inorganic fertilizers on microbial biomass and community functional diversity in a paddy soil derived from quaternary red clay. Appl. Soil Ecol. 36, 84–91.
Contents lists available at ScienceDirect
Science of the Total Environment journal homepage: www.elsevier.com/locate/scitotenv
Long-term combined chemical and manure fertilizations increase soil organic carbon and total nitrogen in aggregate fractions at three typical cropland soils in China Y.T. He a, W.J. Zhang a, M.G. Xu a,⁎, X.G. Tong b, F.X. Sun a, J.Z. Wang a, S.M. Huang c, P. Zhu d, X.H. He a,e a Ministry of Agriculture Key Laboratory of Crop Nutrition and Fertilization, Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural Sciences, Beijing 100081, China b College of Resources and Environment, Northwest A & F University, Yangling, Shannxi 712100, China c Institute of Plant Nutrition, Resources and Environment, Henan Academy of Agricultural Sciences, Zhengzhou 450002, China d Centre of Agricultural Environment and Resources, Jilin Academy of Agricultural Sciences, Changchun 130033, China e School of Plant Biology, University of Western Australia, Crawley, WA 6009, Australia
H I G H L I G H T S • • • • •
Assessed the effects of 17 years fertilization on SOC, TN and its fractions. Manure increased all indexes but straw return had no effects on all indexes at GZL. Chemical fertilization had no effects on TN but decreased MBC in GZL and QY. cfPOC was the most sensitive indicator and MOC, MTN was the main sequestrated form. Straw return was site-dependent and manure was the best for improving soil quality.
a r t i c l e
i n f o
Article history: Received 25 January 2015 Received in revised form 26 May 2015 Accepted 2 June 2015 Available online 25 June 2015 Editor: D. Barcelo Keywords: Long-term fertilization Particulate organic carbon Mineral associated organic C Microbial biomass carbon and nitrogen Luvic Phaeozems Calcaric Cambisol Ferralic Cambisols
a b s t r a c t Soil organic carbon (SOC), total nitrogen (TN), microbial biomass carbon (MBC) and nitrogen (MBN) are important factors of soil fertility. However, effects of the combined chemical fertilizer and organic manure or straw on these factors and their relationships are less addressed under long-term fertilizations. This study addressed changes in SOC, TN, MBC and MBN at 0–20 cm soil depth under three 17 years (September 1990–September 2007) long-term fertilization croplands along a heat and water gradient in China. Four soil physical fractions (coarse free and fine free particulate organic C, cfPOC and ffPOC; intra-microaggregate POC, iPOC; and mineral associated organic C, MOC) were examined under five fertilizations: unfertilized control, chemical nitrogen (N), phosphorus (P) and potassium (K) (NPK), NPK plus straw (NPKS, hereafter straw return), and NPK plus manure (NPKM and 1.5NPKM, hereafter manure). Compared with Control, manure significantly increased all tested parameters. SOC and TN in fractions distributed as MOC N iPOC N cfPOC N ffPOC with the highest increase in cfPOC (329.3%) and cfPTN (431.1%), and the lowest in MOC (40.8%) and MTN (45.4%) under manure. SOC significantly positively correlated with MBC, cfPOC, ffPOC, iPOC and MOC (R2 = 0.51–0.84, P b 0.01), while TN with cfPTN, ffPTN, iPTN and MTN (R2 = 0.45–0.79, P b 0.01), but not with MBN, respectively. Principal component analyses explained 86.9–91.2% variance of SOC, TN, MBC, MBN, SOC and TN in each fraction. Our results demonstrated that cfPOC was a sensitive SOC indicator and manure addition was the best fertilization for improving soil fertility while straw return should take into account climate factors in Chinese croplands. © 2015 Elsevier B.V. All rights reserved.
1. Introduction In cropland soil, the preservation or improvement of soil quality and productivity is of major importance. Soil organic carbon (SOC) is closely associated with a wide range of physical, chemical and biological ⁎ Corresponding author. E-mail address: [email protected] (M.G. Xu).
http://dx.doi.org/10.1016/j.scitotenv.2015.06.011 0048-9697/© 2015 Elsevier B.V. All rights reserved.
properties, and thus has been recognized as a key component of soil quality (Reeves, 1997). Fertilizer application has been widely used as a common management practice to increase soil carbon (C) sequestration and SOC level. For instance, to increase soil fertility and obtain a satisfactory yield, manures have been used for nearly 4000 years in China, Japan and Korea (Dormaar et al., 1988). In addition, in cropland soils SOC also represents a potential sink of atmospheric CO2. As a result, understanding the impact of chemical fertilizer and manure application
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on SOC and its fractions could provide valuable information for maintaining or implementing environmentally sustainable management practices for agroecosystems. In general, the readily decomposable labile C is sensitive and responds more quickly to changes in management practices than recalcitrant C and thus is used as an early indicator of SOC changes (Campbell et al., 1997). The microbial biomass plays a critical role in regulating the C and N cycling processes in soils, and microbial biomass carbon (MBC) and nitrogen (MBN) are sensitive indicators for changes resulting from agronomic practices and other perturbations of soil ecosystems though they are only a small part of SOC and total nitrogen (TN). Numerous studies have reported the effects of fertilization on MBC or MBN, but no consistent results have been obtained (Böhme et al., 2005; Zhong and Cai, 2007). For example, organic manure tends to increase MBC by direct C input and/or the change of microbial community composition (Sun et al., 2004), while chemical fertilization have often produced contradictory effects (He et al., 2013; Sarathchandra et al., 2001). This uncertainty is partly attributed to the short-time study and to variations in soil type, climate condition, and crop system under different fertilizations. In addition, the structure composition of the different fertilizers, the changes in soil enzyme activities and abundance and function of the soil microbial community under different fertilizations also contribute to the contradictory effects (Giacometti et al., 2013, 2014). Therefore, it is important to assess the effects of different fertilizations on MBC or MBN in variable soil types at a long-time scale to better understand soil C transformation or accumulation. Meanwhile, SOC fractions are characterized by differential stabilities and turnover rate, thus also been extensively used as sensitive indicators to provide insight into the consequences of management practices that could not be gleaned from studies of total SOC. Six et al. (2002) proposed a physical fractionation procedure and the associated conceptual SOC model that separated the bulk SOC pool into four conceptual aggregate fractions according to different protection mechanisms. These four conceptual fractions are (1) coarse free and (2) fine free particulate organic C (cfPOC and ffPOC, unprotected SOC inter-aggregate), (3) intramicroaggregate particulate organic C (iPOC, physically protected SOC) and (4) mineral associated organic C (MOC, chemically and biochemically protected SOC). This conceptual model could give an opportunity to understand the effect of soil microbial activities during SOC biodegradation under different management practices (Six et al., 2002). In addition, this physical fractionation technique has been employed to separate SOC fractions that stabilize C and thus could have important implications for soil C sequestration at a long-time scale. In a 44 year field experiment, both cattle manure and crop residue treatments increased SOC and most of these increases (up to 72%) were stored in MOC fraction (Courtier-Murias et al., 2013). However, limited information still exists regarding the long-term impacts of different fertilizations on SOC physical fractions, particularly in cropland soils in China. The quality and quantity of SOC have been suggested as major factors affecting soil N dynamics, and one of the major roles of organic
matter in soil fertility is to release N and other nutrients for crop growth (Hart et al., 1994). Changes in N content in soil fractions therefore may be a good indicator of soil fertility and plant N supplying capabilities of a given soil. For instance, studies have reported changes in N contents within different density fractions under different fertilization managements (Compton and Boone, 2002). However, less is known about the responses of TN content in physical fractionations under long-term different fertilizations. Along a water and heat gradient from north to south, black soil (Luvic Phaeozems for FAO classification, Leptic Phaeozems for WRB classification), fluvo-aquic soil (Calcaric Cambisol for FAO classification and Fluvic Cambisol for WRB classification) and red soil (Ferralic Cambisols for FAO and Ferric Acrisols for WRB classification) are main soil types distributing from northwest, central and south of China, where also the important agricultural regions are located. To develop efficient soil fertility management practices, long-term experiment networks have been established since 1990 to examine the effects of continuous applications of chemical fertilizer and the combination of chemical fertilizer and manure on crop yield and soil fertility over these regions. Using soils under five 17 years long-term (September 1990–September 2007) fertilizations (chemical fertilizer with or without organic manure) from three sites (~500 km away from each site), the aims of this study were thus to address the effects of the sole chemical fertilization and the combined fertilization of chemical fertilizer and organic manure on (1) variations of MBC and MBN; (2) variations of SOC and TN accumulations in the whole soil and different physical fraction pools; (3) relationships between MBC or MBN, fraction pools and SOC or TN accumulations. Here, we paid special attention on the distribution and accumulation of SOC and TN in soil physical fractions. The expected results could identify the key fractions and the best fertilizer management practices for SOC accumulations under different fertilizer managements across different cropping systems in China. 2. Materials and methods 2.1. Site description Along a water and heat gradient from north to south of China, three selected long-term field fertilization sites (established since September 1990) are located in Gongzhuling (GZL), Jilin, northeast China; Zhengzhou (ZZ), Henan, central China; and Qiyang (QY), Hunan, southern China. Information on basic, geography, climate and soil chemical properties of these three sites in 1990 is briefly given in Table 1. 2.2. Cropping systems and plant harvest Two years before the establishment of these three long-term fertilization sites, local crops as follows were cultivated without fertilization to reduce soil fertility variability. The cropping system differed in these three sites: a mono-maize cropping (late April to late September)
Table 1 General description of geography and soil properties (0–20 cm in 1990) at the three 17 years (1990–2007) long-term experimental sites in China.
Location Climate Cropping system Precipitation (mm) Mean temperature (°C) FAO soil classification Soil texture Clay content (%) Bulk density (g cm−3) Initial SOC (g kg−1) Total N (g kg−1) pH (soil:water = 1:2.5)
Gongzhuling
Zhengzhou
Qiyang
43°30′, 124°48′ Mild-temperate, semi-humid Single-cropping, maize 525 4.5 Luvic Phaeozems Clay loam 31.0 1.24 13.5 1.42 7.2
34°47′, 113°40′ Warm-temperate, semi-humid Double-cropping, maize/wheat annually 632 14.3 Calcaric Cambisol Light loam 13.4 1.41 6.70 0.67 8.3
26°45′, 111°52′ Subtropical, humid monsoon Double-cropping, maize/wheat annually 1250 18.0 Ferralic Cambisol Light loam 35.2 1.19 7.89 1.07 5.7
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at GZL, and a wheat–maize double-cropping at both ZZ (mid-October to early June for wheat and mid-June to late September for maize) and QY (early November to early May for wheat and early April between wheat strips to July for maize). No irrigation was given to crops at GZL and QY, but two or three times of irrigations at ZZ to wheat and once to maize (about 75 mm each time) depending on precipitation. Pesticides (3 kg ha−1 carbendazim for wheat rust at a jointing stage, 3.75 kg ha−1 omethoate for aphids at wheat grain filling stage, 45 kg ha−1 carbofuran for corn borer at trumpet stage) were applied during growth when needed. Weeds were removed by hand. All above-ground biomass were manually harvested and then separated as grains and straws, which were oven dried to constant weight.
2.3. Experimental design and fertilization rates The field experiments were in a randomized block design with 3 replications in ZZ (plot size 45 m2), 2 replications in QY (plot size 196 m2) but no replication in GZL (plot size 200 m2). Five treatments were examined in this study: (1) unfertilized control; (2) chemical nitrogen (N) and phosphorus (P) plus potassium (K) (NPK); (3) NPK plus straw (NPKS); (4) NPK plus manure (NPKM); (5) 150% NPKM (1.5NPKM). The annual fertilization rates were summarized in Table 2. At each site, an equivalent total amount of N was applied to all treatments except an extra N from wheat straw under NPKS at QY. In all sites the chemical sources of N, P and K were urea, calcium triple superphosphate and potassium sulfate, respectively. The manure was horse manure from 1990 to 1998 and cattle manure from 1999 to 2007 at ZZ, whereas pig manure from 1990 to 2007 at both GZL and QY. For the two manure treatments, 30% of the total N was from the chemical fertilizer and the rest 70% from the manure. The additional added chemicals P and K in the manure and straw were not adjusted. Chemical fertilizers were applied before seeding, with 30% for wheat and 70% for maize with no topdressing at ZZ and QY, while one-third of the chemical N and the total P and K were applied at sowing, and the rest of N as top-dressing at the jointing stage at GZL. Meanwhile, the entire amount of manure and straw were once applied before wheat seeding.
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2.5. Determination of MBC and MBN The determination of MBC and MBN was in accordance with chloroform fumigation extraction method (Vance et al., 1987) and the conversion factor of 0.45 for both MBC and MBN. The amount of total organic C (TOC) in the extracts was measured using an automatic TOC analyzer (vario TOC cube, Elementar, Hanau, Germany). 2.6. Determination of SOC physical fractions Determination of soil physical fractionations was in accordance with Gale et al. (2000) and Six et al. (2000). In this study four physical fractions were adopted (Tong et al., 2014): (1) the coarse free particulate organic C (cfPOC, N 250 μm, unprotected SOC); (2) the fine free POC (ffPOC, 53–250 μm, unprotected SOC); (3) the intra-microaggregate POC (iPOC, N53 μm from the heavy fraction of ffPOC, physically protected SOC) and (4) the mineral associated organic C fraction (MOC, b 53 μm, chemically and biochemically protected SOC). 2.7. Analyses of carbon and nitrogen in soils Concentrations of SOC and TN in bulk and fraction soils were determined by the wet oxidation with K2Cr2O7 and the semi-micro Kjeldahl methods using air-dried soil samples. 2.8. Statistical analyses One-way ANOVA was performed to test different fertilization effects on soil physicochemical properties, soil microbial properties and physical fractions. Pearson linear correlations between MBC, MBN or soil physical fractions and SOC or TN were determined. Principal components analysis (PCA) was undertaken to identify soil fertility between fertilizations. Statistical significant differences were judged by LSD test at P b 0.05. Graphs were prepared using SigmaPlot 10.0. All the statistical analyses were conducted using the SPSS 17.0. 3. Results and discussion 3.1. Soil organic carbon and total nitrogen
2.4. Soil sampling Soil samples at 0–20 cm depth were collected in September 2007 using a 10 cm diameter soil auger. A total of 9 soil cores from each plot were collected with 3 cores as one composite sample, which was then divided into two subsamples. One subsample was stored at 4 °C prior to the MBC and MBN analyses; another was air-dried and ground for the determination of soil chemical and physical properties.
Generally, significantly higher both SOC and TN among the three sites patterned as GZL N QY ≈ ZZ for the same fertilization, while among five fertilizations for each site as: 1.5NPKM N NPKM N NPKS ≈ NPK ≈ Control, except a higher SOC under NPNKS at ZZ and a lower SOC under the Control at QY (Fig. 1a, b, e, f, i, j). Compared with the Control, NPK plus manure (NPKM or 1.5NPKM, hereafter manure) applications significantly increased SOC (42.6–97.5%) and TN (37.8– 109.7%) at all three sites. These trends could attribute to greater C and
Table 2 Annual fertilization rates of N, P and K (kg ha−1) at the three 17 years (1990–2007) long-term experimental sites in China. Treatmentsa
Control NPK NPKSc NPKMd 1.5NPKM
Gongzhuling
Zhengzhou
Qiyang
Inorganicb N–P–K (kg ha−1)
Organic N (kg ha−1)
Inorganic N–P–K (kg ha−1)
Organic N (kg ha−1)
Inorganic N–P–K (kg ha−1)
Organic N (kg ha−1)
0–0–0 165–36–68 112–36–68 50–36–68 75–54–103
0 0 53 115 172.5
0–0–0 353–78–146 238–78–146 238–78–146 356–117–220
0 0 115 115 173.5
0–0–0 300–53–100 300–53–100 90–53–100 135–79–149
0 0 39 210 315
a Treatment codes: NPK: inorganic nitrogen, phosphorous and potassium, the chemical sources of N, P and K were urea, calcium triple superphosphate and potassium sulfate, respectively; NPKS: NPK plus straw return; NPKM: NPK plus manure; 1.5NPKM: 1.5 times NPKM. b Inorganic N fertilizer is as urea, P as calcium superphosphate, K as potassium sulfate. c Straw rates (3.2 to 7.5 Mg ha−1 year−1) varied with N concentration and sites (1/2 wheat straw and 1/2 corn straw were returned at Qiyang while only maize straw was returned at Gongzhuling and Zhengzhou). d The manures were pig manure since 1990 at Gongzhuling (23.0 Mg ha−1 year−1) and Qiyang (42.0 Mg ha−1 year−1), but horse manure from 1990 to 1998 and cattle manure from 1999 to 2007 at Zhengzhou (12.9 Mg ha−1 year−1). All such manure amounts at these three sites were averaged in the fresh weight during 1990 to 2007.
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Fig. 1. Effects of 17 years (1990–2007) fertilizations on soil organic carbon (SOC), total nitrogen (TN), microbial biomass carbon (MBC) and nitrogen (MBN) of bulk soils at three long-term field sites in China. Data (means ± SD, n = 3) with different letters denote significant differences between fertilizations in the same site (a, b, c, d, e) and between sites for the same fertilization (x, y, z) at P b 0.05. Abbreviations: NPK: inorganic nitrogen, phosphorous and potassium; NPKS: NPK plus straw return; NPKM: NPK plus manure; 1.5NPKM: 1.5 times NPKM. GZL: Gongzhuling; ZZ: Zhengzhou; QY: Qiyang.
N inputs through the input of manure and/or root biomass due to better crop growth. Similar results have been reported from other long-term (10 to 100 years) fertilizations in cropland soils (Blair et al., 2006; Giacometti et al., 2013; Purakayastha et al., 2008). It is worth to note that a higher annual C addition with manure from NPKM to 1.5NPKM produced significant increase of sequestrated C (13.8–23.9%) and N (15.5–52.2%) at all three sites. These findings indicated that the tested soils have further potentials to sequestrate considerable C and N, suggesting the significance of more organic C input from manure could build up SOC and TN pool in our study soils. The sole chemical fertilization (NPK) generally had no effects on SOC and TN except a 22.8% increase of SOC at QY (Fig. 1). The lack of response of SOC to chemical fertilizer might be due to a lower C input, while the non-response of TN might be due to the N loss via leaching, denitrification or some other process such as ammonia volatilization in the cropland (Ju et al., 2009). Meanwhile, the return of straw had no influence on TN at the three sites, while it significantly increased SOC at ZZ (39.5%) and QY (24.8%), but not at GZL, indicating that soil C sequestration could be enhanced, but not N sequestration, when crop
residues had been incorporated into soil. The irresponsible status of SOC at GZL might be due to the low decomposition of straw added under a lower climate temperature in north China, or to an induced SOC decomposition through the straw return. 3.2. Microbial biomass carbon and microbial biomass nitrogen The highest MBC and MBN were observed at both GZL and in QY, but not at ZZ for the same fertilization (Fig. 1c, d, g, h, k, l). Meanwhile, at all three sites a significant increase and a maximum amount of MBC and MBN were under the NMKM and 1.5NPKM treatments (Fig. 1), which were similar to the pattern reported by other studies in the long-term (15–30 years) fertilization experiments in other cropland soils (Liang et al., 2012; Manna et al., 2006). Compared with the Control, MBC was 16.0%–159.6% higher, and MBN was 80.6%–119.1% higher under manure treatments at the three sites. Tu et al. (2006) found that an increase in easily decomposable organic C was likely contributed to the enhanced microbial biomass. Therefore, MBC and MBN were mostly enhanced by the regular supply of the readily metabolizable C and N under
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manure treatments. NPKS treatment had no effects on MBC and MBN at GZL, but significantly increased at ZZ, compared with the Control, which were probably due to the lower decomposition of straw in a lower climatic temperature at GZL and a suitable temperature and precipitation for microbial growth at ZZ. In contrast, QY is characterized by a higher temperature and humidity, which could lead to a faster straw decomposition, and then to a loss of straw-derived C and a release of N, thus MBC was not impacted while MBN was significantly increased under NPKS (Tong et al., 2014). Meanwhile, MBC under NPK was significantly increased at ZZ (48.2%), but significantly decreased at GZL (90.4%) and QY (24.3%), compared with the Control (Fig. 1). The stimulated effects of NPK fertilization to MBC at ZZ might mainly be because of an enhanced growth of crops. At ZZ, crop yield was 285% higher under NPK fertilization than under the control, which might result in an accumulation of MBC through increased root turnover and exudates in soils. Zhong and Cai (2007) also found that MBC was significantly increased by NPK application in a 13 year long-term fertilization in China. However, the
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decreased MBC under NPK at GZL and QY might attribute to serious soil acidity due to a long-term N fertilization. Indeed, our previous study found that NPK treatment significantly increased soil exchangeable acidity dominated by Al and elevated acidification rates at QY during the decreasing of soil pH (Cai et al., 2014). In this present study, the pH was not significantly changed at ZZ but significantly declined from 7.64 under the control to 6.19 under NPK at GZL, and from 5.70 under the control to 4.44 under NPK at QY after 17 years chemical fertilization. Therefore, the lower pH induced Al toxicity could suppress microbial activities and growth of soil microorganisms, and thus consequently lead to a reduction in microbial biomass. 3.3. Soil organic carbon and total nitrogen in physical fractions Averagely, the recoveries of soils after the fraction procedure were 97.3%, 99.3% and 97.2% under different fertilizations for GZL, ZZ and QY, respectively. The MOC fraction accounted for the largest (77.4– 87.2%) portion and ffPOC for the smallest (0.13–0.52%) portion of
Fig. 2. Effects of 17 year (1990–2007) fertilizations on soil organic carbon (means ± SD) of each soil aggregate fractions at three long-term field sites in China. Data (means ± SD, n = 3) with different letters denote significant differences between fertilizations in the same site (a, b, c, d, e), between sites for the same fertilization (x, y, z) and between fractions in the same site under the same treatment (α,β, γ, δ) at P b 0.05. Abbreviations: cfPOC: coarse free particulate organic carbon; ffPOC: fine free particulate organic carbon; iPOC: intramicroaggregate particulate organic carbon; MOC: mineral associated organic carbon; See Fig. 1 for fertilization treatments and sites abbreviations.
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Fig. 3. Effect of 17 year (1990–2007) fertilizations on total nitrogen of each soil aggregate fractions at three long-term field sites in China. Data (means ± SD, n = 3) with different letters denote significant differences between fertilizations in the same site (a, b, c, d, e),between sites for the same fertilization (x, y, z) and between fractions in the same site under the same treatment (α,β, γ, δ) at P b 0.05. Abbreviations: cfPTN: coarse free particulate total nitrogen; ffPTN: fine free particulate total nitrogen; iPTN: intra-microaggregate particulate total nitrogen; MTN: mineral associated total nitrogen; See Fig. 1 for fertilization treatments and site abbreviations.
soils. Additionally, the average recovery of SOC after the fraction procedure were 91.4%, 107.7% and 90.3% and the recovery of TN were 85.6%, 90.2%, 104.3% under different treatments in GZL, ZZ and QY, respectively. As expected, manure application (NPKM and 1.5NPKM) significantly increased SOC and TN in all four soil physical fractions compared with the Control at the three sites (Figs. 2 and 3). At GZL and QY, the SOC and TN in all four soil physical fractions under NPKM and 1.5NPKM were even significantly higher than those under NPKS and NPK treatments. Other studies also observed significant increase in SOC and TN of soil fractions under manure treatments (Purakayastha et al., 2008; Sleutel et al., 2006). Among the four soil physical fractions, the increase under manure treatments was highest in cfPOC fraction for SOC (189.2– 650.6%, averaged 329.3%) and TN (185.2–841.0%, averaged 431.1%), but lowest in MOC fraction for SOC (17.1–56.7%, averaged 40.8%) and TN (3.3–74.7%, averaged 45.4%) (Figs. 2 and 3). In a long-term 100 year experiment at Rothamsted, Blair et al. (2006) reported that the manure application had increased liable organic C by an average of 353%,
which was close to the increase rate of this study. The cfPOC was mainly derived from plant material, which might haven been subject to partial microbial decomposition. Sleutel et al. (2006) found the combined SOC in the cfPOC and ffPOC made up 10–13% of the total SOC under different fertilization treatments in a 42 year long-term cropland fertilization in Hungary. In the present study, the average proportion of these fractions varied between 9.8–22.5% and 4.7–16.7% of the bulk soil SOC and TN across the three test sites (Fig. S1), which correspond fairly with their results. In addition, there was a clear increasing trend of the proportion of the amount of SOC and TN presenting in the cfPOC and cfPTN fraction under manure, chemical fertilization or straw return treatments at the three sites, and the maximum proportion increase was under manure (from 6.9 to 13.6% at GZL, 6.0 to 12.9% at ZZ and 5.3 to 19.6% at QY) (Fig. S1). The highest increase of SOC in the cfPOC fraction in our study confirmed that cfPOC was a good indicator for the change in SOC under fertilizations, especially under manure management (Figs. 2). Due to a larger organic C input through straw, the straw return treatment also generally increased SOC and TN in each fraction at ZZ and QY
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(except for the ffPOC and ffPTN at ZZ), but not at GZL except for an increase in ffPOC and ffPTN, compared with the control (Figs. 2 and 3). Compared to NPK, however, NPKS significantly decreased SOC in each fraction at GZL (Fig. 2a, b, c, d). These results indicated that the returned straw might have stimulated the original soil old C decomposition, and such decompositions could be offset by the new straw C amendment, hence the SOC accumulation was similar under the straw return and the control at GZL. Chemical fertilizer significantly increased SOC of cfPOC (57–197%), ffPOC (95–166%) and iPOC (26–65%), but had no effects on MOC at all
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three sites and on ffPOC at ZZ (Fig. 2). Meanwhile, the TN of the four fractions was all increased under NPK except iPTN and MTN at GZL (Fig. 3). In general iPOC was thought to be stored in aggregates to prevent from the decomposition of microorganisms. Chemical fertilizer contained a large amount of available N that could stimulate the growth of crop as well as the activities of microorganism that might enhance the decomposition of iPOC fraction (Liu et al., 2010). The balanced NPK fertilization might have a stronger stimulation effect on crop growth, which could return more residues to soil than on SOC decomposition and N loss, leading to an increased SOC and TN in the cfPOC, ffPOC or
Fig. 4. Relationships between soil organic carbon (SOC) and microbial biomass carbon (MBC) of the bulk soil, cfPOC, ffPOC, iPOC or MOC of each soil physical fraction; and between total nitrogen (TN) and microbial biomass nitrogen (MBN) of the bulk soil, cfPTN, ffPTN, iPTN or MTN of each soil aggregate fraction under three 17 years (1990–2007) long-term fertilization sites in China (**P b 0.01 and ***P b 0.001). See Fig. 1 for fertilization treatments and site abbreviations, see Figs. 2 and 3 for SOC and TN fractions.
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iPOC fraction. The organic C in the iPOC fraction across these three sites ranged 7.3 to 15.7% of the total SOC (Fig. S1), which were similar to a range of 7.3 to 12.0% observed by Sleutel et al. (2006). MOC was associated with mineral and mainly sequestrated in soil in the form of humus, and the SOC and TN in the MOC and MTN fractions held the largest proportion of the total SOC (63.2–81.4%) and TN (73.1–90.0%) (Fig. S1). Meanwhile, the C input under NPK might not form enough complex organic compounds associated with mineral, which accounted for the non-response of SOC in the MOC fraction under chemical fertilization (Tong et al., 2014). The increase of TN in the MTN fraction under NPK at ZZ and QY was more likely due to the residue return through a stimulating effect on crop growth, whereas an unchanged TN in both the iPTN and MTN fractions under NPK at GZL might be attributed to a large extent on a higher TN concentration in the bulk soil at GZL than at ZZ and QY. Generally, for the same fertilization at the same site, higher TN in fractions generally ranked as MTN N iPTN N cfPTN N ffPTN at the three sites (Fig. 3), while significantly higher SOC in fractions ranked as MOC N iPOC N cfPOC N ffPOC at GZL, MOC N cfPOC ≈ iPOC ≈ ffPOC at ZZ except in ffPOC at NPKM and 1.5NPKM, and MOC N cfPOC N iPOC N ffPOC at QY except under Control and NPKS (Fig. 2). In addition, for the same fertilization among these three sites, higher cfPOC or cfPTN patterned as QY N GZL N ZZ, while in the other three fractions as GZL N QY N ZZ (Figs. 2 and 3).
3.4. Relationships between SOC and TN with MBC, MBN or fraction organic C or N The SOC significantly positively correlated with MBC, cfPOC, ffPOC, iPOC and MOC (R2 = 0.51–0.84, P = 0.01–0.001, Fig. 4a, b, c, d and e), while the TN significantly positively correlated with cfPTN, ffPTN, iPTN and MTN (R2 = 0.45–0.79, P = 0.01–0.001, Fig. 4g, h, i and j) respectively, but not with MBN (Fig. 4f). This meant that both microbial biomass and physical fractions were the components of bulk soil and they could indicate long-term changes of SOM and TN due to fertilization treatments. Chung et al. (2008) found that the SOC of the MOC fraction did not linearly relate with the C input and that the MOC fraction exhibited a C saturation behavior, namely, MOC might not have potential to further sequestrate soil C in soil. The significantly positively linear relationship between the SOC or TN of each physical fractions and the total SOC or TN of the bulk soil in the present study demonstrated that all of these fractions were not saturated. As a result, a potential is plausible for each physical fraction to sequestrate more C and N under different fertilizer managements at these three tested soils. Meanwhile, SOC also significantly positively correlated with TN (Fig. 5a), and SOC in each fraction significantly positively correlated with TN in each fraction across all three sites (R2 = 0.52–0.96, P = 0.01–0.001, Fig. 5b, c, e and f). The C:N ratio significantly decreased in the order of ffPOC (15.1) N cfPOC (14.4) ≈ iPOC (14.2) N MOC (6.6).
Fig. 5. Relationships between soil organic carbon (SOC) and total nitrogen (TN), microbial biomass carbon (MBC) with microbial biomass nitrogen (MBN) of the bulk soil, and between SOC with TN of each physical fractions under three 17 years (1990–2007) long-term fertilization sites in China (**P b 0.01 and ***p b 0.001). See Fig. 1 for fertilization treatments and site abbreviations, see Figs. 2 and 3 for SOC and TN fractions.
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the variance of soil fertility (SOC, TN, MBC, MBN, SOC and TN in each fraction) in GZL (Fig. 6a), ZZ (Fig. 6b) and QY (Fig. 6c), respectively. Soil fertility under fertilizations with the addition of manure was clearly separated with that under the chemical fertilization at all three sites, while under straw return was similar to the control at GZL, to NPKM at ZZ and to NPK at QY, which was well confirmed in all abovementioned results in this study. 4. Conclusions Our results demonstrated that continuous 17 year applications of manure significantly increased SOC and TN concentrations, MBC, MBN, and the SOC and TN in soil physical fraction of cfPOC, ffPOC, iPOC and MOC at three cropland sites of China along a heat and water gradient. Straw return might also have similar effects on SOC, TN, MBC, MBN and the SOC and TN in each soil physical fraction like the manure application, except in the low temperature and humidity site of GZL in northeast of China. Chemical fertilization had showed relatively less effects on the total SOC and TN accumulation in the whole and each soil fraction. As a general rule, cfPOC was the most sensitive indicator to C changes and MOC, MTN was the main form that C and TN sequestrated in soil under long-term fertilizations. MBC, SOC and TN in aggregate fractions were significantly linearly correlated to total SOC and TN in the bulk soil. The overall PCA showed that manure fertilization was the best fertilization management strategy while straw return should be taken into account climate factors in cropland soils in China. Supplementary data to this article can be found online at http://dx. doi.org/10.1016/j.scitotenv.2015.06.011. Acknowledgments We acknowledge our colleagues for their unremitting efforts to the long-term experiments. Financial support was from the National Natural Science Foundation of China (41371247) and National Basic Research Program of China (2011CB100501). References
Fig. 6. Principal component analyses of soil fertility under three 17 years (1990–2007) long-term fertilization sites in China. See Fig. 1 for fertilization treatments and site abbreviations.
The C:N ratio is indicative of the capacity of a soil to store and recycle nutrients. In general, soil C:N ratio decreases with increasing of degradation and humification of organic matter. As a decomposition proceeds, C is released during respiration and some of the mineralized N is lost through leaching or gaseous emissions while some other parts of mineralized N is reincorporated into the SOM pool (Chapin et al., 2002). The decrease of C:N ratio in the four fractions in this study indicates that MOC was most humified, and N was more stored than C in this fraction, which also showed the procession of SOC accumulation and sequestration in soil. Principal components analyses (PCA) showed that overall the principal components (PC1 and PC2) explained 86.9%, 89.6% and 91.2% of
Böhme, L., Langer, U., Böhme, F., 2005. Microbial biomass, enzyme activities and microbial community structure in two European long-term field experiments. Agric. Ecosyst. Environ. 109, 141–152. Blair, N., Faulkner, R., Till, A., Poulton, P., 2006. Long-term management impacts on soil C, N and physical fertility: part I: Broadbalk experiment. Soil Tillage Res. 91, 30–38. Cai, Z., Wang, B., Xu, M., Zhang, H., He, X., Zhang, L., Gao, S., 2014. Intensified soil acidification from chemical N fertilization and prevention by manure in an 18-year field experiment in the red soil of southern China. J. Soils Sediments 15, 260–270. Campbell, C., Janzen, H., Juma, N., 1997. Case studies of soil quality in the Canadian Prairies: long-term field experiments. Dev. Soil Sci. 25, 351–398. Chapin, F.S., Matson, P.A., Mooney, H.A., 2002. Principles of terrestrial ecosystem ecology. Springer, New York. Chung, H.G., Grove, J.H., Six, J., 2008. Indications for soil carbon saturation in a temperate agroecosystem. Soil Sci. Soc. Am. J. 72, 1132–1139. Compton, J.E., Boone, R.D., 2002. Soil nitrogen transformations and the role of light fraction organic matter in forest soils. Soil Biol. Biochem. 34, 933–943. Courtier-Murias, D., Simpson, A.J., Marzadori, C., Baldoni, G., Ciavatta, C., Fernandez, J.M., Lopez-De-Sa, E.G., Plaza, C., 2013. Unraveling the long-term stabilization mechanisms of organic materials in soils by physical fractionation and NMR spectroscopy. Agric. Ecosyst. Environ. 171, 9–18. Dormaar, J., Lindwall, C., Kozub, G., 1988. Effectiveness of manure and commercial fertilizer in restoring productivity of an artificially eroded Dark Brown Chernozemic soil under dryland conditions. Can. J. Soil Sci. 68, 669–679. Gale, W., Cambardella, C., Bailey, T., 2000. Surface residue- and root-derived carbon in stable and unstable aggregates. Soil Sci. Soc. Am. J. 64, 196–201. Giacometti, C., Demyan, M.S., Cavani, L., Marzadori, C., Ciavatta, C., Kandeler, E., 2013. Chemical and microbiological soil quality indicators and their potential to differentiate fertilization regimes in temperate agroecosystems. Appl. Soil Ecol. 64, 32–48. Giacometti, C., Cavani, L., Baldoni, G., Ciavatta, C., Marzadori, C., Kandeler, E., 2014. Microplate-scale fluorometric soil enzyme assays as tools to assess soil quality in a long-term agricultural field experiment. Appl. Soil Ecol. 75, 80–85. Hart, S.C., Nason, G.E., Myrold, D.D., Perry, D.A., 1994. Dynamics of gross nitrogen transformations in an old-growth forest: the carbon connection. Ecology 75, 880–891. He, Y., Qi, Y., Dong, Y., Xiao, S., Peng, Q., Liu, X., Sun, L., 2013. Effects of nitrogen fertilization on soil microbial biomass and community functional diversity in temperate grassland in Inner Mongolia, China. Clean Soil Air Water 41, 1216–1221.
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Y.T. He et al. / Science of the Total Environment 532 (2015) 635–644
Ju, X.T., Xing, G.X., Chen, X.P., Zhang, S.L., Zhang, L.J., Liu, X.J., Cui, Z.L., Yin, B., Christie, P., Zhu, Z.L., 2009. Reducing environmental risk by improving N management in intensive Chinese agricultural systems. Proc. Natl. Acad. Sci. 106, 3041–3046. Liang, Q., Chen, H., Gong, Y., Fan, M., Yang, H., Lal, R., Kuzyakov, Y., 2012. Effects of 15 years of manure and inorganic fertilizers on soil organic carbon fractions in a wheat–maize system in the North China Plain. Nutr. Cycl. Agroecosyst. 92, 21–33. Liu, H., Tong, X.G., Xu, Y.M., Ma, X.W., Wang, X.H., Zhang, W.J., Xu, M.G., 2010. Evolution characteristics of organic carbon fractions in gray desert soil under long-term fertilization. Plant Nutr. Fertil. Sci. 16, 794–800. Manna, M., Swarup, A., Wanjari, R., Singh, Y., Ghosh, P., Singh, K., Tripathi, A., Saha, M., 2006. Soil organic matter in a West Bengal Inceptisol after 30 years of multiple cropping and fertilization. Soil Sci. Soc. Am. J. 70, 121–129. Purakayastha, T., Rudrappa, L., Singh, D., Swarup, A., Bhadraray, S., 2008. Long-term impact of fertilizers on soil organic carbon pools and sequestration rates in maize– wheat–cowpea cropping system. Geoderma 144, 370–378. Reeves, D., 1997. The role of soil organic matter in maintaining soil quality in continuous cropping systems. Soil Tillage Res. 43, 131–167. Sarathchandra, S.U., Ghani, A., Yeates, G.W., Burch, G., Cox, N.R., 2001. Effect of nitrogen and phosphate fertilisers on microbial and nematode diversity in pasture soils. Soil Biol. Biochem. 33, 953–964. Six, J., Elliott, E., Paustian, K., 2000. Soil macroaggregate turnover and microaggregate formation: a mechanism for C sequestration under no-tillage agriculture. Soil Biol. Biochem. 32, 2099–2103.
Six, J., Callewaert, P., Lenders, S., De Gryze, S., Morris, S., Gregorich, E., Paul, E., Paustian, K., 2002. Measuring and understanding carbon storage in afforested soils by physical fractionation. Soil Sci. Soc. Am. J. 66, 1981–1987. Sleutel, S., De Neve, S., Nemeth, T., Toth, T., Hofman, G., 2006. Effect of manure and fertilizer application on the distribution of organic carbon in different soil fractions in long-term field experiments. Eur. J. Agron. 25, 280–288. Sun, H., Deng, S., Raun, W., 2004. Bacterial community structure and diversity in a century-old manure-treated agroecosystem. Appl. Environ. Microbiol. 70, 5868–5874. Tong, X.G., Xu, M.G., Wang, X.J., Bhattacharyya, R., Zhang, W.J., Cong, R.H., 2014. Longterm fertilization effects on organic carbon fractions in a red soil of China. Catena 113, 251–259. Tu, C., Ristaino, J.B., Hu, S., 2006. Soil microbial biomass and activity in organic tomato farming systems: effects of organic inputs and straw mulching. Soil Biol. Biochem. 38, 247–255. Vance, E.D., Brookes, P.C., Jenkinson, D.S., 1987. An extraction method for measuring soil microbial biomass C. Soil Biol. Biochem. 19, 703–707. Zhong, W.H., Cai, Z.C., 2007. Long-term effects of inorganic fertilizers on microbial biomass and community functional diversity in a paddy soil derived from quaternary red clay. Appl. Soil Ecol. 36, 84–91.
