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Microbial C[O.sub.2] production from surface and subsurface soil as affected by temperature, moisture, and nitrogen fertilisation.


Soil organic matter (SOM) is a major reservoir of organic carbon, which is estimated at about 1550 Pg, twice as much as C in the atmosphere (Raich and Potter 1995; Batjes 1996). Since the pool of C in the atmosphere is considerably smaller than the pool of C in the soil, a small relative change in the amount of C in soil will have substantial influence on the C content in the atmosphere (Yang et al. 2004). Thus, understanding the dynamics of SOM is fundamental to evaluating role of soil for C source or sink (Lal 2004; Pan et al. 2005). Most studies on the effects of land-use change on soil organic carbon (SOC) have been limited to the topsoil. This is understandable, given that the strongest effects of land-use change, the highest carbon concentrations (Veldkamp 1994), and the greatest microbial activity (Luizao et al. 1992) have been found in the topsoil. SOC in the subsoil is traditionally considered (Sombroek et al. 1993) to be stable, relatively inert humus that is not likely to be affected by a change in land use. Although organic C concentrations in subsurface horizons are generally much lower than in surface horizons, the total volume of soil contained in subsurface horizons can be very large (Trumbore et al. 1995). On a per unit carbon basis, the rate of microbial mineralisation of the organic C residing in subsurface horizons is generally low and subsurface organic C pools have long mean residence times in the soil (Desjardins et al. 1994; Trumbore 2000). Although subsurface organic C pools are not mineralised at high rates, the amount of C[O.sub.2] produced in deeper soil horizons by microbial mineralisation can be substantial and, in some soils, may account for a significant portion of total soil C[O.sub.2] production (Hendry et al. 1999; Gaudinski et al. 2000; Fierer et al. 2003). However, much less is known on responses of subsurface C stores to modifications of the soil environment.

Nitrogen (N) addition to soil has various effects on soil C[O.sub.2] emission. Some studies (Burton et al. 2002; Bowden et al. 2004) have shown that N input increased soil respiration and suggested that the stimulatory effects of N loading on ecosystems might reduce ecosystem C storage (Aber et al. 1993; Cao and Woodward 1998). Conversely, N fertilisation has also been observed to reduce organic C decomposition and suppress soil respiration, resulting in an increase in SOC (Bowden et al. 2000; Burton et al. 2002; Foereid et al. 2004). Few studies have examined the response of soil respiration on N addition in subsurface soils.

Sanjiang Plain is located in the eastern part of Heilongjiang province, north-east China, and is bordered by Russia. It covers an area of 10.89 x [10.sup.10] [m.sup.2], which was mostly dominated by marshes in 1893, and is presently the second largest mire in China (Liu and Ma 2000). The drainage and use of marshes for agricultural fields such as rice paddies and upland crops has occurred in the past 50 years with the population growth, resulting in the increase in cultivated land from about 2.9 x [10.sup.8] [m.sup.2] in 1893 to 4.57 x [10.sup.10] [m.sup.2] in 1994 (Liu and Ma 2000). Under human disturbance in the past half century, the environment in Sanjiang Plain has undergone significant change. Average soil water content decreased from 42% and 50% to 27% and 35% for surface (0-4).1 m) and subsurface (0.5.0-0.6.0m) soil, respectively, after tillage (J. B. Zhang, unpublished data), whereas, average soil temperature in the growing season increased from 14.7 [+ or -] 4.1[degrees]C and 7.2 [+ or -] 3.5[degrees]C to 22.2 [+ or -] 3.8[degrees]C and 16 [+ or -] 2.1[degrees]C for 0.1.0m and 0.6m horizon, respectively, after tillage (J. B. Zhang, unpublished data). Average N fertilisation has increased from 80kg N/ha in 1980 to 250kg N/ha in 2002in the region. Human activity can significantly affect the rates of microbial C[O.sub.2] production in soils by directly or indirectly altering the soil environmen (Tate 2000). However, there has been little attention to responses of microbial C[O.sub.2] production in the subsurface soil horizon to modifications of the soil temperature, moisture, and N addition in the freshwater marsh of the Sanjiang Plain.


We hypothesised that environmental factors such as soil moisture, soil temperature, and soil N levels affect the rates of SOC mineralisation and the nature of the controls on microbial C[O.sub.2] production to change with depth through the soil profile in the freshwater marsh of the Sanjiang Plain, since the microbial communities residing in subsurface horizons are distinct in composition from those found in surface horizons (Fierer et al. 2003).


Site characteristics and sampling

The study site is located at the Sanjiang Plain, in Heilongjiang province, north-east China, at approximately 48[degrees]36'N, 130[degrees]34'E (Fig. 1). The average altitude is 51.3-75.5m. Mean annual temperature is 1.9[degrees]C, with an average frost-free period of 125 days. Mean annual precipitation is 550-560 mm, with July and August accounting for > 65% of the total precipitation (Liu and Ma 2000).

We selected 3 intact Deyeuxia angustifolia wetlands. The parent material is Quaternary Period sediment, classified as Albaquic Paleudalfs, with silty clay texture. Soil samples were taken in May 2006 at 0.0.1, 0.1-0.2, 0.2-0.4, and 0.4-0.6m depths. Three pits as replicates were sampled at each site. For each horizon, 3 replicates with 0.1 m (length) by 0.05 m (width) by 0.1 m (depth) or 0.1 m (length) by 0.05 m (width) by 0.2 m (depth) were sampled and mixed. Meanwhile, we randomly sampled 3 soil cores to measure bulk density of each depth. The samples were immediately transported back to the laboratory, sieved to 2 mm, homogenised, and stored at 4[degrees]C for no more than 2 weeks before the start of the individual experiments. Prior to sieving, we removed all visible root and fresh litter material from the samples. Care was taken to prevent cross-contamination of the soil samples during and after collection.

Selected physical and chemical characteristics of the soil profile are given in Table 1. The total C and N content was determined using a Fisons NA1500 C/N analyzer. Soil inorganic C concentrations, as determined by standard methods (Allison and Moodie 1965), were very low in the profile samples, so total C is equivalent to total organic C and respiration measurements should not be affected by carbonate dissolution. Soil pH was measured with a pH meter (Coming Model 320) after equilibrating 15g of dry soil with 45 mL of deionised water for 30 min. Particle size was measured using standard methods. We used the chloroform fumigation-extraction method described by Zhang et al. (2006) to measure the microbial biomass levels of samples.

Experiment 1: Soil temperature and soil microbial C[O.sub.2] production rates

We tested the influence of soil temperature on short-term C mineralisation rates through the soil profile. Soil samples (10 g dry-weight equivalent) were incubated at 60% water-holding capacity (WHC) in I-L glass jars sealed with gas-tight lids fitted with rubber septa. Vials with 10mL C[O.sub.2]-free water was contained in the jars, avoiding any loss of water during incubation. We used separate sets of replicate samples to measure respiration rates at each of 7 temperatures (5-35[degrees]C, increments of 5[degrees]C). Soil C mineralisation was measured as C[O.sub.2] production at 1, 2, 3, 4, and 5 days. On each measurement occasion, 10-mL headspace samples were collected through a syringe from each jar, and the C[O.sub.2] concentration was measured by HP 4890 gas chromatography. The jars were flushed with ambient air and resealed for the next measurement. A set of controls (jars without soils) was used as a background reference.

Experiment 2: Soil water content and the soil microbial C[O.sub.2] production rates

We determined the influence of soil water content on C mineralisation rates through the soil profile. We chose to adjust the samples to a series of soil water content (20, 40, 60, 80, 100% WHC). Three replicate soil samples from each depth were adjusted to each of 5 target soil water contents, and after an equilibration period, respiration rates were measured simultaneously on all samples. Soil samples were adjusted to water contents (as determined by preliminary experiments) by either drying at 20[degrees]C or wetting with deionised [H.sub.2]O. Individual soil samples (~10g dry weight) were placed inside 1-L glass jars sealed with gas-tight lids. All samples were preincubated simultaneously at 20[degrees]C for 3 days. After this equilibration period, samples were maintained at 25[degrees]C. Soil C mineralisation was measured as C[O.sub.2] production at 1, 2, and 3 days. On each measurement occasion, 10-mL headspace samples were collected through a syringe from each jar, and the C[O.sub.2] concentration was measured by HP 4890 gas chromatography. The jars were flushed with ambient air and resealed for the next measurement. A set of controls (jars without soils) was used as a background reference.

Experiment 3: N limitations to C[O.sub.2] production

We assessed how N amendments to soil profile samples affect C mineralisation rates for each of the 3 treatments: addition of 5 [micro]g N/g soil ([N.sub.5]), addition of 10 [micro]g N/g soil ([N.sub.10]), and control. Four replicate soil samples (10 g dry-weight equivalent each) were weighed into individual 1-L glass jars sealed with gastight lids. After the moisture contents of all samples were adjusted to approximately 60% WHC by the addition of deionised [H.sub.2]O, all samples were incubated at 20[degrees]C for 3 days. After this preliminary incubation period, 1 mL of the appropriate N[H.sub.4]N[O.sub.3] solution was added to each sample, adjusted to 5 [micro]g N/g soil and 10 [micro]g N/g soil, respectively. Immediately after the addition of the N solutions, all tubes were sealed with gas-tight lids and soil C mineralisation was measured as C[O.sub.2] production at 1, 2, 3, 4, and 5 days, using the technique described for Expt 1.

Data analysis

For all 3 experiments, we calculated the average respiration rates (mg C/g over the incubation period (5 days for Expts 1 and 3, 3 days for Expt 2). The actual respiration rates vary considerably between samples collected from different profile depths. In order to compare the sensitivity responses of soils from different depths to the various treatments and to make variances independent of means, we normalised all respiration data using the procedures described in the captions for Figs 2-4. Both the normalised, or relative, respiration rates and the actual respiration rates are reported. In Expt 1, the relationship between soil temperature and the soil respiration was fitted using an exponential model (Hashimoto 2005):

R = [Ae.sup.kT] (1)

where R is the soil respiration rates, A and k are constants, and T is the soil temperature ([degrees]C). We also calculated the [Q.sub.10] value. [Q.sub.10] is the factor by which the C[O.sub.2] production rate increases when the temperature is increased by 10[degrees]C; it is a widely used parameter in studies of soil respiration. [Q.sub.10] can be expressed as:

[Q.sub.10] = ([Ae.sup.k(T+10)])/[Ae.sup.kT] = [e.sup.10k] (2)




Values for [Q.sub.10] and the rate constant A in Eqn 1 were compared using 1-way ANOVAs in order to assess the significance of soil depth on specific respiration rates (A) and the temperature responses of respiration rates ([Q.sub.10]).

We used Eqn 3, a quadratic equation function, to summarise the response of respiration rates to the range of water content:

y = [ax.sup.2] + bx + c (3)

where y is the soil respiration rate at a given water content, x is the water content, and a, b, and c are constants. We conducted 1-way ANOVA procedures to determine the effect of soil depth on 'a' values. We also used 2 sample t-tests to compare the average relative respiration rates for surface (0-0.20m) and subsurface (0.2-0.6m) soil samples at specific soil water content.

For Expt 3, we conducted 2 separate sets of 1-way ANOVA. Within each sampling depth, we compared actual respiration rates with the various treatments to determine if N additions had a significant effect on respiration rates relative to the control treatment. We also compared the influence of soil depth on relative respiration responses with each of the 2 N amendments ([N.sub.5], [N.sub.10]).

Results and discussion

Soil temperature and microbial C[O.sub.2] production rates Soil respiration rates increased between 5[degrees]C and 35[degrees]C in all samples (Fig. 2a). The exponential function (Eqn 1) used to describe the relationship between soil respiration and soil temperature fitted the individual datasets well and the [R.sup.2] values were always >0.90 for each field replicate sample. The mean values for the rate constant declined exponentially with soil depth (Table 2). The [Q.sub.10] values (Table 2) significantly increased with soil depth through the soil profile (P < 0.05). In each case, the [Q.sub.10] values for the surface samples (0-0.2 m) were significantly lower (P<0.05) than the [Q.sub.10] values for the subsurface samples (0.2-0.6 m). Relative respiration rate was also significantly increased with soil depth through the soil profile (P<0.05) (Fig. 2b). The increase in [Q.sub.10] values and relative respiration rate with depth was evidence that C mineralisation rates were more sensitive to temperature in subsurface soil horizons than in surface horizons.

We estimated that [Q.sub.10] values for the surface soils were 2.6 (0-0.1 m) and 2.8 (0.1-0.2m), within the range of [Q.sub.10] values (generally 1.8-3) reported in similar studies (Raich and Schlesinger 1992; Howard and Howard 1993; Kirschbaum 1995; Katterer et al. 1998). However, the [Q.sub.10] values calculated for the subsurface soil samples were higher than most of the [Q.sub.10] values reported in the literature. It was clear that organic matter mineralisation became more temperature-dependent with depth through the soil profile. Similarly, Lomander et al. (1998) reported that at 15-25[degrees]C, C[O.sub.2] production was more strongly influenced by temperature in subsoil (0.3-0.55m) than in topsoil (0-0.25m) horizons. However, Winkler et al. (1996) observed the opposite trend, with the respiration rates in the surface A horizon having a greater temperature sensitivity than rates in the underlying B horizon.

There were 2 possible explanations as to why respiration rates were more sensitive to temperature in the subsurface soil than the surface soil: (1) differences in microbial community composition, or (2) an interaction between C[O.sub.2] production and nutrient availability.

We know that subsurface microbial communities were distinct from surface communities (Fierer et al. 2003) and that microbial communities may have different thermal optima due to physiological adaptations to specific temperature regimes (Stark and Firestone 1996; Balser 2000). In this study, where average annual temperatures through the profile differ by up to ~7[degrees]C (J. B. Zhang, unpublished data), differences in the thermal optima of the microbial communities may partly account for the significant increase in [Q.sub.10] values with soil depth.

The other possible explanation for the observed increase in [Q.sub.10] values with soil depth was that there was a positive feedback between C[O.sub.2] production and the mineralisation of nutrients other than C, especially in the soil subsurface. Higher soil temperatures may increase the rates of mineralisation of key nutrients such as N. An increased availability of N would enable soil microorganisms, particularly those in nutrient-limited environments, to produce more of the enzymes required for C mineralisation (Tate 2000). Our data suggested that the subsurface microorganisms were more N-limited than in the surface horizons, so this interaction between C mineralisation and N availability may be another possible explanation for the observed increase in [Q.sub.10] values with soil depth.

Soil water content and microbial C[O.sub.2] production rates

Soil water content obviously affected microbial C[O.sub.2] production rates (Fig. 3a). The maximum respiration rate was measured at 60% WHC for each sample. The quadratic equation function adequately describes the relationship between soil respiration and soil water content, and the [R.sup.2] values were >0.80. The sensitivity of microbial C[O.sub.2] production rate response to soil water content for surface soils (0-0.2 m) was slightly lower than for subsurface soils (0.2-0.6 m).

The dependence of relative respiration rate mineralisation rates on soil water content was summarised by the quadratic equation function, and the [R.sup.2] values were > 0.80. Although the slope of C mineralisation rates v. soil water content did not change significantly across the full range of tested water content, the surface soils tended to have lower relative respiration rates at 40 and 60% WHC (Fig. 3). If we compared the average relative respiration rates of surface (0-0.2m) and subsurface (0.2-0.6m) soil samples at these 2 water potentials, we found that the sensitivity of microbial C[O.sub.2] production rate response to soil water content for surface soils was significantly lower (0-0.2 m) than that for subsurface soils (0.2-0.6 m) (P<0.05 and 0.01, respectively).

Across the full range of tested soil water content, microbial respiration rates in surface and subsurface horizons responded similarly to changes in soil water content (Fig. 3). The maximum respiration rate was measured at 60% WHC soil water content for each sample, according with the quadratic equation function. Microbial C cycling was linked to soil water status (Parkin et al. 1996). Linn and Doran (1984) reported a close relationship between microbial respiration and soil moisture content, with a peak of activity at 60% water-filled pore space (WFPS). Doran et al. (1990) reported an optimum WFPS value of 55% for coarse-textured soils. Some studies have indicated that fluxes exhibited significant negative relationships with soil moisture due to the reduction in the activity of obligate aerobic microbes, caused by excessive water above the optimum WFPS (Rochette et al. 1991; Bowden et al. 2004).

If we independently examine respiration rates at the midrange of tested water content (40 and 60% WHC), we find that surface soils have lower sensitivity of microbial C[O.sub.2] production rate response to soil water content than subsurface soils (Fig. 3b). These results suggest that conditions of moderate drought may have a larger relative impact on the rates of C mineralisation from subsurface soil horizons.

Nitrogen limitation to microbial C[O.sub.2] production

The responses of actual soil respiration rates to N fertilisation were different for surface and subsurface soils (Fig. 4a). In the surface soils (0-0.2m), the addition of N caused a slight decrease in respiration rates compared with the control (Fig. 4a), while in the subsurface soils (0.2-0.6m), the addition of N tended to increase microbial C[O.sub.2] production rates relative to the control, and the addition of 10 [micro]g N/g soil caused the greatest increase (Fig. 4a). The response of microbial C[O.sub.2] production rates to soil water content was significantly related to soil depth (Fig. 4b).

At the surface depths, C mineralisation is not strongly limited by N, since the addition of N tends to lower respiration rates relative to the control (Fig. 4b). In subsurface soil, microbial C[O.sub.2] production was strongly N-limited; at 0.4-0.6m depth, the addition of 10 [micro]g N/g soil resulted in approximately a 2-fold increase in C mineralisation rates relative to the control (Fig. 4b). Other studies also found that rates of C metabolism in subsurface samples were often limited by N availability (Thornton-Manning et al. 1987; Swindoll et al. 1988; Ajwa et al. 1998).

We were not able to determine the reasons why surface and subsurface soils had distinct microbial responses to N additions. Comparing data from the literature, the effects of N additions on the microbial mineralisation of soil organic C tend to be highly variable. N additions can had a positive effect, a negative effect, or no effect on microbial respiration rates (Fog 1988). The particular response of a soil to N additions was likely to be a function of a variety of factors, including microbial community composition, microbial physiology, nutrient concentrations, and the chemistry and availability of organic C (Fog 1988; French 1988; Vance and Chapin 2001).

The vertical distribution of C[O.sub.2] production

Using measured soil respiration rates of control in Expt 3 and bulk density, we calculated the vertical distribution of C[O.sub.2] production in the wetland soil profile. Soil respiration rates were highest in the topsoil (0.0-0.1 m) and rapidly decreased with soil depth (Fig. 4). Soil respiration rates expressed on mass basis do not take into account the large soil volume that these soils have in the subsoil. For this reason, we also expressed the soil respiration rates on an area basis using the bulk density data. While our laboratory data on soil respiration rates cannot be assumed to closely parallel respiration levels in the field, the area-based values are heuristically useful in demonstrating that a relatively low basal respiration multiplied over a large volume of soil can result in large values of total respiration. Such area-based values for soil respiration rates were similar in the soil layers 0.2-0.6 m and in the top 0.2 m (Table 2). The amount of soil respiration in the soil layers 0.2-0.6 m was 49% of the total amount over the whole soil profile. Although traditionally it is assumed that the microbial activity is absent or insignificant below the topsoil, Richter and Markewitz (1995) reported considerable amounts of bacteria and fungi in a deeply weathered temperate-zone Ultisol. Veldkamp et al. (2003) also reported that the amount of soil respiration in the subsurface soil (0.3-4 m) was about 50% of the total amount over the whole soil profile. During a 2-year period of monitoring of C[O.sub.2] concentrations down the soil profiles at old-growth forest sites, the highest C[O.sub.2] concentrations were consistently at the lowest sampling depth, 3.5 m in the residual soils, and 2.5 m in the old alluvial soils (Schwendenmann et al. 2003). That the highest C[O.sub.2] concentrations in the soil air space are always sampled at the lowest depth can only be explained if there is a C[O.sub.2] source at or below the lowest sampling depth. The depleted stable isotope signature of this subsoil C[O.sub.2] points to a biological C[O.sub.2] source, and microbial activity is therefore the most likely source of this deep C[O.sub.2] (Veldkamp et al. 2003).


The responses of microbial C[O.sub.2] production to changes of soil moisture, soil temperature, and soil N levels varied with soil depth through the profile. The [Q.sub.10] values and relative respiration rate significantly increased with soil depth through the soil profile (P<0.05), indicating that C mineralisation rates were more sensitive to temperature in subsurface soil horizons than in surface horizons. Nitrogen additions also led to comparatively large increases in the microbial C[O.sub.2] production from subsurface, suggesting microbial C[O.sub.2] production was strongly N-limited in subsurface soil. Our results implicated that the nature of the controls on microbial C[O.sub.2] production changed with depth through the soil profile. By increasing soil temperature and N inputs to the soil subsurface, climate change, land use change and fertilisation of soils by human activity may increase the C mineralisation rate in subsurface soil horizons. Because there were large quantities SOC in subsurface horizons, any increase in C mineralisation rate could obviously affect the C cycle.


We would like to thank the reviewers for their time and suggestions.

Manuscript received 21 September 2007, accepted 3 March 2008


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Xiaobin Jin (A,B), Shenmin Wang (A), and Yinkang Zhou (A)

(A) Department of Land Resources and Tourism Sciences, Nanjing University, No. 22 Han kou Road, Nanjing 210093, China.

(B) Corresponding author. Email:
Table 1. Soils physicochemical properties used in this study

Data shown are means with the standard errors in parentheses (n=3).
Values within a column followed by the same letter are not
significantly different (P>0.05). SOC, Soil organic carbon; C/N, ratio
of soil organic carbon to total nitrogen; MBC, microbial biomass carbon

Depth pH SOC C/N MBC
(m) (g/kg) (mg/kg)

0-0.1 5.5 129.1 (6.8) 22.7 (3.4) 3547.3 (432)
0.1-0.2 5.9 78.2 (4.1) 15.2 (4.4) 2868.5 (126)
0.2-0.4 6.4 11.0 (0.6) 14.9 (1.4) 346.5 (56)
0.4-0.6 6.9 9.1 (0.5) 13.5 (1.6) 82 (11)

Depth Bulk density Particle size composition (g/kg)
(m) (g/[cm.sup.3) >0.05 mm 0.005-0.05 mm <0.005 mm

0-0.1 0.46 (0.2) 382 (62) 462 (34) 156 (8)
0.1-0.2 0.53 (0.1) 253 (39) 466 (29) 281 (35)
0.2-0.4 1.3 (0.2) 116 (31) 522 (61) 362 (37)
0.4-0.6 1.5 (0.1) 92 (15) 533 (72) 375 (36)

Table 2. Temperature dependence on respiration rates and the
vertical distribution of COZ production through the soil profile

[Q.sub.10] and the rate constant A were parameters calculated from
Eqns 1 and 2, respectively. Values were calculated for the temperature
range 5-35[degrees]C. Mean A and [Q.sub.10] values followed by the same
letter are not significantly different (P>0.05) between depths.
Standard errors are reported in parentheses (n=3 for each sampling
depth). The soil respiration rates were expressed on an area basis
using the bulk density data and the vertical distribution of
C[O.sub.2] production calculated

Sampling Vertical distribution of
depth (m) A [Q.sub.10] C[O.sub.2] production (%)

0-0.1 7.7a (0.3) 2.6a (0.09) 38
0.1-0.2 2.4b (0.1) 2.8a (0.1) 13
0.2-0.4 1.1c (0.08) 3.1b (0.2) 25
0.4-0.6 0.7d (0.03) 3.5b (0.2) 24
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Author:Jin, Xiaobin; Wang, Shenmin; Zhou, Yinkang
Publication:Australian Journal of Soil Research
Article Type:Report
Geographic Code:9CHIN
Date:May 1, 2008
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