团聚体更新与碳循环

Short communication Soil macroaggregate turnover and microaggregate formation: a mechanism for C sequestration under no-tillage agriculture J. Six*, E.T. Elliott1, K. Paustian Natural Resource Ecology Laboratory, Colorado State University, Fort Collins, CO 80523, USA Received 27 March 2000; received in revised form 4 July 2000; accepted 29 July 2000 Abstract Soil disturbance from tillage is a major cause of organic matter depletion and reduction in the number and stability of soil aggregates when native ecosystems are converted to agriculture. No-till (NT) cropping systems usually exhibit increased aggregation and soil organic matter relative to conventional tillage (CT). However, the extent of soil organic matter changes in response to NT management varies between soils and the mechanisms of organic matter stabilization in NT systems are unclear. We evaluated a conceptual model which links the turnover of aggregates to soil organic matter dynamics in NT and CT systems; we argue that the rate of macroaggregate formation and degradation (i.e. aggregate turnover) is reduced under NT compared to CT and leads to a formation of stable microaggregates in which carbon is stabilized and sequestered in the long term. Therefore, the link between macroaggregate turnover, microaggregate formation, and C stabilization within microaggregates partly determines the observed soil organic matter increases under NT. q 2000 Elsevier Science Ltd. All rights reserved. Keywords: Aggregate turnover; Carbon sequestration; No-tillage; Particulate organic matter An accumulation of soil organic matter under no-tillage (NT) compared to conventional tillage (CT) confers impor- tant improvements in soil quality, soil fertility and seques- tration of carbon. Mechanisms by which reduced tillage decreases soil organic matter decomposition (e.g. reduced soil disturbance, redistribution of residues) have been known for some time (Oades, 1984; Paustian et al., 1997) but the ultimate mechanisms have not been well elucidated. It has been established that the inclusion of organic materi- als within soil aggregates reduces their decomposition rate (Oades, 1984; Elliott and Coleman, 1988). Increases in aggregation concomitant with increases in organic C have been observed in NT systems (Paustian et al., 2000; Six et al., 2000). Tillage has been found to induce a loss of C-rich macroaggregates and a gain of C-depleted microaggregates (Six et al., 2000). However, this decrease in macroaggre- gates cannot explain the total C loss associated with tillage. Six et al. (1998, 1999a) suggested that increased macroag- gregate turnover under CT is a primary mechanism causing decreases of soil C. Differential macroaggregate turnover induced by tillage and its influence on SOM dynamics are represented in a conceptual model (Fig. 1) we developed to explain differences in C-sequestration between NT and CT. The model forms a basis for the hypotheses tested in this study. At time 1 (t1), macroaggregates (250–2000 mm) are formed around fresh residue which then becomes coarse intra-aggregate particulate organic matter (iPOM) (Fig. 1). The fresh residue induces the formation of macroaggregates because it is a C source for microbial activity and the production of microbial-derived binding agents (Golchin et al., 1994; Jastrow, 1996; Six et al., 1999a). The model assumes similar rates of macroaggregate formation in NT versus CT (at t1) because the residue input is often similar in both management systems (Paul et al., 1997). Six et al. (1999a) found that the proportion of crop-derived C (i.e. newer C) relative to native grassland C (i.e. older C) was similar in NT and CT macroaggregates, confirming that the rate of macroaggregate formation was similar in both management systems. Fine iPOM within a macroaggregate is derived from the decomposition and subsequent fragmentation of coarse iPOM (t1 to t2; Fig. 1). This process is supported by the obser- vations that decomposition causes decreases in POM size (Guggenberger et al., 1994) and that fine iPOM is older than coarse iPOM (Six et al., 1998). Consequently, fine iPOM concentration is expected to increase with macroaggregate Soil Biology & Biochemistry 32 (2000) 2099–2103 0038-0717/00/$ - see front matter q 2000 Elsevier Science Ltd. All rights reserved. PII: S0038-0717(00)00179-6 www.elsevier.com/locate/soilbio * Corresponding author. Tel.: 11-970-491-5599; fax: 11-970-491-1965. E-mail address: johan@nrel.colostate.edu (J. Six). 1 Present address: School of Natural Resource Sciences, University of Nebraska at Lincoln, Lincoln, NE 68583-0758, USA. age. Therefore, an abundance of older macroaggregates suggests a slower macroaggregate turnover and the ratio of fine iPOM to coarse iPOM within macroaggregates can be used as a relative measure of the turnover of macroaggregates. At four agricultural experiment sites this ratio was approxi- mately twice …2:10 ^ 0:30† as large in NT as in CT (Fig. 2), suggesting that macroaggregate turnover is approximately twice as slow in NT compared to CT. As fine iPOM is formed it gradually becomes encrusted with clay particles and microbial products (t2 to t3) to form microaggregates within macroaggregates (Six et al., 1998, 1999a). In isotope tracer studies, labeled C was redistributed from macroaggregates to microaggregates with time (Angers et al., 1997; Gale et al., 2000) suggesting that microaggregates are formed within macroaggregates (Oades, 1984; Elliott and Coleman, 1988). Eventually, the binding agents in macroag- gregates degrade, resulting in loss of macroaggregate stability (t4) and the release of stable microaggregates, which become the building blocks for the next cycle of macroaggregate formation (Tisdall and Oades, 1982). The model suggests that the increases in macroaggregate turnover induced by tillage yields fewer new free microag- gregates in CT compared to NT at t4 (Fig. 1). Supporting this, less accumulation of crop-derived C in free micro- aggregates has been observed in CT compared to NT (Six et al., 1999a). This incorporation of new C into free microaggregates is an important factor contributing to C- sequestration (Skjemstad et al., 1990) since C contained in J. Six et al. / Soil Biology & Biochemistry 32 (2000) 2099–21032100 Fig. 1. This conceptual model shows the “life cycle” of a macroaggregate and the formation of microaggregates. These processes are the result of the interrelationship between the turnover of macroaggregates, the turnover of SOM and controlling factors such as disturbance (i.e. tillage). Turnover occurs through time as an aggregate is formed, becomes unstable and is eventually disrupted. Disturbances such as tillage shortcut this “life cycle” of macroaggregates and diminish the formation rate of new microaggregates and thus the sequestration of C within microaggregates and the soil as a whole. (iPOMˆ intra- aggregate particulate organic matter; POMˆ particulate organic matter; tˆ time; ˆ process rate modifier). free microaggregates has a slower turnover than C in macro- aggregates (Jastrow et al., 1996). Based on the accumulated understanding embodied in our conceptual model, we advanced the following two hypotheses. H1: in NT soils, there are more microaggregates contained within macroaggregates and there is more fine iPOM-C within these microaggregates than in CT soils. H2: in NT soils, the SOM-C and iPOM-C of microaggre- gates that are contained within macroaggregates are younger than in CT soils. The rationale for these two hypotheses is as follows. A slow macroaggregate turnover in NT allows time for the formation of fine iPOM from recent crop-derived coarse iPOM and the subsequent encapsulation of this fine iPOM by mineral parti- cles and microbial byproducts to form stable microaggregates containing young crop-derived C. In contrast, the turnover of macroaggregates in CT is faster, providing less opportunity for the formation of crop-derived fine iPOM and stable microag- gregates. Thus the organic matter contained in microaggre- gates of CT soils is dominated by older C derived from the pre-cultivation vegetation. Direct testing of these hypotheses was accomplished by isolating microaggregates held within macroaggregates using a new method. Soil samples (0–5 cm) were taken at a long-term tillage experiment located at Sidney, NE. The experiment is on a Duroc loam, fine silty, mixed, mesic Pachic Haplustoll and includes NT and CT under wheat fallow, and a native grassland treatment. Prior to establish- ment of the experiment (in 1969) the entire area was native grassland that had never been cultivated. To isolate micro- aggregates held within macroaggregates, we built a device to completely break up macroaggregates while minimizing the break down of the released microaggregates. We only analyzed macroaggregates from the 0–5 cm layer because we did not observe any significant differences between NT and CT in aggregate carbon and fine iPOM-C in the 5– 20 cm layer at this site (Six et al., 1999a). Macroaggregates (10 g) were immersed in deionized water on top of a 250- mm mesh screen and gently shaken with 50 glass beads (dia.ˆ 4 mm). Continuous and steady water flow through the device ensured that microaggregates were immediately flushed onto a 53-mm sieve and were not exposed to any further disruption by the beads. After all macroaggregates were broken up, the material on the 53-mm sieve was sieved to ensure that the isolated microaggregates were water- stable. The inter-microaggregate POM retained together with the microaggregates on the sieve was isolated by density flotation in 1.85 g cm23 sodium polytungstate (Six et al., 1998). After density flotation, the microaggregates were dispersed in 5 g hexametaphosphate per liter and intra-microaggregate POM isolated by sieving (Six et al., 1998). To avoid cross contamination of C, and especially 13C, among samples, sodium polytungstate was recycled according to Six et al. (1999b). The proportion of micro- aggregate (53–250 mm) weight within macroaggregates (250–2000 mm) was calculated as: microaggregate weight 2 weight of 53–250 mm sized sand macroaggregate weight 2 weight of 250–2000 mm sized sand …1† The weights of macro- and microaggregates were corrected for the sand content of the same size as the aggregates because sand of the same size as the aggregate is usually not a part of an aggregate and should consequently not be weighed as an aggregate. Carbon concentrations were measured with a LECO CHN-1000 analyzer and carbon- isotope ratios were determined using a Carlo Erba NA 1500 CN analyzer coupled to a Micromass VG isochrom- EA masspectrometer. Our hypotheses were corroborated with data from this new approach. We found that microaggregates within macroaggre- gates accounted for only 27% of the macroaggregate weight in CT, while 47% of the macroaggregate weight in NT consists of microaggregates (Table 1). Hence, the formation of new microaggregates within macroaggregates was reduced by a factor of about 2 (27 versus 47%) in CT compared to NT. These data are congruent with the previous observation that macroaggregates turn over twice as fast in CT compared to NT based on the ratio of fine iPOM to coarse iPOM (Fig. 2). Thus, macroaggregate turnover and microaggregate formation appear to be linked: a doubling of macroaggregate turnover reduces the microaggregate formation within macroaggre- gates by a factor of 2. Within macroaggregates, the concentration of intra- J. Six et al. / Soil Biology & Biochemistry 32 (2000) 2099–2103 2101 Fig. 2. Ratio of fine intra-particulate organic matter (iPOM) over coarse iPOM in the surface layer (0–5 cm) of NT and CT soils across four agricultural experiment sites (Sidney, NE; Wooster, OH; Kellogg Bio- logical Station, MI; Lexington, KY). The ratio’s are calculated based on data presented in Six et al. (1999a). microaggregate POM-C was 3-fold greater in NT compared to CT while the concentration of inter-microaggregate POM-C (i.e. POM-C held within macroaggregates but not within microaggregates) was 2-fold greater in CT compared to NT (Table 1). In addition, the proportion of fine iPOM-C held within microaggregates that occurs within macroaggre- gates was much larger in NT compared to CT (90 versus 58%, respectively) leading us to conclude that the slower macroaggregate turnover in NT leads to a sequestration of C, primarily as fine iPOM held within stable microaggre- gates that are formed within macroaggregates. The greater accumulation of microaggregates rich in fine iPOM contri- butes to the greater total SOM-C under NT. Six et al. (1999a) found that the increase in total fine iPOM (i.e. inter- plus intra-microaggregate iPOM) alone accounted, on average, for 21% of the total C difference between NT and CT at four agricultural experiment sites. Both the microaggregates within macroaggregates and the intra-microaggregate POM-C were younger in NT than in CT (Table 2). This is attributed to the slower turn- over of macroaggregates in NT, resulting in more seques- tration of crop-derived C within stable microaggregates formed within macroaggregates under NT. In addition, the d 13C signature of the mineral fraction (,53 mm) contained within the macroaggregates suggests that C sequestration is also enhanced in this fraction (Table 2). The halved rate of macroaggregate turnover, as suggested by the data in Fig. 2, results in twice as many microaggre- gates formed within macroaggregates which, in turn, leads to twice as much fine iPOM accumulating in NT compared to CT. We have reported a doubling of both the amount of macroaggregates (Six et al., 2000) and the mean residence time of total soil C (Paustian et al., 2000; Six et al., 1999a) in NT compared to CT in several soils. The linkage of macroaggregate turnover, microaggregate formation and SOM dynamics hypothesized in our model, was strongly supported by our data on the composition of macro- and microaggregates and their respective C dynamics. The linkage of these processes gives a mechan- istic explanation as to why there is greater accumulation of SOM-C under NT agriculture. Our results underscore the importance of soil aggregation and more specifically the interactions of SOM and aggregate dynamics in controlling C-sequestration in soils. Acknowledgements We appreciate the assistance of Dan Reuss, Karolien Denef and Heleen Bossuyt during methods development. We thank Jason Kaye, Rich Conant, and Serita Frey for comments on the manuscript. Clay Combrink and Caroline Krumm are acknowledged for help with analyses. This work was funded by the US National Science Foundation and the US Department of Energy. J. Six et al. / Soil Biology & Biochemistry 32 (2000) 2099–21032102 Table 1 Percent microaggregates in macroaggregates and concentrations of inter-microaggregate particulate organic matter (POM) and intra-microaggregate POM in no-tillage (NT) and conventional tillage (CT) surface layer (0–5 cm) at Sidney, NE Treatment Microaggregates in macroaggregates a Inter-microaggregate POM Intra-microaggregate POM (%) (g C kg21 sandfree macroaggregates) (g C kg21 sandfree macroaggregates) NT 47.1 ab 1.3 b 11.1 a CT 27.0 b 2.8 a 3.8 b a The data presents the % of macroaggregate soil found in microaggregates (sand-corrected). b Values followed by a different lowercase letter between management treatments are significantly different …P , 0:05† according to Tukey’s HSD mean separation test. Table 2 d 13C signature (per mille) of different aggregate size classes and particulate organic matter (POM) fractions in the surface layer (0–5 cm) of no-tillage (NT) and conventional tillage (CT at Sidney, NE). Wheat residues had a d 13C of 227.57 compared to a d 13C of 218.43 for the native grassland soil present prior to initial cultivation in 1969. Thus more negative values indicate a greater proportion of crop-derived carbon and consequently a younger age Fraction NT CT (per mille) (per mille) (per mille) Macroaggregate (250–2000 mm) 2 21.70 a Ba 2 21.96 a B Microaggregate within macroaggregate 2 21.39 a B 2 20.32 b C Intra-microaggregate POM 2 23.56 a A 2 22.73 b A Mineral fractionb 2 19.89 a D 2 18.47 b E Free microaggregate (53–250 mm) 2 20.55 a C 2 19.19 b D a Values followed by a different lowercase letter between management treatments and within a fraction are significantly different …P , 0:05† according to Tukey’s HSD mean separation test. Values followed by a different uppercase letter between fraction and within a management treatment are significantly different …P , 0:05† according to Tukey’s HSD mean separation test. b Macroaggregates contain ,53 mm particles. 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