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DIVISION S-3-SOIL BIOLOGY & BIOCHEMISTRY

Separating Soil Respiration into Plant and Soil Components Using Analyses of the Natural Abundance of Carbon-13

^a Agriculture and Agri-Food Canada, Soils and Crops Research and Development Centre, 2560 Hochelaga Blvd., Ste-Foy, QC, Canada G1V 2J3
^b Dep. of Biological Sciences, Univ. of Lethbridge, 4401 University Dr., Lethbridge, AB, Canada, T1K 3M4
^c Agriculture and Agri-Food Canada, Eastern Cereal and Oilseed Research Centre, Neatby Bldg., Central Experimental Farm, Ottawa, ON, Canada, K1A 0C6

rochettep{at}em.agr.ca

	ABSTRACT

TOP ABSTRACT INTRODUCTION Materials and methods Results and discussion Conclusions REFERENCES

 
In presence of vegetation, the CO₂–C produced by respiration activity in soils originates from plant C (rhizosphere respiration, R_rh) and from soil C (soil respiration, R_s). Quantitative estimates of the CO₂ produced by each source are required in many studies of C dynamics in the soil–plant system. In this study, we (i) used measurements of the ¹³C value of soil CO₂ to separate total soil respiration (R_t) into subcomponents R_rh and R_s in a maize (Zea mays L.) field under undisturbed conditions and (ii) compared these R_rh estimates with values obtained using the root-exclusion approach. The maximum contribution of R_rh to total respiration was 45%, observed in August. Estimates of R_rh increased from zero 30 d after planting to 2 g CO₂–C m^-2 d^-1 70 d after planting, remained relatively constant at that level in August, and then decreased until the end of the growing season. The total C losses as R_rh were 17% of the crop net assimilation. Estimates of R_s gradually declined from 3.3 g CO₂–C m^-2 d^-1 in late June to 1.4 g CO₂–C m^-2 d^-1 at the end of the season. Losses of soil C represented 6% of total soil C. Variable values of ¹³C of the soil CO₂ in the control plot after Day 250 made the technique less reliable late in the season. However, several observations indicated that the approach has potential to provide quantitative estimates of R_rh and R_s. First, the seasonal pattern of the R_rh estimates coincided with that of the plant growth and physiological activity. Second, the cumulated R_rh across the growing season agreed well with published data obtained using ¹⁴C labeling techniques. Third, in the maize plot, variation in the estimated R_s was closely correlated with changes in soil temperature with a Q₁₀ of 1.99 . Finally, the estimates of R_rh obtained using the isotopic approach agreed well with those obtained using the root exclusion technique.

	INTRODUCTION

TOP ABSTRACT INTRODUCTION Materials and methods Results and discussion Conclusions REFERENCES

 
RESPIRATION PROCESSES in soils produce large quantities of CO₂. Emission rates of CO₂ at the soil surface have been used for several decades as a measurement of the soil biological activity (Lundegrdh, 1924). In the absence of living plants, soil surface CO₂ emissions provide a direct assessment of the short-term dynamics of soil C (Rochette et al., 1992; Reicosky and Lindstrom, 1993). However, when plants are present, the interpretation of total soil respiration (R_t) is complicated by the CO₂ produced by rhizosphere respiration, which includes the respiration of living roots and of the microorganisms feeding on root-derived C (exudates and dead roots).

A few approaches have been developed to separate R_t into its rhizosphere (R_rh) and soil (R_s) components under field conditions. They consist of estimating either R_rh or R_s and calculating the other component by difference with R_t. The root-exclusion method calculates R_rh as the difference between CO₂ emission rates from soil volumes in which roots are either present or excluded (Hanson et al., 1999). The root-exclusion approach has been used by Hall et al. (1990) in a sunflower (Helianthus annuus L.) field but its use is most common in forest ecosystems (Hanson et al., 1999). This technique is relatively simple and has provided realistic estimates of R_rh and R_s. However, soil disturbance, absence of root–soil interactions, and differences in temperature and moisture between bare soil and soil with vegetation cover may influence R_s.

Rhizosphere respiration can be measured by pulse-labeling plants with ¹⁴C. This method provides information on the fate of recently fixed C but does not allow for the uniform labeling of all plant C pools (Lynch and Whipps, 1990). Values of R_rh using this method are therefore underestimates of the actual R_rh. Rochette and Flanagan (1997) proposed using the variations in natural abundance of ¹³C among plants to quantify R_rh. Their approach requires that the C isotopic ratio (¹³C/¹²C, ¹³C) of the growing crop contrasts with the ¹³C of the soil organic C. Under such conditions, the contribution of R_rh to total soil CO₂ can be estimated using the difference in ¹³C of the soil CO₂ between a cropped soil and a noncropped control. The ¹³C labeling approach has important advantages over other field techniques: (i) all C pools of the plant are labeled, (ii) it is a nonintrusive method, and (iii) it does not involve handling of radioactive material. On the other hand, the technique is new and the range of conditions under which it has been assessed is limited. Further testing of the technique is necessary in order to evaluate its potential to provide quantitative estimates of R_rh.

In this study, we (i) used measurements of the ¹³C value of soil CO₂ to separate R_t into R_rh and R_s in a maize field under conditions typical of the agricultural practices in northern North America and (ii) compared the estimates of R_rh obtained using the ¹³C approach with estimates obtained using the root-exclusion approach.

	Materials and methods

TOP ABSTRACT INTRODUCTION Materials and methods Results and discussion Conclusions REFERENCES

 
The experiment was conducted at the Central Experimental Farm, Ottawa, Ontario, Canada (45°22'N, 75°43'W, 79 m) from Day 148 to 303 in 1996. The soil, classified as a Brandon loam (fine loamy, mixed, mesic Typic Endoaquoll) had been under spring wheat (Triticum aestivum L.) in 1994 and 1995 following 3 yr under perennial forages. To our knowledge, the soil has never been planted to maize or other C4 crops. Glyphosate [N-(phosphonomethyl)glycine; 890 g a.i. ha^-1] was sprayed on Day 124 to control quackgrass [Elytrigia repens var. repens (L.) Desv. ex B.D. Jackson]. The soil was moldboard plowed (Day 134), disked (Days 137 and 138), and the fertilizer was applied according to soil tests (Day 137). Maize was planted at a rate of 6.5 plants m^-2 with 0.75-m interrows on Day 145 on a 40 by 60 m plot. Total aboveground dry biomass was measured on Day 230 on 15 randomly selected maize plants. An adjacent 20 by 60 m control plot was kept free of vegetation during the experiment by manual and mechanical weeding.

Total soil respiration was measured using a dynamic closed chamber system described by Rochette et al. (1997). It consisted of a cylindrical acrylic chamber (internal diameter 60 cm, height 20 cm, wall thickness 6.35 mm) connected to a portable CO₂ analyzer (LI-6200, Li-Cor, Lincoln, NE). At the time of measurement, the chamber was attached to cylindrical acrylic collars by clamps. The collars were 0.15 m high and were pushed 0.10 m into the soil. The rate of increase of CO₂ concentration was monitored for two successive periods of 30 s. The respiration rate was calculated for each period and both values were averaged for the final flux estimate. Twelve collars for soil respiration were installed on Day 138 in the control plot and twelve on Day 145 in the maize plot (between rows). On sampling days, R_t was measured on the twenty-four sites between 1000 and 1200 h. Measurements began on Day 148 and were repeated weekly until Day 303.

Soil air was sampled at 10-, 20-, and 40-cm depths at four locations on each plot 19 times during the season. The soil air probes consisted of tubing (Bev-A-Line IV, Labcor, Anjou, Québec, Canada) attached to plastic mesh cylinders containing glass beads (diameter 3 mm). Composite air samples were drawn simultaneously from four probes at each depth at each location. The probes were placed in the soil in pairs 40 cm apart. In the maize plot, one pair of probes was placed in the middle of the interrow while the other was located at 10 cm away from the row. Air sampling probes were installed at the same time as soil respiration collars. Air was removed from the tubes using evacuated 250-mL glass gas sampling flasks fitted with high vacuum stopcocks (Kontes, Vineland, NJ). Before collecting the soil air sample, 20 mL of air was removed from the tubes and discarded to account for the dead volume of the tubes. After collecting the soil air sample, the flasks were returned to a lab for cryogenic extraction of the CO₂ following the technique described by Rochette and Flanagan (1997).

Measurements of soil temperature using copper-constantan thermocouples and soil moisture using time-domain reflectometry probes (Topp et al., 1984) were performed at depths of 10, 20, and 40 cm at four locations in each plot on CO₂ sampling days. Thermocouples were read with digital thermometers (Model HH23, Omega, Stamford, CT and Model 600-2820, Barnant Co., Barrington, IL). Rainfall observations were taken at the Central Experimental Farm weather station (Ottawa, ON) located 400 m east of our experimental site.

Organic Material Collection and Preparation
On Day 185, nine maize plants were collected from the field. The plants were washed and subsamples of leaves and roots were taken from a range of positions on the plant. The subsamples were combined for an individual plant, and the material was dried at 65°C, and ground to a fine powder with a tissue grinder. Soil samples were collected from Ap horizon at 48 locations on Day 118. Roots from the previous vegetation were removed from the samples, and the soil was ground to a fine powder with a mortar and pestle and dried in an oven at 60°C for 24 h. The organic C content of the soil samples was determined by automated dry combustion-gas chromatography using a Carlo-Erba NA-1500 elemental analyzer (Carlo-Erba, Milan, Italy).

The organic tissue samples were prepared for measurements of C isotopic composition by combustion. A subsample of ground tissue (2–3 mg for leaf or root tissue, 20 mg for soil) was sealed in an evacuated quartz tube with cupric oxide wire and silver foil. The tubes were heated to 850°C for 6 h followed by an 8- to 9-h period of cooling to room temperature. The CO₂ generated from the combustion was purified cryogenically within 2 d.

Isotopic Analysis
The CO₂ from soil air samples and organic samples were analyzed on a gas isotope ratio mass spectrometer (Sira 12, VG Isotech, Middlewich, Cheshire, UK) at the Ottawa-Carleton Stable Isotope Facility. Isotopic compositions are expressed using delta notation:

(1)

The international standard for CO₂ samples is CO₂ from Pee Dee Belemnite (PDB) limestone (Ehleringer and Osmond, 1989). The values are presented in parts per thousand (). Isotope ratios in soil CO₂ samples were corrected for the presence of N₂O using the procedure described by Friedli and Siegenthaler (1988).

A mass balance approach was used to calculate the contribution of rhizosphere respiration to the total soil surface CO₂ flux (R_rh,frac). This approach is similar to that proposed by Rochette and Flanagan (1997):

(2)

where _sa,ma and _sa,ctl are the ¹³C values of the soil CO₂ in the maize and control plots, respectively, and _ma and _sc are the ¹³C values of the maize C and soil C, respectively.

	Results and discussion

TOP ABSTRACT INTRODUCTION Materials and methods Results and discussion Conclusions REFERENCES

 
Total Respiration
Total respiration in the maize plot was variable early in the season, increased during the summer months, and gradually decreased after Day 250 (Fig. 1a) . Both the magnitude and the spatial variability of R_t were typical of respiration measurements in soils under continuous cropping in Eastern Canada (Rochette et al., 1991; Gregorich et al., 1998). Values of R_t in the control plot fluctuated between 2.7 and 4.1 g CO₂–C m^-2 s^-1 during the first 100 d of the study, with the exception of a 1.5 g CO₂–C m^-2 s^-1 reading on Day 215. A total of 32 mm of rain fell on Day 214, and it is likely that the lower R_t on the following day was the result of poor gas diffusion through the wet surface soil (Rochette et al., 1991). Compared with R_t values in the maize plot, those in the control plot were similar before Day 180 but were consistently lower after that date.

View larger version (22K): [in this window] [in a new window]   Fig. 1 (a) Total soil respiration (Rt); (b) soil temperature, and (c) soil moisture at 20 cm in maize and control plots during the 1996 growing season. Vertical bars indicate ± SD

View larger version (15K): [in this window] [in a new window]   Fig. 2 Total soil respiration (Rt) response to soil temperature (Ts) at the 10-cm depth in maize and control plots during the 1996 growing season. Open squares indicate measurements made in the maize plot before Day 184 when plants were small; these data points were not used to calculate the Rt–Ts relationship in the maize plot

Carbon-13 of Soil Carbon Dioxide

Cerling et al. (1991) have shown that the ¹³C value of soil CO₂ should change in association with changes in the concentration of soil CO₂, which depends on the soil respiration rate, soil porosity, and invasion of atmospheric CO₂, among other parameters. In a soil with a high respiration rate (>2 g CO₂–C m^-2 d^-1), the C isotope ratio of soil CO₂ is expected to be enriched in ¹³C by 4.4 relative to both the source (metabolically produced CO₂) and the CO₂ that is released at the soil surface. This shift of 4.4 is caused by fractionation that occurs during diffusion of CO₂ out of the soil. However, the magnitude of the difference between the ¹³C value of soil CO₂ and metabolically produced CO₂ in the soil depends on soil respiration rate and other factors that affect the diffusion of CO₂ out of the soil (Cerling et al., 1991). In our experiment, the ¹³C value of soil CO₂ in the control plot was constant at approximately -24 during the first 100 d of the study (Fig. 3) . Assuming that the respired CO₂ had the same ¹³C as the soil organic C (-25.01), the ¹³C of the soil CO₂ would be expected to be approximately -21 under conditions where soil respiration rate was high. The reasons for this difference are not clear. Higher soil water content in the control than in the maize plot may have had an influence by decreasing gas diffusivity in the control plot compared with the maize plot. However, ¹³C values of soil CO₂ in the control plot were not correlated with soil water content at any depth (R 0.37). Also, equal ¹³C in both plots at the beginning of the study (Day <175) indicates that the factors responsible for this difference acted in both plots. This difference between predicted and observed ¹³C of CO₂ stresses the importance of measuring ¹³C of CO₂ simultaneously in cropped and control plots to account for the influence of any parameters specific to the conditions of the experiment that will affect soil CO₂ concentration.

View larger version (25K): [in this window] [in a new window]   Fig. 3 Seasonal variation in the C isotopic ratio (13C) of soil CO2 at three depths in maize and control plots during the 1996 growing season. Vertical bars indicate ± SD

Maize had no influence on the ¹³C of soil CO₂ during the first 40 d after planting (Fig. 3), as indicated by equal soil CO₂ ¹³C values measured on both plots. Therefore, the amount of respired CO₂ by plant roots and microbes in the rhizosphere was very small compared with the heterotrophic activity using native soil C substrate in the early stages of crop growth. This is in agreement with the observation of equal CO₂ fluxes in maize and control plots before Day 180 (Fig. 1a). Retarded germination of maize (from Day 153–167) due to the absence of rain between Day 141 and 156 may be partly responsible for the delay between planting and the enrichment of soil CO₂ in ¹³C. The ¹³C of soil CO₂ in the maize plot increased from Day 180 to 210, and peaked between Day 210 and 250. This pattern coincided with the seasonal variation of root density observed by Mengel and Barber (1974) for a maize crop under field conditions.

The contribution of rhizosphere respiration to total soil respiration has been calculated for each soil depth using Eq [2]. Estimates of R_rh from planting to Day 180 were zero. After that date, the R_rh contribution increased linearly to reach 45% of R_t on Day 210 (Fig. 4) , at which level it remained until Day 250 when it began to decrease until the end of the growing season. The values calculated for 40 cm before Day 210 were lower than those calculated at the two more shallow depths, probably reflecting the growing patterns of maize roots. Hanson et al. (1999) reviewed the published estimates of R_rh as a fraction of R_t and reported that estimates of R_rh for nonforest ecosystems ranged from 10 to >90% of R_t. Clearly, it is unlikely that a unique coefficient can be used to estimate R_rh from R_t in agricultural ecosystems because of (i) the growing patterns of the annual crops and (ii) conditions created by the soil and crop management in agricultural ecosystems in which the biological activity of the plants are not always directly proportional to R_t. For example, in continuous maize systems, it is likely that the relative contribution of the R_rh of a silage maize crop to R_t will be lower than that of a grain maize crop because of lower R_s resulting from differences in the amount of residues returned to the soil.

View larger version (16K): [in this window] [in a new window]   Fig. 4 Contribution of maize rhizosphere respiration (Rrh) to total respiration (Rt) in a maize crop during the 1996 growing season

View larger version (20K): [in this window] [in a new window]   Fig. 5 Total soil (Rt), rhizosphere (Rrh), and soil (Rs) respiration in a maize crop during the 1996 growing season. Estimates of Rrh were obtained by the 13C isotopic technique (Rrh,iso) and the root-exclusion technique (Rrh,excl). Vertical bars indicate ± SD

Both estimates of rhizosphere respiration show that the contribution of the plants to belowground CO₂ production is undetectable until approximately Day 180, or 35 d after planting. This date (Day 180) also coincides with the beginning of the exponential increase in aboveground phytomass accumulation and maximum net photosynthesis in maize in Ottawa (Rochette et al., 1996). At that stage, maize crops have usually accumulated <50 g dry matter m^-2. Any production of plant-derived CO₂–C prior to that stage appears to be within the variation of measurement in both R_t and ¹³C of soil CO₂.

The rate of oxidation of soil C (R_s) in the maize plot was calculated by the difference between R_t and R_rh obtained using the isotopic technique (Fig. 5). Values were highest early in the season and tended to decrease as the season progressed. Variations in R_s were closely related to T_s, with a Q₁₀ of 1.99 (Fig. 6) . In the absence of extreme soil water contents, a close relationship between R_s and T_s was expected. Therefore, this observation suggests that R_s and R_rh estimates are accurate or that the error is constant or proportional to T_s.

View larger version (10K): [in this window] [in a new window]   Fig. 6 Response of the rate of oxidation of soil C (Rs) to soil temperature (Ts) at the 10-cm depth in the maize plot during the 1996 growing season

The total seasonal CO₂–C losses as R_rh by the maize crop were calculated using the same approach as for R_s. Total cumulative R_rh was 1.58 Mg C ha^-1 or 17% of the crop net assimilation (A_n) calculated from total above-ground dry phytomass (7.87 Mg C ha^-1; SD = 1.22, n = 15 plants) and a root/shoot ratio of 0.2. There are few reports of R_rh/A_n for maize in the literature. Rochette and Flanagan (1997), using daily estimates of R_rh and A_n, calculated R_rh/A_n varying between 10 and 35% across an 80-d period under field conditions. Whipps (1985) measured R_rh/A_n by continuously labeling young maize plants with ¹⁴C in a growth cabinet. He obtained values of 4 and 10% at 14 and 28 d after emergence, respectively. Reports of R_rh/A_n obtained in growth cabinets are most abundant for spring wheat with values between 15 and 20% (Whipps and Lynch, 1983; Whipps, 1984; Merckx et al., 1985, 1986; Liljeroth et al., 1990). Our field estimates of R_rh were therefore within the range of values reported for annual crops.

	Conclusions

TOP ABSTRACT INTRODUCTION Materials and methods Results and discussion Conclusions REFERENCES

 
In situations where C4 plants are grown on a soil in which the organic C is derived from C3 plants, measurements of the natural abundance of ¹³C in the soil CO₂ has been proposed for separating total soil respiration into its plant and soil components. The maximum contribution of R_rh to total respiration was 45%, observed in August. Estimates of R_rh increased from zero 30 d after planting to 2.0 g CO₂–C m^-2 d^-1 70 d after planting, remained relatively constant at that level in August, and then decreased until the end of the growing season. Values of R_s gradually declined from 3.3 g m^-2 d^-1 in late June to 1.4 g m^-2 d^-1 at the end of the season. Our estimates of R_rh in a maize crop using the ¹³C approach has revealed some limitations of the technique. The ¹³C values of the soil CO₂ in the control plot were unstable after Day 250, probably as a result of variation in soil respiration rate and associated changes in the concentration of soil CO₂, which allow for greater input and greater influence of the enriched ¹³C composition of the aboveground atmospheric CO₂. Such variation makes the approach less reliable late in the season. There are no absolute references against which the accuracy of R_rh or R_s measurements can be evaluated. However, several observations indicated that the approach has potential to provide quantitative estimates of R_rh and R_s: (i) the coinciding of the seasonal pattern of the R_rh estimates with that of the plant growth and physiological activity, (ii) the good agreement between the cumulative R_rh and R_s over the growing season and published data obtained using ¹⁴C labeling techniques, (iii) the close relation of estimated R_s under maize and soil temperature with a Q₁₀ of 1.99, and (iv) the good agreement between estimates of R_rh obtained using the isotopic approach and those obtained using the root-exclusion technique.

	ACKNOWLEDGMENTS

 
This work was supported by the AAFC Green Plan Initiatives through grants to P. Rochette, by the PERD program through grants to E.G. Gregorich and P. Rochette, and by the Natural Sciences and Engineering Research Council of Canada through grants to L.B. Flanagan. We thank D.S. Kubien for help with sample collection and isotope analyses, and C. Lafontaine, R. Lessard, and R. Baillargeon for assistance in soil respiration measurements and plot maintenance.

Received for publication June 30, 1998.

	REFERENCES

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