Soil Science Society of America Journal 64:201-207 (2000)
© 2000 Soil Science Society of America
DIVISION S-3-SOIL BIOLOGY & BIOCHEMISTRY
Root-Derived Carbon and the Formation and Stabilization of Aggregates
W.J. Galea,
C.A. Cambardellaa and
T.B. Baileyb
a USDA-ARS National Soil Tilth Lab., 2150 Pammel Dr., Ames, IA 50011 USA
b Dep. of Statistics, Iowa St. Univ., Ames, IA 50011 USA
cindyc{at}nstl.gov
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ABSTRACT
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It is hypothesized that particulate organic matter (POM) contributes to aggregate stability. However, little is known about the dynamics of the POM fraction or its role in aggregate formation. A simulated no-till study was conducted to examine changes in free and aggregate-associated POM during the decomposition of in situ 14C-labeled roots during a 1-yr incubation in a loess-derived silt loam. Two water pretreatments (capillary-wetted and slaked) were applied to soil samples collected during the incubation, and the samples were then wet sieved to obtain five aggregate size fractions. Densiometric separations were used to isolate free and released POM (frPOM) and intraaggregate POM (iPOM). Small macroaggregates (250–2000 µm) were enriched in iPOM-14C on Day 0 which suggested that many of these aggregates formed around cores of new, root-derived POM during the growth and senescence of the oat plants. Slaking resulted in the disruption of many of the small macroaggregates (250–2000 µm) and a large increase in frPOM-14C on Day 0. The amount of 14C released into the frPOM pool with slaking declined with time. In contrast, there was a significant linear increase in the amount of new, root-derived iPOM-14C in large microaggregates (53–250 µm) that were released when unstable macroaggregates (>250 µm) slaked. These data support the hypothesis that new microaggregates are formed within existing macroaggregates and provide strong evidence that, in no-till, aggregate formation and stabilization processes are directly related to the decomposition of root-residue and the dynamics of POM C in the soil.
Abbreviations: frPOM, free and released particulate organic matter • iPOM, intraaggregate particulate organic matter • POM, particulate organic matter • SOM, soil organic matter
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INTRODUCTION
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AGGREGATES DETERMINE MANY PHYSICAL PROPERTIES in the soil and serve as control points for the decomposition of organic matter (Elliott and Coleman, 1988). Despite the importance of stable aggregates in the soil, many questions regarding the processes by which aggregates are formed and stabilized remain unanswered. Tisdall and Oades (1982) presented a conceptual, hierarchical model that describes the formation of stable aggregates in grassland soils. According to the model, highly stable microaggregates (<250 µm) are pulled together and temporarily stabilized by the enmeshing effect of plant roots and fungal hyphae to form relatively less stable macroaggregates (>250 µm). The alternative view of aggregate organization is that macroaggregates form first in the soil and that microaggregates form around organic material that is occluded within the macroaggregate (Oades, 1984; Elliott and Coleman, 1988). Specifically, Golchin et al. (1994, 1998) proposed that macroaggregates form as POM (plant or root debris) becomes colonized by microorganisms and encrusted by mineral materials. As the POM decomposes, it becomes fragmented and the overall stability of the macroaggregate decreases. The unstable macroaggregate eventually fractures, resulting in the release of newly formed microaggregates containing the residual POM.
This paper is the third in a series of three manuscripts examining fundamental aspects of aggregate dynamics under simulated no-till conditions. Paper one (Gale and Cambardella, 2000, this issue) reported clear differences in the partitioning of root-derived and surface residue–derived new C to the soil and atmospheric sinks, specifically that a greater percentage of root- than surface residue–derived C is retained in the soil. Paper two (Gale et al., 2000, this issue) presented evidence that the most stable macroaggregates in soil, defined as those able to survive slaking, possess higher concentrations of new, primarily root-derived POM C than do less stable macroaggregates. The objective of this final paper is to present a conceptual model of aggregate formation, stabilization, and degradation based on data that quantifies the movement of new C into and out of soil C pools with time. The model is conceptualized using data that quantifies changes with time in total amounts of aggregate-associated 14C, iPOM-14C, and frPOM-14C per kilogram of soil. Most aggregation studies have examined the characteristics of stable aggregates. This study was unique in attempting to characterize changes with time in the material that is associated with unstable aggregates.
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Methods
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Experimental Setup
Detailed descriptions of the experimental set-up, 14C-labeling procedure, aggregate separations, and soil organic matter (SOM) fractionation sequences were reported previously (Gale and Cambardella, 2000, this issue; Gale et al., 2000, this issue). Briefly, soil was collected from the surface horizon of a Monona silt loam soil (fine-silty, mixed, mesic Typic Hapludoll) and passed through an 8-mm sieve in the field-moist state. The moist soil was mixed and the equivalent of 2420 g of dry soil was placed into each of 30 plastic pots. We planted oats (Avena sativa cv. Ogle) in the pots and placed 15 pots in each of two growth chambers. The plants in one chamber were pulse labeled with 14CO2 on 15, 20, 26, 31, 37, 46, and 52 d after emergence and the plants in the other chamber were not labeled. At senescence, the plants were cut off at the soil surface and the leaves were separated from the stems and dried. Dried unlabeled oat leaves were placed on the soil surface of pots containing in situ, 14C-labeled roots and soil. The pots were arranged in a completely randomized design in a growth chamber at 25°C and incubated for 1-yr.
Three pots were destructively sampled on Days 0, 90, 180, 270, and 360. After the surface residue was removed, the soil and roots in each pot were separated. Roots that were longer than 
2 cm were removed by hand. The moist soil remaining in each pot was passed through an 8-mm sieve, air dried, and stored at room temperature.
Aggregate Separations
Aggregate size fractions were isolated by wet sieving using air-dry 8-mm sieved soil. Two 100-g subsamples were capillary-wetted to 280 g H2O kg-1 dry soil and two 100 subsamples were left air dry. Samples from these treatments will be referred to as capillary-wetted and slaked, respectively. The samples were allowed to equilibrate overnight at 4°C and were then wet sieved to obtain five aggregate size fractions (µm diameter): (i) >2000, (ii) 250 to 2000, (iii) 53 to 250, (iv) 20 to 53, and (v) <20. All size fractions were dried at 70°C. Subsamples from each aggregate size class were ground on a roller mill to pass a 250-µm sieve and stored at room temperature.
Separation of Free and Released Particulate Organic Matter and Intraagregate Particulate Organic Matter
Subsamples (10 g) from each of the three largest aggregate size classes were moistened to 280 g H2O kg-1 and equilibrated overnight at 4°C. Any free POM (frPOM) present was isolated from each sample using sodium polytungstate (Geoliquids Inc., Prospect Heights, IL)1
adjusted to a density of 1.85 g cm-3. The frPOM was collected at the surface of the heavy liquid and was removed by aspiration after equilibration overnight.
The material that did not float at 1.85 g cm-3 was centrifuged at 900 x g for 10 min and the soil pellet was rinsed into a polypropylene bottle. The sample was dispersed with 100 mL of 5 g L-1 sodium hexametaphosphate and shaken overnight on a reciprocal shaker. The dispersed samples were passed through a 53-µm sieve, rinsed with water, and the material retained on the sieve was backwashed onto a 20-µm nylon filter and rinsed into beakers with sodium polytungstate (1.85 g cm-3). The samples were allowed to separate overnight and the floating iPOM was isolated by aspiration.
The frPOM and iPOM fractions were dried at 50°C, ground to a fine powder in a ball mill and stored at room temperature.
Carbon and Nitrogen Determination
The amount of 14C in each fraction was measured by combusting subsamples in a Harvey Biological Oxidizer, model OX500 (R.J. Harvey Instrument Corp., Hillsdale, NJ). The 14C released during oxidation was trapped in Harvey's 14C cocktail and counted on a 1900 TR Liquid Scintillation Analyzer (Packard Instrument Co., Downers Grove, IL).
Calculations and Statistical Analyses
The amount of 14C in a given fraction was calculated by multiplying the concentration of 14C by the mass of the fraction. Aggregate 14C (-frPOM) was calculated as the difference between total 14C in a size class and frPOM-14C in the fraction. Because we were interested in the total amount of 14C in each fraction and not the 14C concentration, there was no need to make a correction for the sand content of the aggregates.
There were two factors in our experiment which was analyzed as a split plot. The whole plot factor was water pretreatment (capillary-wetted or slaked) prior to sieving. Five aggregate size classes were isolated for each water pretreatment. Thus aggregate size was the split plot factor. These two factors yielded a total of 10 treatment combinations that were measured on five dates (Days 0, 90, 180 270, and 360).
Changes in each variable across time (days) were characterized for each water pretreatment and size combination with regression models that included linear and quadratic components. Also, to examine the effect of water pretreatment, we completed a t test to determine if the difference (net change) between each mean in the slaked pretreatment and the corresponding mean in the capillary-wetted was significantly different from zero.
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Results and discussion
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We differentiated stable macroaggregates from unstable macroaggregates based on their resistance to slaking. When air-dry soil is submerged in water, the air that is trapped inside soil pores is rapidly displaced with water. Slaking occurs as a consequence of the sudden release of this large buildup of internal air pressure, which disrupts unstable macroaggregates. In contrast, slowly wetting the soil by capillary action allows air to escape with minimal disruption to macroaggregates. Therefore, the macroaggregate pool for the capillary-wetted treatment contains both stable and unstable macroaggregates, but the macroaggregate pool in the slaked treatment contains only stable macroaggregates. The unstable macroaggregate pool is calculated as the difference between these two pools. For example, on Day 0, the small macroaggregate (250–2000 µm) fraction contained 7.84 and 4.19 µBq kg-1 soil in the capillary-wetted and slaked treatment, respectively (Table 1)
. The difference in 14C between the two treatments, 3.65 µBq kg-1 soil, represents the amount of 14C that was present in unstable, small macroaggregates (250–2000 µm) (Table 1, net change). We quantified the amount of material released from unstable macroaggregates (>250 µm) by calculating the net increase with slaking in the amount of 14C in the three smaller size classes. For example, on d 0, the large microaggregate (53–250 µm) fraction contained 2.62 and 3.86 µBq kg-1 soil in the capillary-wetted and slaked treatment, respectively (Table 1). The difference between the two treatments, 1.24 µBq kg-1, represents the net increase in the amount of 14C in that size class due to slaking (Table 1, net change). The specific activity of the material that was gained or lost from each fraction with slaking was estimated by dividing the net change in 14C of the fraction by the net change in total organic C.
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Table 1 Changes with time in the aggregate 14C content (excluding frPOM ) within aggregate size class under two different prewetting treatments on a whole soil basis
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Aggregate Carbon-14
The distribution of root-derived 14C in the various aggregate size classes was strongly influenced by water pretreatment. In the capillary-wetted treatment, more than 60% of the root-derived aggregate-14C was associated with macroaggregates (>250 µm) (Table 1). Rapid wetting in the slaked treatment resulted in the disruption of unstable macroaggregates and a net increase in the amount of aggregate-14C in the microaggregate size classes (<250 µm). The total amount of aggregate-14C changed significantly with time during the 1-yr incubation (Table 1). The largest changes occurred in the slaked treatment, where the total amount of 14C in small macroaggregates (250–2000 µm) decreased and the amount of 14C in large microaggregates (53–250 µm) increased significantly with time. Similarly, Angers et al. (1997) observed that when labeled wheat residue was incorporated into the soil, macroaggregates were initially enriched in new C relative to microaggregates, but later the proportion of new C in macroaggregates decreased and the enrichment in microaggregates increased. The loss of 14C from macroaggregates and the simultaneous increase in microaggregate-14C suggests that new, root-derived C moved from macroaggregates into microaggregates. A possible mechanism for this transfer is presented in the following section.
Intraaggregate Particulate Organic Matter and Free and Released Particulate Organic Matter
Partitioning of iPOM-14C was similar to the pattern we observed for aggregate-14C (Table 2)
. Most (>63%) of the iPOM-14C was occluded within macroaggregates (>250 µm) in the capillary-wetted treatment. The disruption of unstable macroaggregates (>250 µm) by slaking resulted in a 50 to 75% decrease in the amount of iPOM-14C contained in the macroaggregate (>250 µm) size classes with the subsequent redistribution of the labeled organic material into the frPOM pool or into smaller aggregate size classes.
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Table 2 Changes with time in the iPOM-14C content within size class under two prewetting treatments on a whole soil basis
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On Day 0, the total amount of iPOM-14C in small macroaggregates (250–2000 µm) was much higher than in the other aggregate size classes (Table 2), which suggests these aggregates formed around cores of root-derived POM during the growth and senescence of oat plants. Rapid wetting in the slaked treatment resulted in a total loss of 61% (2.01 µBq kg-1 soil) of iPOM-14C from macroaggregates (>250 µm) (Table 2, net loss). This indicates that many of the newly formed macroaggregates were unstable. The iPOM present within unstable macroaggregates has two potential fates: (i) it may remain occluded within smaller aggregates that are released by slaking or (ii) it may be released and exist freely outside of aggregates (frPOM). On Day 0, there was a large net increase due to slaking in the dry weight of large microaggregates (53–250 µm) (Gale et al., 2000, this issue), however, the net change in iPOM-14C of large microaggregates (53–250 µm) was not significantly different from zero (Table 2, net change). This means that there was essentially no new, root-derived iPOM in large microaggregates (53–250 µm) released from unstable macroaggregates (>250 µm) on Day 0. In contrast, slaking resulted in a significant net increase in the amount of medium-size (250–2000 µm) frPOM-14C (Table 3
, net change) and the net increase was similar in size to the net loss of iPOM-14C from macroaggregates (>250 µm) (Table 2, net change). Thus, essentially all the root-derived iPOM in unstable macroaggregates on Day 0 was released into the frPOM pool. The data from Day 0 suggest that many macroaggregates were loosely formed around medium-size (250–2000 µm), root-derived POM during the growth and senescence of the oat plants. These newly formed aggregates were relatively unstable and many were disrupted by the rapid wetting resulting in the release of root-derived POM into the frPOM pool. The large microaggregates (53–250 µm) released from the unstable macroaggregates (>250 µm) on Day 0 did not contain a significant amount of iPOM-14C. In other words, during the growth and senescence of the oat plants, the data suggest that relatively unstable macroaggregates developed in the oat rhizosphere but stable microaggregates did not form around decomposing bits of new, root-derived POM inside these unstable macroaggregates.
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Table 3 Changes with time in the frPOM-14C content within size class under two prewetting treatments on a whole soil basis
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On Day 90, the disruption of unstable macroaggregates (>250 µm) resulted in a significant net increase in the amount (Table 2, net change) of iPOM-14C in the large (53–250 µm) microaggregate size class. That is, on Day 90, the microaggregates released from unstable macroaggregates contained recently occluded, root-derived 14C-labeled POM. Since the 14C-labeled POM was derived from root residue, the data indicate the microaggregates formed around decomposing roots within macroaggregates between Days 0 and 90. Slaking also resulted in a net increase in the amount of frPOM-14C in the soil on Day 90 (Table 3, net change), but this increase was significant only for the fine (53–250 µm) fraction. This means that the amount of material released from unstable macroaggregates (>250 µm) into the frPOM pool on Day 90 was much less than on Day 0 and that the released POM was much smaller in size than on Day 0. The total amount of iPOM-14C in small macroaggregates (250–2000 µm) declined between Days 0 and 90 (Table 2), suggesting that medium-size (250–2000 µm) iPOM occluded in unstable macroaggregates on Day 0 was rapidly decomposed during the first 3 mo of the incubation. The iPOM probably fragmented into smaller pieces as it decomposed and the POM fragments became the cores of newly-forming microaggregates. The root-derived iPOM may have been mineralized and released as 14CO2. For example, we previously reported that nearly 40% of the original root-derived 14C in the soil was evolved as 14CO2 within the first 90 d of incubation (Gale and Cambardella, 2000, this issue). It is also likely that a portion of the macroaggregate-iPOM-14C was redistributed into other fractions in the soil as decomposition proceeded. This idea is supported by the observations that large microaggregate-iPOM-14C (53–250 µm) increased twofold between Days 0 and 90 in the capillary wetted treatment and that large microaggregates (53–250 µm) released from unstable macroaggregates (>250 µm) were more enriched in iPOM-14C on Day 90 compared to Day 0 (Fig. 1)
. In summary, during the first 3 mo of the incubation, as medium-size pieces of iPOM decomposed inside unstable macroaggregates, some of the new, root-derived C was lost through respiration as 14CO2 and some was stabilized inside microaggregates that were developing inside the unstable macroaggregates. Therefore, by Day 90, most of the macroaggregates were still unstable but many microaggregates that had formed inside the macroaggregates were stabilized.
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Fig. 1 Changes with time in the specific activity of intraaggregate particulate organic matter (iPOM) in large microaggregates released from unstable macroaggregates with slaking. The specific activity was estimated by dividing the net change in iPOM-14C of the fraction due to slaking by the net change in total (12C + 14C) iPOM-C. The bars represent the standard error
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On Days 180 and 270, we continued to observe significant net increases in large microaggregate-iPOM-14C (53–250 µm) released from unstable macroaggregates (>250 µm) (Table 2, net change). In contrast, the net change in frPOM-14C due to slaking for these two sample dates was not significantly different from zero for any of the size classes (Table 3, net change). This indicates that no new, root-derived POM was released into the frPOM pool when macroaggregates (>250 µm) slaked on Days 180 or 270. We previously reported that macroaggregate (>250 µm) stability was at a maximum during this time period (Gale et al., 2000, this issue). The data indicate that macroaggregates (>250 µm) were more resistant to slaking on Days 180 and 270 compared to the other sample dates during the incubation. The macroaggregates (>250 µm) that did slake yielded large microaggregates (53–250 µm) that were enriched in new root-derived iPOM, but no root-derived material was released into the frPOM pool. This means that after 6 mo of incubation, new root-derived POM was occluded inside stable large microaggregates (53–250 µm) which were themselves occluded within relatively stable macroaggregates (>250 µm). The macroaggregates remained relatively stable between Day 180 and 270 of the incubation.
There was a significant net increase due to slaking in iPOM-14C in the large microaggregate size class on Day 360. In fact, on Day 360, the total amount (0.55 µBq kg-1 soil) of iPOM-14C contained in large microaggregates released from unstable macroaggregates was greater than on any other sample date. Furthermore, the specific activity of large microaggregate-iPOM (53–250 µm) was 1.4 times higher on Day 360 compared to the other sample dates (Fig. 1). Overall, the data show that the amount and concentration of new, root-derived POM occluded within large microaggregates found inside unstable macroaggregates increased with time. This supports the idea that microaggregates were forming around new root-derived POM within macroaggregates throughout the incubation period.
We previously reported a decrease in the stability of both macroaggregates and large microaggregates between Days 270 and 360 of the incubation (Gale et al., 2000, this issue). In the current study, we also observed a significant net increase with slaking in fine (53–250 µm) frPOM-14C on Day 360. This indicates there were more unstable aggregates on Day 360 than on Days 180 or 270 and that aggregate-occluded POM was released into the frPOM pool as the unstable aggregates slaked. Since the material released into the frPOM pool was very small in size, it probably came from inside large microaggregates that were originally inside macroaggregates. Golchin et al. (1994) hypothesized that microaggregate stability declines as the organic core of the aggregate decomposes and the weakened microaggregate eventually breaks apart, releasing the highly decomposed core. Our results corroborate this hypothesis.
Conceptual Model
A detailed list of observations and the corresponding conclusions for each sample date are summarized in Table 4
. A conceptual model based on our observations and the hypothesis that microaggregates are formed within macroaggregates is presented in Fig. 2
and described in the following paragraphs:
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Fig. 2 Conceptual model describing the formation and stabilization of aggregates. The red color indicates root-derived 14C
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Many macroaggregates form around new root-derived POM during the period of vegetative growth and senescence of the oat plants prior to the initiation of the decomposition phase of the experiment. Most of these newly formed macroaggregates are unstable and are disrupted by slaking, resulting in the release of new root-derived POM into the frPOM pool. The new root-derived POM is labile and a significant portion of it is rapidly decomposed. The POM C is either mineralized and released as CO2 or redistributed into other organic matter fractions.
After the death of the oat plant, macroaggregates continue to form around new root-derived POM. As the dead oat roots decompose, microbial-binding agents are produced that result in an increase in macroaggregate stability with time. Increases in macroaggregate stability are accompanied by decreases in the amount of POM released by slaking. The POM entrapped inside the relatively stable macroaggregates continues to decompose. The microbial exudates produced as a result of POM decomposition become encrusted with clay particles and a microaggregate is formed within the preexisting macroaggregate.
After Day 180, the most labile portions of the POM have been decomposed. This results in a decrease in microbial activity and the subsequent production of microbial-binding agents. As a consequence, the stability of the macroaggregates begins to decline as evidenced by the release of large microaggregates which contain cores of new root-derived POM. Some of the microaggregates containing new root-derived POM C become unstable after about 1 yr and release labile POM C that is now available for further decomposition.
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Conclusions
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This study was unique in attempting to characterize changes with time in the material that is released from unstable macroaggregates upon slaking. The results corroborate the hypothesis that new microaggregates form around decomposing pieces of root-derived POM inside existing macroaggregates as suggested by Oades (1984), Elliott and Coleman (1988), and Golchin et al. (1994, 1998). Our experimental design did not allow us to completely rule out the alternative hypothesis that microaggregates are formed free in the soil and are subsequently bound together to form macroaggregates. However, the data present compelling evidence that, at least in relatively undisturbed systems like no-till, aggregate formation and stabilization processes are directly related to the decomposition of root-residue and the dynamics of POM C in the soil. Further work is needed to determine if the mechanisms of aggregate formation and stabilization are spatially compartmentalized in soil. Specifically, two interesting and important hypotheses need to be addressed: Hypothesis 1: New microaggregates are formed inside existing macroaggregates in the rhizosphere; Hypothesis 2: New microaggregates are formed outside of macroaggregates and are subsequently bound together to form macroaggregates in nonrhizosphere soil.Gale Cambardella Bailey 1999
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NOTES
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1 Reference to trade names and companies is made for information purposes only and does not imply endorsement by the the USDA. 
Received for publication July 9, 1998.
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REFERENCES
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- Golchin A., Baldock J.A., Oades J.M. A model linking organic matter decomposition, chemistry, and aggregate dynamics. In: Lal R., et al. , ed. Soil processes and the carbon cycle. Boca Raton, FL: Lewis Publ., CRC Press, 1998:245-266.
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[Abstract]
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P. Puget and L.E. Drinkwater
Short-Term Dynamics of Root- and Shoot-Derived Carbon from a Leguminous Green Manure
Soil Sci. Soc. Am. J.,
May 1, 2001;
65(3):
771 - 779.
[Abstract]
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TOP
ABSTRACT
INTRODUCTION
