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Effect of Long-Term Rice Straw Return on Soil Glomalin, Carbon and Nitrogen1
Pedosphere 17(3): 295-302, 2007 ISSN 1002-0160/CN 32-1315/P @ 2007 Soil Science Society of China Published by Elsevier Limited and Science Press
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Effect of Long-Term Rice Straw Return on Soil Glomalin, Carbon and Nitrogen*' NIE J u n l ~ ~ZHOU , ~ , Jian-Min'>*', WANG Huo-Yan', CHEN Xiao-Qin' and DU Chang-Wen' Institute of Soil Science, Chinese Academy of Sciences, Nanjing 21 0008 (China). E-mail: [email protected]. cn 2Soil and Fertilizer Institute of Hunan, Changsha 410125 (China) Graduate University of Chinese Academy of Sciences, Beijing 100049 (China) (Received August 26, 2006; revised January 16, 2007)
ABSTRACT A long-term experiment was conducted to investigate how long-term fertilization and rice straw incorporation into soil affect soil glomalin, C and N. The combined application of chemical fertilizer and straw resulted in a significant increase in both soil easily extractable glomalin (EEG) and total glomalin (TG) concentrations, as compared with application of only chemical fertilizer or no fertilizer application. The EEG and TG concentrations of the NPKS (nitrogen, phosphorus, and potassium fertilizer application rice straw return) plot were 4.68% and 5.67% higher than those of the CK (unfertilized control) plot, and 9.87% and 6.23% higher than those of the NPK (nitrogen, phosphorus, and potassium fertilizer applied annually) plot, respectively. Application of only chemical fertilizer did not cause a statistically significant change of soil glomalin compared with no fertilizer application. The changes of soil organic C (SOC) and total N ( T N ) contents demonstrated a similar trend to soil glomalin in these plots. The SOC and TN contents of NPKS plot were 15.01% and 9.18% higher than those of the CK plot, and 8.85% and 14.76% higher than those of the NPK plot, respectively. Rice straw return also enhanced the contents of microbial biomass C (MBC) and microbial biomass N (MBN) in the NPKS plot by 7.76% for MBC and 31.42% for MBN compared with the CK plot, and 12.66% for MBC and 15.07% for MBN compared with the NPK plots, respectively. Application of only chemical fertilizer, however, increased MBN concentration, but decreased MBC concentration in soil.
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Key Words:
C, glomalin, long-term fertilizer experiment, N, rice straw return
Citation: Nie, J., Zhou, J . M., Wang, €1. Y., Chen, X. Q. and Du, C. W. 2007. Effect of long-term rice straw return on soil glomalin, carbon and nitrogen. Pedosphere. 17(3): 295-302.
INTRODUCTION Arbuscular mycorrhizal fungi (AMF) are ubiquitous root symbiotic fungi that are closely associated with host plants, including major food crops (wheat, corn, sorghum, etc.) and pasture plants. AMF play a significant role in the soil environment, function as an extension of the root system into the soil, and have numerous effects on plant physiology and plant communities (Allen, 1991; Smith and Read, 1997; Gai et al., 2005). Their effects on soil structure, water retention capacity, and nutrient cycling are of critical importance t o the maintenance of soil function in both natural and cultivated ecosystems. Recent studies indicated that hyphae of AMF play an important role in soil aggregation (Miller and Jastrow, 1990; Tisdall, 1991; Jastrow et al., 1998). Recently, glomalin, a glycoprotein, produced by AMF has been detected. Glomalin can be extracted from the hyphae of all the isolates of AMF examined to date (Wright et al., 1996; Rillig and Steinberg, 2002), and glomalin was secreted into soil through turnover of AMF. Glomalin in soil is characterized as follows: insoluble in water, but can be solubilized by 20 or 50 mmol L-l citrate at 121 "C (Wright et al., 1996); highly correlated with soil C and N (Rillig et al., 2001); sequesters potentially toxic elements in soil (Gonzalez-Chavez et al., 2004); linked with an oligosaccharide (Wright et al., 1998); strongly *'Project supported by the National Key Basic Research Support Foundation of China (No. 2002CB410810). *2Corresponding author. E-mail: [email protected].
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positively correlated with soil aggregate stability (Wright and Updhyaya, 1998; Rillig, 2004); and has a relatively long lifespan in soil (Rillig e t al., 2003; Steinberg and Rillig, 2003). Moreover, the effect of glomalin on soil aggregation is stronger than that of AMF (Driver et al., 2005) because glomalin acts as an insoluble glue for the stabilization of aggregates (Wright and Updhyaya, 1996, 1998). Furthermore, there is abundant glomalin in natural and cultivated soil, and the concentration of glomalin in soil ranges from 4.4 to 14.8 mg g-' soil (Wright et al., 1996). Land management practices, such as fertilization, tillage, and irrigation, have a significant impact on soil chemical, physical, and biological properties. For example, soil glomalin concentration responded to land use change (Rillig e t al., 2003), tillage practices (Wright et al., 1999), and crop rotation (Wright and Anderson, 2000). Fertilization is perhaps the most important practice that affects chemical, physical, biological, and biochemical properties of soil (Zhang e t al., 2005), but there is little understanding about the effect of fertilization on soil glomalin concentration. Rice is one of the most important crops in China, and the seeded area reached 2.65 x lo7 ha. The annual production amounted t o 1.61 x lo5 Mg in 2003 (Editorial Committee of China Agriculture Yearbook, 2004). As a by-product, the annual rice straw production also amounted to 1.72 x lo5 Mg, and increased with the breeding and wide use of high-yielding rice varieties. Rice straw is not only an agricultural residue, but also an important fertilizer resource. Rice straw return into soil is a common practice in China. Rice straw supplies abundant nitrogen, phosphate, potassium, and other essential nutrient elements to plants (Wang et al., 2005), and rice straw return into soil can improve physical-chemical and biological properties of soil and thereby enhance soil fertility. It has been reported that rice straw plays a significant role in maintaining soil fertility (Lu et al., 2005; Wang e t al., 2003) and microbial biomass communities (Chilima et aL, 2002). This has become an important aspect of sustaining long-term fertility in cropping systems. However, little is known about the effects of chemical fertilizer application and the combined application of chemical fertilizer and rice straw on soil glomalin concentration. The objective of this study was to investigate glomalin, organic carbon (OC), total N (TN), microbial biomass C (MBC), and microbial biomass N (MBN) concentrations in response to longterm chemical fertilizer application and the application of chemical fertilizer in combination with rice straw return into soil. MATERIALS AND METHODS Site description
A long-term field experiment was initiated in 1981 at the Key Field Monitoring Experimental Station for Reddish Paddy Soil Eco-environment in Wangcheng, Ministry of Agriculture of China. The station is located in Huangjin Village Town (112' 80' N, 28' 37' E, 100 m altitude), Wangcheng County of Hunan Province in the central region of the Xiangjiang River (a branch of Dongting Lake), China. The climate of this area is subtropical monsoonal climate. Average annual precipitation is approximately 1370 mm and annual mean temperature is 17 ' C , with the lowest monthly temperature of 4.4 "C in January and the highest monthly temperature of 30 "C in July. The annual frost-free period is approximately 300 d. The soil is a Fe-accumuli-Stagnic Anthrosols derived from Quaternary red clay (clay loam). On the basis of the analysis of soil samples taken from the experimental site on October 1981, the characteristics of the top soil (15 cm) were: pH 6.9; soil organic matter (SOM) 35.5 g kg-', total N (N) 2.05 g kg-l, hydrolysable N 151.0 mg kg-', available P 10.2 mg kg-', and exchangeable K 62.3 mg kg-'.
Experimental design and treatments The cropping system of this area comprised cropping of early rice and late rice each year. Each experimental plot was 6.67 m wide by 10 m long. Three fertilization treatments were arranged in a randomized complete block design with three replications. The treatments were: 1) CK, unfertilized control; 2) NPK, nitrogen, phosphorus, and potassium fertilizer applied annually; 3) NPKS, straw (S)
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and same fertilization in NPK. Adjacent plots were separated by concrete ridges (30 cm width), and the blocks were separated by irrigation furrows (50 cm width) and two ridges (30 cm width). The inorganic fertilizer sources of N, P, and K in three treatments were commercial fertilizers such as urea, single super phosphate, and potassium chloride. The analysis of nutrients of rice straw varied from one year to another, but on the average, rice straw contained 8.6 g kg-l total N, 3.0 g kg-I total PzO5, and 25.0 g kg-l total KzO. Nitrogen fertilizer was applied at 150 kg N ha-' t o early rice and 180 kg N ha-' to late rice during 1981-2005. Phosphate fertilizer was applied at 75 kg-' PzO5 ha-l to both early rice and late rice during 1981-1990, and 60 kg P205 ha-' to both early rice and late rice from 1991 to 2005, respectively. Potassium fertilizer was applied at 120 kg KzO ha-l to both early rice and late rice during 1981-2005. Rice straw was applied at 2.62 t ha-' to both early and late rice.
Soil samples and analyses Soil samples were collected in March 2005 to a depth of 15 cm before early rice was transplanted. Each sample was a composite mixture of 10 cores that were randomly selected using a 2.4-cm diameter soil corer. The samples were taken from within areas (6 m x 9 m) to avoid inclusion of the additional factor. SOC and T N were determined in air-dried soil (< 180 pm) using a C/N/S-analyzer (Vario MAX). MBC and MBN were determined on a field moist soil sample (< 2 mm) by chloroform-fumigationextraction method as described by Vance et al. (1987), using 0.5 mol L-l K2S04 as an extractant. Organic C and N from the fumigated (24 h) and nonfumigated (control) soil were quantified by a TOC analyzer (Phoenix 8000) and a flow injection analyzer (FIAstar 5000), respectively. The nonfumigated control values were subtracted from the fumigated values. The MBC and MBN were calculated by dividing the differences of C and N contents in the non-fumigated and the fumigated soil samples with conversion factors of 0.45 (Wu et al., 1990) and 0.54 (Jenkinson, 1988), respectively. Each sample was subjected to three analyses, and results were expressed without considering the moisture factor. Soil moisture was determined after drying at 105 "C for 48 h.
Glomalin extraction methods Glomalin extractions from soil were carried out as described by Wright and Upadahyaya (1996). Before the glomalin was extracted, aggregates were analyzed after the soil samples were stored for 3 months using the method and apparatus described by Kemper and Rosenau (1986). Then replicate containing 1 g of soil samples of 1-2-mm aggregates were extracted with 8 mL of extiactant. The easily extractable glomalin (EEG) fraction was extracted with 20 mmol L-l sodium citrate (pH 7.0) at 121 " C for 30 min. Samples were centrifuged at 10000 x g for 5 min immediately after extraction, and the supernatant containing the extracted protein was removed for analysis. The total glomalin (TG) fraction was extracted with 50 mmol L-l sodium citrate (pH 8.0) at 121 "C for 60 min, and then immediately centrifuged at 10000 x g for 5 min. After each cycle, the supernatant was removed and sodium citrate was replenished for the extraction of glomalin again until the supernatant showed no red-brown color, which is typical for glomalin. The supernatant was stored for analysis. Both fractions were analyzed using the Bradford protein assay, which utilizes an acidic solution of Coomassie brilliant blue G-250 dye to bind to amino acid residues of protein. Bovine serum albumin was used to prepare as the standard for the assay.
Statistical analyses Statistical analyses were performed with SPSS10. Standard analysis of variance techniques were used to analyze the effects of treatments. The main significant effects were separated by the least significant difference test.
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RESULTS AND DISCUSSION Easily extractable glomalin and total glomalin concentration The results in Fig.1 showed that fertilizers with rice straw increased the concentrations of easily extractable glomalin (EEG) and total glomalin (TG) in soil. The EEG concentrations were significantly influenced by different fertilizations ( F = 14.548; P = 0.005), and the EEG concentrations of NPKS plot were higher than those of CK plot by 4.68% and NPK plot by 9.87%. Similarly, soil TG concentrations were also significantly affected by different fertilizations ( F = 9.848; P = 0.013), and the TG concentrations of NPKS plot were higher than those of CK plot by 5.67% and NPK plot by 6.23%. Furthermore, the results indicated that soil EEG and TG concentrations of NPK plot were actually lower than those of CK plot, although the difference was not statistically significant.
Fig. 1 Effect of long-term fertilizer application o n easily extractable glomalin (EEG) and total glomalin (TG) in soil. CK = no fertilizer application; NPK = nitrogen, phosphorus, and potassium fertilizer application; NPKS = nitrogen, phosphorus, and potassium fertilizer application rice straw return. Error bars indicate standard deviations of the means (n = 3).
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Many reports have been published on soil glomalin concentrations in natural and agricultural ecosystern affected by different plants (Rillig et al., 2002), land use change (Rillig et al., 2003), and alternative crop rotations (Wright and Anderson 2000). Unlike most known AMF that are nonhost specific, Bever et al. (1996) discovered a preferential association of mycobionts with certain host plants. They believed that different host plants were colonized by different subsets of the AMF community, which enhanced soil glomalin concentrations in response to plants, land use change, and crop rotation. The results of this study from the same field and on the same host plant (rice) showed that the soil glomalin concentrations varied significantly in different fertilization plots. While the NPKS treatment increased soil glomalin concentration, chemical fertilizer application without straw did not increase soil glomalin concentration. This might be partially responsible for the increase of soil rigidity after long-term chemical fertilizer application in agricultural soils. Therefore, to maintain soil structure and promote sustainable agriculture and thereby to improve soil quality, the combined application of chemical fertilizer arid rice straw or organic manure should be adopted in cultivated soil.
Soil organic C and total N Soil organic matter (SOM) or soil organic carbon (SOC) is considered to be a key attribute of soil quality because it is one of the important physical and biological properties of soil (Yang et al., 2005). In this study, the averages of SOC concentration were significantly different among the treatments ( F = 9.360; P = 0.014). The SOC concentration in NPKS plot was higher than that in NPK by 15.01% and CK plot by 8.85% (Fig.2). Compared with CK plot, the application of only chemical fertilizer application (NPK plot) lowered SOC, but the difference was not significant. Similarly, the
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averages of T N concentrations also reached statistically significant level ( F = 11.146; P = 0,010). The TN concentration in NPKS plot was 2.65 mg g-' and was significantly higher than that in CK plot by 9.18% and NPK plot by 14.76%; however, there were no significant difference of total N between CK and NPK plots. These results were in agreement with other reports (Jenkinson and Ryner, 1977; Nel et al., 1996; Aref and Wander, 1998), wherein they discovered that long-term fertilizer application resulted in loss of soil organic matter and total N. Therefore, straw return in soil perhaps is a good practice to maintain soil fertility and improve productivity. 25
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Fig. 2 Effect of long-term fertilizer application on organic C (OC) and total N (TN) in soil. CK = no fertilizer application; NPK = nitrogen, phosphorus, and potassium fertilizer application; NPKS = nitrogen, phosphorus, and potassium fertilizer application rice straw return. Error bars indicate standard deviations of the means ( n = 3).
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Wright and Upadhyaya (1998) postulated that EEG and TG in soil were highly correlated with soil C and N (Rillig et al., 2003). In this study, because the range of treatments was not large enough, no correlation was found between soil EEG or TG concentration and soil organic C or total N concentration. Nevertheless, the changes of SOC and T N in different plots demonstrated a similar trend with regard to the changes of soil EEG and TG. Therefore, fertilization with straw may be an effective agricultural practice that can enhance the formation and concentration of soil glomalin. Soil microbial biomass C and microbial biomass N
Soil microbial biomass C (MBC) is the active component in soil organic matter. The change of MBC reflects the process of microorganism propagation and degradation utilizing soil carbon. Fig. 3 indicated that application of only chemical fertilizer resulted in little decrease in MBC concentration in the surface layer (0-15 cm) compared to that of CK plot. MBC in the CK plot was higher than that in the NPK plot by 4.55%. Whereas, the combined application of chemical fertilizer and straw significantly
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Fig. 3 Effect of long-term fertilizer application on microbial biomass C (MBC) and microbial biomass N (MBN) in soil. CK = no fertilizer application; NPK = nitrogen, phosphorus, and potassium fertilizer application; NPKS = nitrogen, phosphorus, and potassium fertilizer application ( n = 3).
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increased soil MBC concentration by 7.76% compared t o that of CK plot and 12.66% compared to that of NPK plot. The statistical analysis indicated that the difference of MBC among different treatment plots reached a significant level ( F = 36.953; P < 0.001). The results (Fig. 3) indicated that different fertilizations in this experiment evidently affected soil microbial biomass N (MBN) ( F = 9.880; P = 0.013). The MBN concentrations in NPK and NPKS plots were significantly higher than those in CK plots, representing an increase of 14.25% and 31.42%, respectively. The results also showed that the combined application of chemical fertilizer and straw significantly enhanced soil MBN by another 15.07% over the NPK plot. Soil MBC and MBN concentrations were determined by the addition of organic matter nitrogen fertilizer. Because there was no organic matter or nitrogen fertilizer inputs for 25 years in the CK plot, the soil might not have enough C and N resources for the propagation of microbes, resulting in low soil MBC and MBN. The results also suggested that rice straw return into soil could obviously promote soil microbe breed and thereby enhance soil MBC and MBN concentrations. The reason for a low MBC concentration in NPK plot compared to that in the CK plot may be explained by increased degradation rate of soil organic matter caused by N application in NPK plot, and the higher yield resulted in enhanced formation of soil C.
Ratios of MBC:TC, MBN:TN, MBC:MBN, and S 0 C : T N The ratio of MBC:MBN can reflect the effect of different treatments on soil microbial biomass and microbial community structure. The results indicated that there was no obvious difference in the ratios of MBC:SOC and MBN:TN among the three different fertilizers plots (Table I). The ratio of MBN:TN in NPK and NPKS plots was 19.85% and 20.22% higher than that in the CK plot, respectively, whereas the ratio of MBC:MBN in CK plot was significantly higher than that in NPK and NPKS plots by 19.47% and 22.04%, respectively. TABLE I Ratios of microbial biomass C (MBC):organic C (OC), microbial biomass N (MBN):total N (TN), MBC:MBN, and 0C:TN in soils under different treatments Treat m e i t a)
MBC:OC
MBN:TN
MBC:MBN
0C:TN
CK NPK NPKS
0.0351aAb) 0.0355aA 0.0348aA
0.0272aA 0.0326bA 0.0327bA
11.3465aA 9.5024bAB 9.3035bB
8.7857aA 8.7399aA 8.7592aA
CK = no fertilizer application; NPK = nitrogen, phosphorus, and potassium fertilizer application; NPKS = nitrogen, rice straw return. phosphorus, and potassium fertilizer application b)Values followed by the same letter (lowercase for P < 0.05 and uppercase for P < 0.01) within a column were not significantly different.
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The percentage change of MBC in SOC may be related t o organic matter formation, and the efficiency of conversion of recalcitrant C into MBC (Sparling, 1992). It can be an indicator of whether soil organic matter is decreasing, increasing, or in a steady state (Anderson and Domsch, 1989; Insam, 1990). The results of this study indicated that long-term chemical fertilizer applications or the combined application of chemical fertilizer and straw had no obvious effect on soil organic matter formation and degradation. Jenkinson and Ladd (1981) suggested 2.2% as a threshold value for whether a soil was in equilibrium. The results showed values much higher than this threshold. Generally, if a soil is intensively disturbed, MBC will decline faster than the organic matter, and the percentage of total C also decreases with the decrease in MBC (Powlson and Jenkinson, 1981; Sparling, 1992). The results of this study suggested that the ratio of MBC to total C under cultivation conditions for paddy soil could be regarded as an indicator of C accumulation in subtropical regions. The sole application of chemical fertilizers or the combined application of chemical fertilizers with rice straw significantly reduced the ratio of MBC:MBN by increasing the N concentration in microbe
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and decreasing C concentration. CONCLUSIONS Application of only chemical fertilizer had little impact on soil glomalin concentration, whereas the combined application of fertilization and rice straw significantly raised soil glomalin concentration. The changes of soil organic C and total N showed a similar trend to the changes of soil glomalin concentration caused by continuous fertilizer applications for 25 years. Straw return in soil may be one of the most important practices in raising soil glomalin concentration. The combined application of chemical fertilizer and rice straw significantly increased soil MBC and MBN concentrations compared with the application of only chemical fertilizer, which enhanced soil MBN but decreased soil MBC. There was no obvious difference in the ratios of MBC:SOC and S0C:TN among the three plots. Nevertheless, with no fertilizer application, the ratio of MBN:TN decreased, whereas the MBC:MBN ratio increased, implying that fertilization may be related to soil N accumulation. REFERENCES Allen, M. F. 1991. The Ecology of Mycorrhizae. Cambridge University Press, Cambridge. 184pp. Anderson, T. H. and Domsch, K. H. 1989. Ratios of microbial biomass carbon t o total organic carbon in arable soils. Soil Biol. Biochem. 21: 471-479. Aref, S. and Wander, M. M. 1998. Long-term trends of corn yield and soil organic matter in different crop sequences and soil fertility treatments on the Morrow Plots. Advance in Agronomy. 62: 153-161. Bever, J . D., Morton, 3. B., Antonovics, J. and Schultz, P. A. 1996. Host-dependent sporulation and species diversity of aarbuscular mycorrhizal fungi in a mown grassland. J. Ecol. 84: 71-82. Chilima, J., Huang, C. and Wu, C. 2002. Microbial biomass carbon trends in black and red soils under single straw application: Effect of straw placement, mineral N addition and tillage. Pedosphere. 12: 59-72. Driver, J . D., Holben, W. E. and Rillig, M. C. 2005. Characterization of glomalin as a hyphal wall component of arbuscular mycorrhizal fungi. Soil Biol. Biochem. 37: 101-106. Editorial Committee of China Agriculture Yearbook. 2004. China Agriculture Yearbook (in Chinese). Chinese Agriculture Press, Beijing. 133pp. Gai, J. P., Feng, G. G and Li, X. L. 2005. Review of researches on biodiversity of arbuscular mycorrhizal fungi. Soils (in Chinese). 37: 236-242. Gonzalez-Chavez, M. C., Carrillo-Gonzalez, R., Wright, S . F. and Nichols, K. A. 2004. The role of glomalin, a protein produced by arbuscular mycorrhizal fungi, in sequestering potentially toxic elements. Environmental Pollution. 130: 317-323. Insam, H. 1990. Are the soil microbial biomass and basal respiration governed by the climatic regime? Soil Biol. Biochern. 22: 525-532. Jastrow, J . D., Miller, R. M. and Lussenhop, J. 1998. Contribution of interacting biological mechanisms to soil aggregate stabilization in restored prairie. Soil Biol. Biochem. 30: 905-916. Jenkinson, D. S. 1988. Determination of microbial biomass carbon and nitrogen in soil. In Wilson, J . R. (ed.) Advances in Nitrogen Cycling in Agricultural Ecosystems. Marcel dekker, New Youk. pp. 368-386. Jenkinson, D. S. and Ladd, J. N. 1981. Microbial biomass in soil: Measurement and turnover. In Paul, E. A. and Ladd, J. M. (eds.) Soil Biochemistry. Vol. 5. Marcel Decker, New York. pp. 415-471. Jenkinson, D. S. and Rayner, J. H. 1977. The turnover of soil organic matter in some of the Rothamsted classical experiments. Soil Sci. 125: 298-305. Kemper, W.D. and Rosenau, R. C. 1986. Aggregate stability and size distribution. In Klute, A. and Page, A. L. (eds.) Methods of Soil Analysis. Part 1. Physical and Mineralogical Methods. American Society of Agronomy, Madison, WI. pp. 425-442. Lu, B., &in, J. H and Zhao, Y. C. 2005. Effect of wheat straw mulching on soil fertility and crop production on salinealkaline soil. Soils (in Chinese). 37: 52-55. Miller, R. M. and Jastrow, J . D. 1990. Hierarchy of root and mycorrhizal fungal interactions with soil aggregation. Soil Biol. Biochem. 22: 579-584. Nel, P. C., Barnard, R. O., Steynberg, R. E., De Beer, J. M. and Groeneveld, H. T. 1996. Trends in maize grain yields in a long-term fertilizer trial. Field Crops Res. 47: 53-64. Powlson, D. S. and Jenkinson, D. S. 1981. A comparison of the organic matter, biomass, adenosine triphosphate and mineralizable nitrogen contents of ploughed and direct-drilled soils. J . Agric. Sci. 97: 713-721. Rillig, M. C. 2004. Arbuscular mycorrhizae, glomalin, and soil aggregation. Can. J . Soil. Sci. 84: 355-363.
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J . NIE et al.
Rillig, M. C. and Steinberg, P. D. 2002. Glomalin production by an arbuscular mycorrhizal fungus: A mechanism of habitat modification? Soil Biol. Biochem. 34: 1371-1 374. Rillig, M. C., Ramsey, P. W., Morris, S . and Paul, E. A. 2003. Glomalin, an arbuscular-mycorrhizal fungal soil protein, responds to land-use change. Plant and Soil. 253: 293-299. Rillig, M. C., Wright, S. F. and Eviner, V. 2002. The role of arbuscular mycorrhizal fungi and glomalin in soil aggregation: Comparing effects of five plant spacies. Plant and Soil. 238: 325-333. Rillig, M. C., Wright, S. F., Nichols, K. A., Schmidt, W. F. and Torn, M. S. 2001. Large contribution of arbuscular mycorrhizal fungi to soil carbon pools in tropical forest soils. Plant and Soil. 233: 167-177. Smith, S . E. and Read, D. J. 1997. Mycorrhizae Symbiosis. Academic Press, San Diego, CA. Sparling, G. P. 1992. Ratio of microbial biomass carbon to soil organic carbon as a sensitive indicator of changes in soil organic matter. Aust. J. Soil Res. 30: 195-207. Steinberg, P. D. and Rillig, M. C. 2003. Differential decomposition of arbuscular mycorrhizal fungal hyphae and glomalin. Soil Biol. Bzochem. 35: 191-194. Tisdall, J. M. 1991. Fungal hyphae and structural stability of soil. Aust. J . Soil Res. 29: 729-743. Vance, E. D., Brookes, P. C. and Jenkinson, D. S. 1987. An extraction method for measuring soil microbial biomass C. Soil Biol. Biochem. 19: 703-707. Wang, X.D., Shi, X. J. and Song, G. Y. 2005. Effects of long-term rice straw returning on the fertility and productivity of purplish paddy soil. Plant Nutrition and Fertilizer Science (in Chinese). 11: 302-307. Wang, Z. M., Zhu, P. L., Huang, D. M and Liu, H. Q. 2003. Straw carbon decomposition in situ in field and characteristics of soil biomass carbon turnover. Acta Pedologica Sinica (in Chinese). 40: 446-453. Wright, S. F. and Anderson, R. L. 2000. Aggregate stability and glomalin in alternative crop rotations for the central Great Plains. Biol. Fert. of Soils. 31: 249-253. Wright, S. F., Franke-Snyder, M., Morton, J. B. and Upadhyaya, A. 1996. Time-course study and partial characterization of a protein on hyphae of arbuscular mycorrhizal fungi during active colonization of roots. Plant and Soil. 181: 193-203. Wright, S. F., Starr, J. L. and Paltineanu, I. C. 1999. Changes in aggregate stability and concentration of glomalin during tillage management transition. Soil Sci. SOC. Am. J. 63: 1825-1 829. Wright, S. F. and Upadhyaya, A. 1996. Extraction of an abundant and unusual protein from soil and comparison with hyphal protein of arbuscular mycorrhizal fungi. Soil Sci. 161: 575-586. Wright, S. F., and Upadhyaya, A. 1998. A survey of soils for aggregate stability and glomalin, a glycoprotein produced by hyphae of arbuscular mycorrhizal fungi. Plant and Soil. 198: 97-107. Wright, S. F., Upadhyaya, A. and Buyer, J. S. 1998. Comparison of N-linked oligosaccharides of glomalin from arbuscular mycorrhizal fungi and soils by capillary electrophoresis. Soil Biol. Biochem. 30: 1 853-1 857. Wu, J., Joergensen, R. G., Pommerening, B., Chaussod, R. and Brookes, P. C. 1990. Measurement of soil microbial biomass by fumigation-extraction-An automated procedure. Soil Biol. Biochem. 22: 1167-1 169. Yang, C. M., Yang, L. Z. and Yan, T. M. 2005. Chemical and microbiological parameters of paddy soil quality as affected by different nutrient and water regimes. Pedosphere. 15: 369-378. Zhang, Q . C . , Wang, G. H. and Fang, B. 2005. Influence of fertilization treatment on nutrients uptake by rice and soil ecological characteristics of soil microorganism in paddy field. Acta Pedologica Sinica (in Chinese). 42: 116-121.
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Effect of Long-Term Rice Straw Return on Soil Glomalin, Carbon and Nitrogen*' NIE J u n l ~ ~ZHOU , ~ , Jian-Min'>*', WANG Huo-Yan', CHEN Xiao-Qin' and DU Chang-Wen' Institute of Soil Science, Chinese Academy of Sciences, Nanjing 21 0008 (China). E-mail: [email protected]. cn 2Soil and Fertilizer Institute of Hunan, Changsha 410125 (China) Graduate University of Chinese Academy of Sciences, Beijing 100049 (China) (Received August 26, 2006; revised January 16, 2007)
ABSTRACT A long-term experiment was conducted to investigate how long-term fertilization and rice straw incorporation into soil affect soil glomalin, C and N. The combined application of chemical fertilizer and straw resulted in a significant increase in both soil easily extractable glomalin (EEG) and total glomalin (TG) concentrations, as compared with application of only chemical fertilizer or no fertilizer application. The EEG and TG concentrations of the NPKS (nitrogen, phosphorus, and potassium fertilizer application rice straw return) plot were 4.68% and 5.67% higher than those of the CK (unfertilized control) plot, and 9.87% and 6.23% higher than those of the NPK (nitrogen, phosphorus, and potassium fertilizer applied annually) plot, respectively. Application of only chemical fertilizer did not cause a statistically significant change of soil glomalin compared with no fertilizer application. The changes of soil organic C (SOC) and total N ( T N ) contents demonstrated a similar trend to soil glomalin in these plots. The SOC and TN contents of NPKS plot were 15.01% and 9.18% higher than those of the CK plot, and 8.85% and 14.76% higher than those of the NPK plot, respectively. Rice straw return also enhanced the contents of microbial biomass C (MBC) and microbial biomass N (MBN) in the NPKS plot by 7.76% for MBC and 31.42% for MBN compared with the CK plot, and 12.66% for MBC and 15.07% for MBN compared with the NPK plots, respectively. Application of only chemical fertilizer, however, increased MBN concentration, but decreased MBC concentration in soil.
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Key Words:
C, glomalin, long-term fertilizer experiment, N, rice straw return
Citation: Nie, J., Zhou, J . M., Wang, €1. Y., Chen, X. Q. and Du, C. W. 2007. Effect of long-term rice straw return on soil glomalin, carbon and nitrogen. Pedosphere. 17(3): 295-302.
INTRODUCTION Arbuscular mycorrhizal fungi (AMF) are ubiquitous root symbiotic fungi that are closely associated with host plants, including major food crops (wheat, corn, sorghum, etc.) and pasture plants. AMF play a significant role in the soil environment, function as an extension of the root system into the soil, and have numerous effects on plant physiology and plant communities (Allen, 1991; Smith and Read, 1997; Gai et al., 2005). Their effects on soil structure, water retention capacity, and nutrient cycling are of critical importance t o the maintenance of soil function in both natural and cultivated ecosystems. Recent studies indicated that hyphae of AMF play an important role in soil aggregation (Miller and Jastrow, 1990; Tisdall, 1991; Jastrow et al., 1998). Recently, glomalin, a glycoprotein, produced by AMF has been detected. Glomalin can be extracted from the hyphae of all the isolates of AMF examined to date (Wright et al., 1996; Rillig and Steinberg, 2002), and glomalin was secreted into soil through turnover of AMF. Glomalin in soil is characterized as follows: insoluble in water, but can be solubilized by 20 or 50 mmol L-l citrate at 121 "C (Wright et al., 1996); highly correlated with soil C and N (Rillig et al., 2001); sequesters potentially toxic elements in soil (Gonzalez-Chavez et al., 2004); linked with an oligosaccharide (Wright et al., 1998); strongly *'Project supported by the National Key Basic Research Support Foundation of China (No. 2002CB410810). *2Corresponding author. E-mail: [email protected].
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positively correlated with soil aggregate stability (Wright and Updhyaya, 1998; Rillig, 2004); and has a relatively long lifespan in soil (Rillig e t al., 2003; Steinberg and Rillig, 2003). Moreover, the effect of glomalin on soil aggregation is stronger than that of AMF (Driver et al., 2005) because glomalin acts as an insoluble glue for the stabilization of aggregates (Wright and Updhyaya, 1996, 1998). Furthermore, there is abundant glomalin in natural and cultivated soil, and the concentration of glomalin in soil ranges from 4.4 to 14.8 mg g-' soil (Wright et al., 1996). Land management practices, such as fertilization, tillage, and irrigation, have a significant impact on soil chemical, physical, and biological properties. For example, soil glomalin concentration responded to land use change (Rillig e t al., 2003), tillage practices (Wright et al., 1999), and crop rotation (Wright and Anderson, 2000). Fertilization is perhaps the most important practice that affects chemical, physical, biological, and biochemical properties of soil (Zhang e t al., 2005), but there is little understanding about the effect of fertilization on soil glomalin concentration. Rice is one of the most important crops in China, and the seeded area reached 2.65 x lo7 ha. The annual production amounted t o 1.61 x lo5 Mg in 2003 (Editorial Committee of China Agriculture Yearbook, 2004). As a by-product, the annual rice straw production also amounted to 1.72 x lo5 Mg, and increased with the breeding and wide use of high-yielding rice varieties. Rice straw is not only an agricultural residue, but also an important fertilizer resource. Rice straw return into soil is a common practice in China. Rice straw supplies abundant nitrogen, phosphate, potassium, and other essential nutrient elements to plants (Wang et al., 2005), and rice straw return into soil can improve physical-chemical and biological properties of soil and thereby enhance soil fertility. It has been reported that rice straw plays a significant role in maintaining soil fertility (Lu et al., 2005; Wang e t al., 2003) and microbial biomass communities (Chilima et aL, 2002). This has become an important aspect of sustaining long-term fertility in cropping systems. However, little is known about the effects of chemical fertilizer application and the combined application of chemical fertilizer and rice straw on soil glomalin concentration. The objective of this study was to investigate glomalin, organic carbon (OC), total N (TN), microbial biomass C (MBC), and microbial biomass N (MBN) concentrations in response to longterm chemical fertilizer application and the application of chemical fertilizer in combination with rice straw return into soil. MATERIALS AND METHODS Site description
A long-term field experiment was initiated in 1981 at the Key Field Monitoring Experimental Station for Reddish Paddy Soil Eco-environment in Wangcheng, Ministry of Agriculture of China. The station is located in Huangjin Village Town (112' 80' N, 28' 37' E, 100 m altitude), Wangcheng County of Hunan Province in the central region of the Xiangjiang River (a branch of Dongting Lake), China. The climate of this area is subtropical monsoonal climate. Average annual precipitation is approximately 1370 mm and annual mean temperature is 17 ' C , with the lowest monthly temperature of 4.4 "C in January and the highest monthly temperature of 30 "C in July. The annual frost-free period is approximately 300 d. The soil is a Fe-accumuli-Stagnic Anthrosols derived from Quaternary red clay (clay loam). On the basis of the analysis of soil samples taken from the experimental site on October 1981, the characteristics of the top soil (15 cm) were: pH 6.9; soil organic matter (SOM) 35.5 g kg-', total N (N) 2.05 g kg-l, hydrolysable N 151.0 mg kg-', available P 10.2 mg kg-', and exchangeable K 62.3 mg kg-'.
Experimental design and treatments The cropping system of this area comprised cropping of early rice and late rice each year. Each experimental plot was 6.67 m wide by 10 m long. Three fertilization treatments were arranged in a randomized complete block design with three replications. The treatments were: 1) CK, unfertilized control; 2) NPK, nitrogen, phosphorus, and potassium fertilizer applied annually; 3) NPKS, straw (S)
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and same fertilization in NPK. Adjacent plots were separated by concrete ridges (30 cm width), and the blocks were separated by irrigation furrows (50 cm width) and two ridges (30 cm width). The inorganic fertilizer sources of N, P, and K in three treatments were commercial fertilizers such as urea, single super phosphate, and potassium chloride. The analysis of nutrients of rice straw varied from one year to another, but on the average, rice straw contained 8.6 g kg-l total N, 3.0 g kg-I total PzO5, and 25.0 g kg-l total KzO. Nitrogen fertilizer was applied at 150 kg N ha-' t o early rice and 180 kg N ha-' to late rice during 1981-2005. Phosphate fertilizer was applied at 75 kg-' PzO5 ha-l to both early rice and late rice during 1981-1990, and 60 kg P205 ha-' to both early rice and late rice from 1991 to 2005, respectively. Potassium fertilizer was applied at 120 kg KzO ha-l to both early rice and late rice during 1981-2005. Rice straw was applied at 2.62 t ha-' to both early and late rice.
Soil samples and analyses Soil samples were collected in March 2005 to a depth of 15 cm before early rice was transplanted. Each sample was a composite mixture of 10 cores that were randomly selected using a 2.4-cm diameter soil corer. The samples were taken from within areas (6 m x 9 m) to avoid inclusion of the additional factor. SOC and T N were determined in air-dried soil (< 180 pm) using a C/N/S-analyzer (Vario MAX). MBC and MBN were determined on a field moist soil sample (< 2 mm) by chloroform-fumigationextraction method as described by Vance et al. (1987), using 0.5 mol L-l K2S04 as an extractant. Organic C and N from the fumigated (24 h) and nonfumigated (control) soil were quantified by a TOC analyzer (Phoenix 8000) and a flow injection analyzer (FIAstar 5000), respectively. The nonfumigated control values were subtracted from the fumigated values. The MBC and MBN were calculated by dividing the differences of C and N contents in the non-fumigated and the fumigated soil samples with conversion factors of 0.45 (Wu et al., 1990) and 0.54 (Jenkinson, 1988), respectively. Each sample was subjected to three analyses, and results were expressed without considering the moisture factor. Soil moisture was determined after drying at 105 "C for 48 h.
Glomalin extraction methods Glomalin extractions from soil were carried out as described by Wright and Upadahyaya (1996). Before the glomalin was extracted, aggregates were analyzed after the soil samples were stored for 3 months using the method and apparatus described by Kemper and Rosenau (1986). Then replicate containing 1 g of soil samples of 1-2-mm aggregates were extracted with 8 mL of extiactant. The easily extractable glomalin (EEG) fraction was extracted with 20 mmol L-l sodium citrate (pH 7.0) at 121 " C for 30 min. Samples were centrifuged at 10000 x g for 5 min immediately after extraction, and the supernatant containing the extracted protein was removed for analysis. The total glomalin (TG) fraction was extracted with 50 mmol L-l sodium citrate (pH 8.0) at 121 "C for 60 min, and then immediately centrifuged at 10000 x g for 5 min. After each cycle, the supernatant was removed and sodium citrate was replenished for the extraction of glomalin again until the supernatant showed no red-brown color, which is typical for glomalin. The supernatant was stored for analysis. Both fractions were analyzed using the Bradford protein assay, which utilizes an acidic solution of Coomassie brilliant blue G-250 dye to bind to amino acid residues of protein. Bovine serum albumin was used to prepare as the standard for the assay.
Statistical analyses Statistical analyses were performed with SPSS10. Standard analysis of variance techniques were used to analyze the effects of treatments. The main significant effects were separated by the least significant difference test.
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RESULTS AND DISCUSSION Easily extractable glomalin and total glomalin concentration The results in Fig.1 showed that fertilizers with rice straw increased the concentrations of easily extractable glomalin (EEG) and total glomalin (TG) in soil. The EEG concentrations were significantly influenced by different fertilizations ( F = 14.548; P = 0.005), and the EEG concentrations of NPKS plot were higher than those of CK plot by 4.68% and NPK plot by 9.87%. Similarly, soil TG concentrations were also significantly affected by different fertilizations ( F = 9.848; P = 0.013), and the TG concentrations of NPKS plot were higher than those of CK plot by 5.67% and NPK plot by 6.23%. Furthermore, the results indicated that soil EEG and TG concentrations of NPK plot were actually lower than those of CK plot, although the difference was not statistically significant.
Fig. 1 Effect of long-term fertilizer application o n easily extractable glomalin (EEG) and total glomalin (TG) in soil. CK = no fertilizer application; NPK = nitrogen, phosphorus, and potassium fertilizer application; NPKS = nitrogen, phosphorus, and potassium fertilizer application rice straw return. Error bars indicate standard deviations of the means (n = 3).
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Many reports have been published on soil glomalin concentrations in natural and agricultural ecosystern affected by different plants (Rillig et al., 2002), land use change (Rillig et al., 2003), and alternative crop rotations (Wright and Anderson 2000). Unlike most known AMF that are nonhost specific, Bever et al. (1996) discovered a preferential association of mycobionts with certain host plants. They believed that different host plants were colonized by different subsets of the AMF community, which enhanced soil glomalin concentrations in response to plants, land use change, and crop rotation. The results of this study from the same field and on the same host plant (rice) showed that the soil glomalin concentrations varied significantly in different fertilization plots. While the NPKS treatment increased soil glomalin concentration, chemical fertilizer application without straw did not increase soil glomalin concentration. This might be partially responsible for the increase of soil rigidity after long-term chemical fertilizer application in agricultural soils. Therefore, to maintain soil structure and promote sustainable agriculture and thereby to improve soil quality, the combined application of chemical fertilizer arid rice straw or organic manure should be adopted in cultivated soil.
Soil organic C and total N Soil organic matter (SOM) or soil organic carbon (SOC) is considered to be a key attribute of soil quality because it is one of the important physical and biological properties of soil (Yang et al., 2005). In this study, the averages of SOC concentration were significantly different among the treatments ( F = 9.360; P = 0.014). The SOC concentration in NPKS plot was higher than that in NPK by 15.01% and CK plot by 8.85% (Fig.2). Compared with CK plot, the application of only chemical fertilizer application (NPK plot) lowered SOC, but the difference was not significant. Similarly, the
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averages of T N concentrations also reached statistically significant level ( F = 11.146; P = 0,010). The TN concentration in NPKS plot was 2.65 mg g-' and was significantly higher than that in CK plot by 9.18% and NPK plot by 14.76%; however, there were no significant difference of total N between CK and NPK plots. These results were in agreement with other reports (Jenkinson and Ryner, 1977; Nel et al., 1996; Aref and Wander, 1998), wherein they discovered that long-term fertilizer application resulted in loss of soil organic matter and total N. Therefore, straw return in soil perhaps is a good practice to maintain soil fertility and improve productivity. 25
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Fig. 2 Effect of long-term fertilizer application on organic C (OC) and total N (TN) in soil. CK = no fertilizer application; NPK = nitrogen, phosphorus, and potassium fertilizer application; NPKS = nitrogen, phosphorus, and potassium fertilizer application rice straw return. Error bars indicate standard deviations of the means ( n = 3).
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Wright and Upadhyaya (1998) postulated that EEG and TG in soil were highly correlated with soil C and N (Rillig et al., 2003). In this study, because the range of treatments was not large enough, no correlation was found between soil EEG or TG concentration and soil organic C or total N concentration. Nevertheless, the changes of SOC and T N in different plots demonstrated a similar trend with regard to the changes of soil EEG and TG. Therefore, fertilization with straw may be an effective agricultural practice that can enhance the formation and concentration of soil glomalin. Soil microbial biomass C and microbial biomass N
Soil microbial biomass C (MBC) is the active component in soil organic matter. The change of MBC reflects the process of microorganism propagation and degradation utilizing soil carbon. Fig. 3 indicated that application of only chemical fertilizer resulted in little decrease in MBC concentration in the surface layer (0-15 cm) compared to that of CK plot. MBC in the CK plot was higher than that in the NPK plot by 4.55%. Whereas, the combined application of chemical fertilizer and straw significantly
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Fig. 3 Effect of long-term fertilizer application on microbial biomass C (MBC) and microbial biomass N (MBN) in soil. CK = no fertilizer application; NPK = nitrogen, phosphorus, and potassium fertilizer application; NPKS = nitrogen, phosphorus, and potassium fertilizer application ( n = 3).
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increased soil MBC concentration by 7.76% compared t o that of CK plot and 12.66% compared to that of NPK plot. The statistical analysis indicated that the difference of MBC among different treatment plots reached a significant level ( F = 36.953; P < 0.001). The results (Fig. 3) indicated that different fertilizations in this experiment evidently affected soil microbial biomass N (MBN) ( F = 9.880; P = 0.013). The MBN concentrations in NPK and NPKS plots were significantly higher than those in CK plots, representing an increase of 14.25% and 31.42%, respectively. The results also showed that the combined application of chemical fertilizer and straw significantly enhanced soil MBN by another 15.07% over the NPK plot. Soil MBC and MBN concentrations were determined by the addition of organic matter nitrogen fertilizer. Because there was no organic matter or nitrogen fertilizer inputs for 25 years in the CK plot, the soil might not have enough C and N resources for the propagation of microbes, resulting in low soil MBC and MBN. The results also suggested that rice straw return into soil could obviously promote soil microbe breed and thereby enhance soil MBC and MBN concentrations. The reason for a low MBC concentration in NPK plot compared to that in the CK plot may be explained by increased degradation rate of soil organic matter caused by N application in NPK plot, and the higher yield resulted in enhanced formation of soil C.
Ratios of MBC:TC, MBN:TN, MBC:MBN, and S 0 C : T N The ratio of MBC:MBN can reflect the effect of different treatments on soil microbial biomass and microbial community structure. The results indicated that there was no obvious difference in the ratios of MBC:SOC and MBN:TN among the three different fertilizers plots (Table I). The ratio of MBN:TN in NPK and NPKS plots was 19.85% and 20.22% higher than that in the CK plot, respectively, whereas the ratio of MBC:MBN in CK plot was significantly higher than that in NPK and NPKS plots by 19.47% and 22.04%, respectively. TABLE I Ratios of microbial biomass C (MBC):organic C (OC), microbial biomass N (MBN):total N (TN), MBC:MBN, and 0C:TN in soils under different treatments Treat m e i t a)
MBC:OC
MBN:TN
MBC:MBN
0C:TN
CK NPK NPKS
0.0351aAb) 0.0355aA 0.0348aA
0.0272aA 0.0326bA 0.0327bA
11.3465aA 9.5024bAB 9.3035bB
8.7857aA 8.7399aA 8.7592aA
CK = no fertilizer application; NPK = nitrogen, phosphorus, and potassium fertilizer application; NPKS = nitrogen, rice straw return. phosphorus, and potassium fertilizer application b)Values followed by the same letter (lowercase for P < 0.05 and uppercase for P < 0.01) within a column were not significantly different.
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The percentage change of MBC in SOC may be related t o organic matter formation, and the efficiency of conversion of recalcitrant C into MBC (Sparling, 1992). It can be an indicator of whether soil organic matter is decreasing, increasing, or in a steady state (Anderson and Domsch, 1989; Insam, 1990). The results of this study indicated that long-term chemical fertilizer applications or the combined application of chemical fertilizer and straw had no obvious effect on soil organic matter formation and degradation. Jenkinson and Ladd (1981) suggested 2.2% as a threshold value for whether a soil was in equilibrium. The results showed values much higher than this threshold. Generally, if a soil is intensively disturbed, MBC will decline faster than the organic matter, and the percentage of total C also decreases with the decrease in MBC (Powlson and Jenkinson, 1981; Sparling, 1992). The results of this study suggested that the ratio of MBC to total C under cultivation conditions for paddy soil could be regarded as an indicator of C accumulation in subtropical regions. The sole application of chemical fertilizers or the combined application of chemical fertilizers with rice straw significantly reduced the ratio of MBC:MBN by increasing the N concentration in microbe
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and decreasing C concentration. CONCLUSIONS Application of only chemical fertilizer had little impact on soil glomalin concentration, whereas the combined application of fertilization and rice straw significantly raised soil glomalin concentration. The changes of soil organic C and total N showed a similar trend to the changes of soil glomalin concentration caused by continuous fertilizer applications for 25 years. Straw return in soil may be one of the most important practices in raising soil glomalin concentration. The combined application of chemical fertilizer and rice straw significantly increased soil MBC and MBN concentrations compared with the application of only chemical fertilizer, which enhanced soil MBN but decreased soil MBC. There was no obvious difference in the ratios of MBC:SOC and S0C:TN among the three plots. Nevertheless, with no fertilizer application, the ratio of MBN:TN decreased, whereas the MBC:MBN ratio increased, implying that fertilization may be related to soil N accumulation. REFERENCES Allen, M. F. 1991. The Ecology of Mycorrhizae. Cambridge University Press, Cambridge. 184pp. Anderson, T. H. and Domsch, K. H. 1989. Ratios of microbial biomass carbon t o total organic carbon in arable soils. Soil Biol. Biochem. 21: 471-479. Aref, S. and Wander, M. M. 1998. Long-term trends of corn yield and soil organic matter in different crop sequences and soil fertility treatments on the Morrow Plots. Advance in Agronomy. 62: 153-161. Bever, J . D., Morton, 3. B., Antonovics, J. and Schultz, P. A. 1996. Host-dependent sporulation and species diversity of aarbuscular mycorrhizal fungi in a mown grassland. J. Ecol. 84: 71-82. Chilima, J., Huang, C. and Wu, C. 2002. Microbial biomass carbon trends in black and red soils under single straw application: Effect of straw placement, mineral N addition and tillage. Pedosphere. 12: 59-72. Driver, J . D., Holben, W. E. and Rillig, M. C. 2005. Characterization of glomalin as a hyphal wall component of arbuscular mycorrhizal fungi. Soil Biol. Biochem. 37: 101-106. Editorial Committee of China Agriculture Yearbook. 2004. China Agriculture Yearbook (in Chinese). Chinese Agriculture Press, Beijing. 133pp. Gai, J. P., Feng, G. G and Li, X. L. 2005. Review of researches on biodiversity of arbuscular mycorrhizal fungi. Soils (in Chinese). 37: 236-242. Gonzalez-Chavez, M. C., Carrillo-Gonzalez, R., Wright, S . F. and Nichols, K. A. 2004. The role of glomalin, a protein produced by arbuscular mycorrhizal fungi, in sequestering potentially toxic elements. Environmental Pollution. 130: 317-323. Insam, H. 1990. Are the soil microbial biomass and basal respiration governed by the climatic regime? Soil Biol. Biochern. 22: 525-532. Jastrow, J . D., Miller, R. M. and Lussenhop, J. 1998. Contribution of interacting biological mechanisms to soil aggregate stabilization in restored prairie. Soil Biol. Biochem. 30: 905-916. Jenkinson, D. S. 1988. Determination of microbial biomass carbon and nitrogen in soil. In Wilson, J . R. (ed.) Advances in Nitrogen Cycling in Agricultural Ecosystems. Marcel dekker, New Youk. pp. 368-386. Jenkinson, D. S. and Ladd, J. N. 1981. Microbial biomass in soil: Measurement and turnover. In Paul, E. A. and Ladd, J. M. (eds.) Soil Biochemistry. Vol. 5. Marcel Decker, New York. pp. 415-471. Jenkinson, D. S. and Rayner, J. H. 1977. The turnover of soil organic matter in some of the Rothamsted classical experiments. Soil Sci. 125: 298-305. Kemper, W.D. and Rosenau, R. C. 1986. Aggregate stability and size distribution. In Klute, A. and Page, A. L. (eds.) Methods of Soil Analysis. Part 1. Physical and Mineralogical Methods. American Society of Agronomy, Madison, WI. pp. 425-442. Lu, B., &in, J. H and Zhao, Y. C. 2005. Effect of wheat straw mulching on soil fertility and crop production on salinealkaline soil. Soils (in Chinese). 37: 52-55. Miller, R. M. and Jastrow, J . D. 1990. Hierarchy of root and mycorrhizal fungal interactions with soil aggregation. Soil Biol. Biochem. 22: 579-584. Nel, P. C., Barnard, R. O., Steynberg, R. E., De Beer, J. M. and Groeneveld, H. T. 1996. Trends in maize grain yields in a long-term fertilizer trial. Field Crops Res. 47: 53-64. Powlson, D. S. and Jenkinson, D. S. 1981. A comparison of the organic matter, biomass, adenosine triphosphate and mineralizable nitrogen contents of ploughed and direct-drilled soils. J . Agric. Sci. 97: 713-721. Rillig, M. C. 2004. Arbuscular mycorrhizae, glomalin, and soil aggregation. Can. J . Soil. Sci. 84: 355-363.
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Rillig, M. C. and Steinberg, P. D. 2002. Glomalin production by an arbuscular mycorrhizal fungus: A mechanism of habitat modification? Soil Biol. Biochem. 34: 1371-1 374. Rillig, M. C., Ramsey, P. W., Morris, S . and Paul, E. A. 2003. Glomalin, an arbuscular-mycorrhizal fungal soil protein, responds to land-use change. Plant and Soil. 253: 293-299. Rillig, M. C., Wright, S. F. and Eviner, V. 2002. The role of arbuscular mycorrhizal fungi and glomalin in soil aggregation: Comparing effects of five plant spacies. Plant and Soil. 238: 325-333. Rillig, M. C., Wright, S. F., Nichols, K. A., Schmidt, W. F. and Torn, M. S. 2001. Large contribution of arbuscular mycorrhizal fungi to soil carbon pools in tropical forest soils. Plant and Soil. 233: 167-177. Smith, S . E. and Read, D. J. 1997. Mycorrhizae Symbiosis. Academic Press, San Diego, CA. Sparling, G. P. 1992. Ratio of microbial biomass carbon to soil organic carbon as a sensitive indicator of changes in soil organic matter. Aust. J. Soil Res. 30: 195-207. Steinberg, P. D. and Rillig, M. C. 2003. Differential decomposition of arbuscular mycorrhizal fungal hyphae and glomalin. Soil Biol. Bzochem. 35: 191-194. Tisdall, J. M. 1991. Fungal hyphae and structural stability of soil. Aust. J . Soil Res. 29: 729-743. Vance, E. D., Brookes, P. C. and Jenkinson, D. S. 1987. An extraction method for measuring soil microbial biomass C. Soil Biol. Biochem. 19: 703-707. Wang, X.D., Shi, X. J. and Song, G. Y. 2005. Effects of long-term rice straw returning on the fertility and productivity of purplish paddy soil. Plant Nutrition and Fertilizer Science (in Chinese). 11: 302-307. Wang, Z. M., Zhu, P. L., Huang, D. M and Liu, H. Q. 2003. Straw carbon decomposition in situ in field and characteristics of soil biomass carbon turnover. Acta Pedologica Sinica (in Chinese). 40: 446-453. Wright, S. F. and Anderson, R. L. 2000. Aggregate stability and glomalin in alternative crop rotations for the central Great Plains. Biol. Fert. of Soils. 31: 249-253. Wright, S. F., Franke-Snyder, M., Morton, J. B. and Upadhyaya, A. 1996. Time-course study and partial characterization of a protein on hyphae of arbuscular mycorrhizal fungi during active colonization of roots. Plant and Soil. 181: 193-203. Wright, S. F., Starr, J. L. and Paltineanu, I. C. 1999. Changes in aggregate stability and concentration of glomalin during tillage management transition. Soil Sci. SOC. Am. J. 63: 1825-1 829. Wright, S. F. and Upadhyaya, A. 1996. Extraction of an abundant and unusual protein from soil and comparison with hyphal protein of arbuscular mycorrhizal fungi. Soil Sci. 161: 575-586. Wright, S. F., and Upadhyaya, A. 1998. A survey of soils for aggregate stability and glomalin, a glycoprotein produced by hyphae of arbuscular mycorrhizal fungi. Plant and Soil. 198: 97-107. Wright, S. F., Upadhyaya, A. and Buyer, J. S. 1998. Comparison of N-linked oligosaccharides of glomalin from arbuscular mycorrhizal fungi and soils by capillary electrophoresis. Soil Biol. Biochem. 30: 1 853-1 857. Wu, J., Joergensen, R. G., Pommerening, B., Chaussod, R. and Brookes, P. C. 1990. Measurement of soil microbial biomass by fumigation-extraction-An automated procedure. Soil Biol. Biochem. 22: 1167-1 169. Yang, C. M., Yang, L. Z. and Yan, T. M. 2005. Chemical and microbiological parameters of paddy soil quality as affected by different nutrient and water regimes. Pedosphere. 15: 369-378. Zhang, Q . C . , Wang, G. H. and Fang, B. 2005. Influence of fertilization treatment on nutrients uptake by rice and soil ecological characteristics of soil microorganism in paddy field. Acta Pedologica Sinica (in Chinese). 42: 116-121.