Fluxes of CO₂, N₂O and CH₄ by ²²²Rn and chamber methods in cold-temperate grassland soil, northern Japan

Abstract

This study conducted flux measurements of carbon dioxide (CO₂), nitrous oxide (N₂O) and methane (CH₄), estimated by ²²²Rn (Radon) and chamber methods in a cold-temperate northern Japanese grassland soil during summer and winter seasons. Our research aims to compare these fluxes of CO₂, N₂O and CH₄ calculated by ²²²Rn and static chamber methods, and to understand the responses of fluxes by ²²²Rn and chamber methods to temperature. ²²²Rn fluxes ranged from 0.0046 to 0.0157 Bq m² s⁻¹, and the average was 0.0068 ± 0.0013 Bq m² s⁻¹ on sandy soil (> 50% sand). The average diffusion coefficients for CO₂, N₂O and CH₄ calculated using the ²²²Rn method were 0.049 ± 0.008 cm² s⁻¹, 0.023 ± 0.005 cm² s⁻¹ and 0.054 ± 0.008 cm² s⁻¹, respectively, reflecting seasonality. CO₂, N₂O and CH₄ flux measurements from the ²²²Rn method were in good agreement with those of the static chamber method, within the observed range of error, suggesting a high correlation coefficient of > 89% between the methods. Also, the temperatures of air and soil at 5-cm depth played a significant role in determining the fluxes of CO₂ and CH₄ measured by the ²²²Rn and chamber methods; meanwhile, the N₂O flux displayed an inverse exponential relation to temperature. This suggests that N₂O flux may be regulated by other factors such as soil water content and soil oxygen concentration. The contribution of winter fluxes of CO₂, N₂O and CH₄ corresponded to 9, 51 and 3% of the annual fluxes of CO₂, N₂O and CH₄, respectively, reflecting higher winter N₂O production due to the constraint of oxygen in soil.

Key words:

• fluxes of CO₂
• N₂O and CH₄
• ²²²Rn and chamber methods
• relaxation depth
• diffusion coefficient
• temperature
• northern Japan

1. INTRODUCTION

Carbon dioxide (CO₂), nitrous oxide (N₂O) and methane (CH₄) are important major trace gases as they absorb the Earth’s infrared radiation and contribute to global warming. CH₄ and N₂O have 23 and 296 times higher greenhouse warming potential than CO₂ (Houghton et al. 2001), respectively. Further, CH₄ is well known as a precursor of ozone destruction in the troposphere, and N₂O is an agent in decreasing the stratospheric ozone level (Houghton et al. 2001).

In a natural environment, an aerated (i.e., unsaturated) soil plays a significant role in the emission of CO₂ and N₂O, and in the oxidation of atmospheric CH₄. N₂O production by aerated soils is 20% of the total global N₂O source, and CH₄ oxidation by soils contributes about 5% to the global CH₄ sink (Houghton et al. 2001). CO₂ is produced in soil by microbial decomposition of soil organic matter and by root respiration (Raich and Schlesinger 1992). These gases are principally transported to the soil air by molecular diffusion in aerated soil. The fluxes of CO₂, N₂O and CH₄ at the soil surface and their concentrations in soil air depend on environmental factors such as temperature and soil moisture, as well as soil features including accumulated soil organic matter, soil microbial activity, soil type, soil pore space and so on (Dörr and Münnich 1987, 1990; Born et al. 1990; Nazaroff 1992; Dueñas et al. 1999; Kim and Tanaka 2002).

Gas transport in the soil was examined using the radioactive, inert, noble gas ²²²Rn (Radon, half-life: 3.82 d), which is produced by α-decay of ²²⁶Ra (Radium, half-life: 1602 y), and which has been used as a tracer of unsaturated soil in the method adopted by Born et al. (1990), Dörr and Münnich (1987, 1990), Trumbore et al. (1990), Davidson and Trumbore (1995), Dueñas et al. (1999), and Kim and Tanaka (2002). The ²²²Rn method requires significant additional labor compared to the static chamber method, because of the need to measure both depth profiles of ²²²Rn and other trace gases in the soil, and ²²²Rn flux at the soil surface. However, the ²²²Rn method does give significant information about trace gas diffusion in the soil throughout the year. Only a small fraction of ²²²Rn is produced by recoil from soil particles into the air, depending on the specific surface area of soil particles—and thus depending also on grain size distribution (Trumbore et al. 1990; Davidson and Trumbore 1995; Dueñas et al. 1999; Kim and Tanaka 2002). ²²²Rn flux at the soil surface is affected by ²²⁶Ra contents, as well as soil physical properties such as grain size distribution and resistance to molecular diffusion in the unsaturated soil zone. ²²²Rn flux at the soil surface and ²²²Rn concentration in soil air are also influenced by soil characteristics such as moisture content, tortuosity and porosity, which can be determined by measuring the ²²²Rn flux and concentration gradient at the same site. Further, the spatial variation of the ²²²Rn flux has been found to depend more on soil type than on the ²²⁶Ra activity of the soil material (Dörr and Münnich 1987, 1990; Dueñas et al. 1999). Further, the ²²²Rn method provides a proxy for temporal changes in diffusivity within the soil. This enables us to estimate rates of emission of CO₂ and N₂O, oxidation of CH₄ through the soil to the atmosphere, production of CO₂ and N₂O within the soil using a one-dimensional vertical diffusion box model under a non-steady state condition, and mixing of ²²²Rn without any disturbance and contamination. Kim and Tanaka (2002) previously reported the emission and production rates of N₂O through snowpack to the atmosphere using this ²²²Rn method. To this point, previous reports have used the ²²²Rn method to estimate soil fluxes of CO₂ and CH₄. In response, we used ²²²Rn and static chamber methods to estimate fluxes of CO₂, N₂O and CH₄ in a cold-temperate aerated grassland soil, located in northern Japan. The purposes of this study are (1) to compare the fluxes of CO₂, N₂O and CH₄ calculated by ²²²Rn and static chamber methods, and (2) to understand ²²²Rn- and chamber-measured flux responses to temperature in our cold-temperate grassland soil of northern Japan, during summer and winter seasons.

2. THEORETICAL CONSIDERATIONS

The ²²²Rn method used to calculate fluxes of CO₂, N₂O and CH₄ was based on a one-dimensional vertical model, as shown below. The diffusion transport of four gases (²²²Rn, CO₂, CH₄ and N₂O) in the unsaturated soil zone are described by Fick’s first law:

(1)

where J represents flux, C is concentration and D is the diffusion coefficient of the gas under consideration. The D in aerated soil zone can also be expressed as follows:

(2)

where D₀ is the molecular diffusion coefficient in air, ε₀-H is the porosity of the air-filled portion of the soil—which can be expressed as the difference between the total porosity, ε₀, and the volumetric soil moisture content, H—and k is tortuosity. This tortuosity describes the higher diffusion resistance in soil than in air, owing to variations in the soil diffusion cross-section, and from soil grains and water-filled capillary regions (Dörr and Münnich 1990).

Assuming horizontal homogeneity (i.e., advective transport = 0), our changes in soil air ²²²Rn concentrations with depth (z, taken as positive in the downward direction) and time (t) are described by the diffusion equation:

(3)

where C_Rn is ²²²Rn concentration, D_Rn is the ²²²Rn diffusion coefficient in aerated soil, Q_Rn is the production rate normalized to a unit soil volume and λ is the ²²²Rn decay constant (2.1 × 10⁻⁶ s⁻¹). Diffusion equations for CO₂ and N₂O (hereinafter CO₂, N₂O in equations) and CH₄, which are non-radioactive gases, are also obtained from Eq. 3 by setting λ = 0 and in soil:

(4)

(5)

where and are the concentrations of CO₂, N₂O and CH₄ and and are the diffusion coefficients of CO₂, N₂O and CH₄ in the aerated soil. denotes the production rates of CO₂ and N₂O in the soil.

Assuming a steady-state condition, a vertically homogeneous Q_Rn and a depth-independent diffusion coefficient (D_Rn), the ²²²Rn concentration profile is obtained by solving Eq. 3 with boundary condition C_Rn (z = 0) = 0, since the atmospheric ²²²Rn concentration is essentially equal to zero, and :

(6)

where Z = (D_Rn/λ)^1/2 is the relaxation depth and is the concentration at depth z ≫ Z. In this study, relaxation depth (Z) was calculated as from 107 to 206 cm in this study site, reflecting the seasonality of relaxation depth. Thus, Eq. 6 was adapted to our sampling scheme and rewritten as a linear function for a particular depth (shallower than 100 cm) as:

(7)

From Eq. 1, the relationship between ²²²Rn flux, J_Rn and the ²²²Rn concentration gradient , can be expressed as:

(8)

The ²²²Rn diffusion coefficient, D_Rn, can then be rewritten as:

(9)

Simultaneous measurements of ²²²Rn flux at the soil surface and the ²²²Rn concentration profile in soil air give the ²²²Rn diffusion coefficient, from Eq. 9.

The ratio of molecular diffusion coefficients is constant at a given temperature of 15°C (Dörr and Münnich 1987, 1990). The diffusion coefficient of CO₂, N₂O and CH₄, and , can thus be calculated as

(10)

(11)

The diffusion coefficient of CO₂, N₂O, and CH₄ ( and ) can be expressed as a product of the calculated ²²²Rn diffusion coefficient, D_Rn, from the measurement. Further, concentration gradients of CO₂, N₂O and CH₄ at the soil surface were calculated from the observed profiles of CO₂, N₂O and CH₄. The fluxes of CO₂, N₂O and CH₄ at the soil surface are then obtained using Eq. 1 and the diffusion coefficients of CO₂, N₂O and CH₄ ( and ):

(12)

(13)

Thus, using Eq. 9 and 10 for CO₂ and N₂O fluxes, and using Eq. 9 and 11 for CH₄ flux, Eq. 12 and 13 can also expressed as:

(14)

(15)

Fluxes of CO₂, N₂O and CH₄ at the soil surface are calculated from Eq. 14 and 15, using measured CO₂, N₂O, CH₄ and ²²²Rn concentration profiles and the directly measured ²²²Rn fluxes.

All equations are derived under the assumption that gas transport in the soil water phase can be neglected. This assumption is true for the most relevant gases (and especially for ²²²Rn, CO₂, N₂O and CH₄), as the molecular diffusion coefficient of gases is 10⁴ times smaller in water than in air, and solubility is on the order of 1 or even less (Nazaroff 1992), though we could not clearly measure soil moisture using this study.

3. MATERIALS AND METHODS

3.1 Research sites

The study site was located at the Institute of Low Temperature Science (H-1: 43°04’N, 141°20’E, 65 m above sea level) of the main campus of Hokkaido University, Sapporo, on the northern island of Japan. The site was typified by the brown forest and lowland soils of the characteristic Brown Lowland Soils (Fluvisol; Cultivated Soil Classification Committee 1995; IUSS Working Group WRB 2007), and by a cold-temperate climate. The average summer (July to August) and winter (January to February) temperatures in Sapporo for last 40 years are 21.2 ± 1.5°C and –3.8 ± 2.1°C, respectively. The average annual precipitation and the maximum snow depth for 40 years are 94 ± 30 cm and 98 ± 20 cm, respectively (Sapporo District Meteorological Observatory). The site H-1 is covered dominantly with orchard grass (Dactylis glomerata), and the soil shows an average bulk density of 0.69 ± 0.12 Mg m⁻³; 37% silt, 11% clay and 52% sand; and with 21.2 kg cm⁻² and 2.05 kg cm⁻² carbon and nitrogen organic matter by weight, respectively (Sapporo Regional Forest Office 1970). The study site had only been mowed—not fertilized, seeded or plowed—as part of site management. Grasslands porosity measurement varied from 0.152 to 0.274, according to the method of Osozawa and Kubota (1987). A portable thermometer (Digital Thermometer, Iuchi Ltd., Japan) was used to measure temperatures in the air and the soil at 5 cm below the surface. The sampling interval was approximately 10 d, depending on the weather conditions, and was assumed to reach a steady-state condition for the ²²²Rn method. During the winter season of 1996–97, snow depths for Dec 24, 1996, and Jan 26, 1997, were 16 and 20 cm, respectively. Soil temperatures for these two observation days, during which the soil was still frozen, were –2.0 and –0.8°C, respectively.

3.2 Sampling by chamber and soil profile

²²²Rn fluxes from soil at site H-1 were measured simultaneously by monitoring of ²²²Rn in a static chamber placed over the soil. The flux chamber base was located within a few meters of in-soil probes, and had a stainless steel collar with a top diameter of 50 cm, a cross section area of 0.2 m² and a height of 10 cm. This chamber was placed over the soil surface at the beginning of each measurement series, so as not to disrupt the soil surface. Air samples were drawn four to five times from the headspace in the chamber at 10–20 min intervals after deployment. The collected air sample was 10–20 mL, relatively small compared to the chamber volume.

Flux was calculated from the gradient of the relationship between concentration variations of ²²²Rn and the sampling period. The correlation coefficient (R²) was over 0.99, and the curve was linear (Livingston and Hutchinson 1995). These samples were introduced directly into the Lucas cell after radioactive equilibrium of ²²⁰Rn (Thoron: half-life 55 s) and the removal of water. Flux measurements and soil air sampling were carried out on clear afternoons.

²²²Rn flux from the soil surface can be calculated from the rate of concentration increase in the chamber:

(16)

where J is the flux, V is the volume of air in the chamber, A is the cross-section area covered by the chamber, C represents the chamber concentrations of CO₂, N₂O and CH₄ and ∂C/∂t is the rate of concentration change in the chamber air. This static chamber method was also used to estimate CO₂, N₂O and CH₄ fluxes from the soil under a smaller chamber (22 cm inner diameter, 8 cm height), deployed in a manner similar to that used for the radon chamber. Air in the chamber was sampled every five minutes with a 20-mL plastic syringe, and collected in an aluminum foil bag.

Soil air samples for CO₂, N₂O, CH₄ and ²²²Rn measurements were taken through a specially made concentric probe, preset at the selected depths a half month prior to the start of the series of air collections. The body of each probe consists of a modified stainless steel tube (0.2 cm inner diameter, 0.6 cm outer diameter, 100 cm length; GL Science, Inc., Japan). Probes were inserted vertically into the soil, and the horizontal distance between probes was approximately 10 cm. Sampling depths were at 5, 10, 20, 30, 40, 50, 70 and 100 cm during the summer season, and at 5, 10, 15, 20, 30 and 40 cm during winter—relatively shallower than summer, due to the frozen soil surface at site H-1. Probes were connected to polypropylene tubing, sealed with a rubber septum at the distal end. Ten milliliters of soil gas were collected with a plastic syringe from each probe and transferred to an aluminum foil bag (GL Science, Inc, Japan) for the analyses of CO₂, N₂O, CH₄ and ²²²Rn.

3.3 Analyses of CO₂, N₂O, CH₄ and ²²²Rn

These gas-filled bags were transported to the laboratory for analyses of CO₂, N₂O and CH₄. CO₂ concentrations were measured using a gas chromatograph equipped with a thermal conductivity detector (TCD-GC, GC-14B, Shimadzu Ltd., Japan), with a column packed with Porapack Q (80/100 mesh). Calibration was done with a series of standard gases containing 338 ± 7, 491 ± 10 and 5000 ± 100 ppmv CO₂ in synthetic air (Nihon Sanso CO. Ltd., Japan). Calibration range precision was usually better than 1%. Soil air CO₂ was analyzed within 10 h after sample collection, necessary due to the problem of sample preservation (data not shown), which was itself due to the higher CO₂ transmissivity of the aluminum-made sampling bag. Concentrations of N₂O were measured with a gas chromatograph equipped with an electron capture detector (ECD-GC, GC-14B, Shimadzu Ltd., Japan), with a column packed with Porasil Q (80/100 mesh). Calibration was conducted using a series of standard gases containing 302 ± 6, 784 ± 8 and 1308 ± 15 ppbv N₂O in synthetic air (Nihon Sanso CO. Ltd., Japan). Calibration range precision was usually better than 2%. CH₄ concentrations were measured with a gas chromatograph equipped with a flame ionization detector (FID-GC, GC-14B, Shimadzu Ltd., Japan), with a column packed with Molecular Sieve 13X (80/100 mesh). Calibration was conducted using a series of standard gases containing 0.79 ± 0.016, 1.61 ± 0.020 and 2.43 ± 0.048 ppmv CH₄ in synthetic air (Nihon Sanso CO. Ltd., Japan). Calibration range precision was usually better than 3%.

Five milliliters of soil air for ²²²Rn measurements were collected from the soil probe in the same manner as for CO₂, N₂O and CH₄ samples. This sampled air was immediately introduced into an evacuated phosphor-coated [ZnS(Ag)] Lucas cell (RDX-386, EDA Instruments Inc., Toronto, ON, Canada). Lucas cell air volume was 110 mL. ²²²Rn activity was measured using an alpha-ray scintillation counter (Model-2200 Scaler Ratemeter and Model-182 Radon Flask Counter, Ludlum Co., Ltd., Canada). ²²²Rn activities in the cell were counted after 3.5 h to attain radioactive equilibria with the short-lived daughter nuclides, including ²¹⁸Po (Polonium, half-life: 3.05 m), ²¹⁴Pb (Lead, half-life: 26.8 m), ²¹⁴Bi (Bismuth, half-life: 19.7 m) ²¹⁰Bi, and ²¹⁴Po (half-life: 164 µs). The background value was counted for the evacuated cell after several repeated measurements of each gas sample. The background of each Lucas cell used ranged from 0.13 to 0.47 counts per minute (cpm). ²²²Rn activity was corrected for the background count of each cell and calibrated against a standard solution of ²²⁶Ra, of 12.9 Bq m⁻³. Uncertainty for the ²²²Rn measurements was about 7%, after we made ²²²Rn standard from a ²²⁶Ra standard solution in 20-L glass bottle and measured ²²²Rn activity a month later.

4. RESULTS

4.1 Concentration profiles of ²²²Rn, CO₂, N₂O and CH₄

The concentration profiles of ²²²Rn, CO₂ and N₂O measured in aerated grassland soils increased exponentially with depth (Fig. 1a–c). Concentration gradients of ²²²Rn, CO₂ and N₂O in the aerated grassland soil were 10.8 ± 2.5 Bq m⁻³ cm⁻¹, 520 ± 140 ppm cm⁻¹ and 7.8 ± 1.7 ppb cm⁻¹ through the observed soil column during the summer season, and 58 ± 25 Bq m⁻³ cm⁻¹, 1160 ± 870 ppm cm⁻¹ and 155 ± 26 ppb cm⁻¹, respectively, during the winter. CH₄ profile decreased with depth (Fig. 1d), and the gradient was –0.021 ± 0.001 ppm cm⁻¹ during the summer season and –0.040 ± 0.020 ppm cm⁻¹ during the winter.

The profiles of these gases changed temporally throughout the year; production of ²²²Rn, CO₂, and N₂O, and CH₄ oxidation, may be attributed to changes in effective pore space, depending on soil moisture, oxygen content and magnitude of soil microbial activity controlled by soil temperature. Generally, the profiles of ²²²Rn, CO₂, N₂O and CH₄ during the winter season were much more different than during the summer.

4.2 Flux measurements by the chamber method

Fluxes of CO₂, CH₄ and N₂O were also calculated using Eq. 16, and average CO₂, CH₄ and N₂O fluxes were 38 ± 6.1 mg carbon (C) m² h⁻¹ (coefficient of variation, CV: 15%), 6.1 ± 0.8 µg nitrogen (N) m² h⁻¹ (12%) and –6.9 ± 1.1 µg C m² h⁻¹ (16%) during summer, and 4.4 ± 3.1 mg C m² h⁻¹ (72%), 8.5 ± 3.0 µg N m² h⁻¹ (35%) and –0.2 ± 0.2 µgC m² h⁻¹ (73%) respectively, during winter at site H-1. CO₂ and CH₄ fluxes during summer were 9- and 35-fold higher, respectively, than in winter. On the other hand, N₂O flux during summer was slightly lower than during winter, which suggests that denitrification may have occurred due to constraint of soil oxygen by the frozen soil surface (Kim and Tanaka 2002), as shown in Fig. 1c.

Figure 1 Concentration profiles of (a) ²²²Rn, (b) CO₂, (c) N₂O and (d) CH₄, observed within northern Japanese grassland aerated soil during the summer and winter seasons. ²²²Rn, CO₂, N₂O, and CH₄ profiles were fitted with exponential curves using the ²²²Rn method (R² > 0.85). Each symbol denotes a sampling date of 1996/97.

4.3 ²²²Rn flux from the soil surface

The ²²²Rn flux from the chamber method ranged from 0.0041 to 0.0157 Bq m² s⁻¹, with an average of 0.0068 ± 0.0013 Bq m² s⁻¹ on sandy soil (> 50% sand; CV 20%) over summer and winter seasons. According to Dörr and Münnich (1990), in the temperate soils of western Germany, the wide variety of observed fluxes is caused by variations in ²²²Rn emanation rate, depending on the surface to volume ratio, as well as on the grain-size diameter of soil particles in different soil types, such as sand, loam, clay and silt. Thus, it is difficult to quantify the influence of soil moisture on tortuosity and emanation rate in this study.

The ²²²Rn fluxes measured in this study ranged between the lower ²²²Rn fluxes (0.0046–0.0093 Bq m² s⁻¹) of sandy soils (> 65% sand) and the higher ²²²Rn fluxes (0.0185–0.0278 Bq m² s⁻¹) of loamy and clay-like soils (> 35% clay) found in West Germany (Dörr and Münnich 1990). The value of the diffusion coefficient (D_Rn) ranged from 0.024 cm² s⁻¹ on September 26 to 0.093 cm² s⁻¹ on August 29, with an average of 0.050 ± 0.010 cm² s⁻¹ (CV: 21%). The average diffusion coefficient of ²²²Rn was similar to that estimated by Osozawa and Kubota (1987) for the relative gas diffusion coefficient (0.048 ± 0.020 cm² s⁻¹), measured from soil horizons at the same site.

4.4 Fluxes of CO₂, N₂O and CH₄ by the ²²²Rn method

Fluxes of CO₂, N₂O and CH₄ were calculated using the ²²²Rn method and Eq. 14 and 15. Average diffusion coefficients of , and were 0.049 ± 0.008 cm² s⁻¹ (CV 16%), 0.023 ± 0.005 cm² s⁻¹ (CV 20%) and 0.054 ± 0.008 cm² s⁻¹ (CV 15%) respectively, in aerated sandy soil, as shown in Table 1. values ranged between 0.0013 cm² s⁻¹ in clay-like soil and 0.068 cm² s⁻¹ in sandy soil (> 68%), and values varied from 0.0017 cm² s⁻¹ in clay-like soil and 0.069 cm² s⁻¹ in sandy soil (Dörr and Münnich 1990; Trumbore et al. 1990; Dueñas et al. 1999). However, there are few reports for the measurements of from the ²²²Rn method, which yielded 0.002–0.046 cm² s⁻¹. The average relaxation depth of ²²²Rn was 152 ± 17 cm (CV: 11%) in sandy soil, which is similar to the value measured by Dorr and Munnich (1990). The relaxation depths of CO₂, N₂O and CH₄ are shown in Table 1, representing estimations of CO₂, N₂O and CH₄ fluxes from the ²²²Rn method. The average relaxation depths of CO₂, N₂O and CH₄ were 127 ± 14 cm (CV 9%), 211 ± 78 cm (CV 37%) and 152 ± 17 cm (CV 11%) respectively, at site H-1. CO₂ and CH₄ profiles showed similar relaxation depths, indicating similar depth distributions of the CO₂ source and CH₄ sink (Dörr and Münnich 1990; Dueñas et al. 1999). Contrary to the profiles of CO₂ and CH₄, the N₂O profile is relatively shallower than the depths of CO₂ and CH₄, suggesting the depth of the N₂O source may be shallower than that of CO₂ in aerated sandy soil.

Table 1 Calculated diffusion coefficients, relaxation depths, and fluxes of CO₂, N₂O and CH₄ by the ²²²Rn method in grassland aerated soil, northern Japan, during the summer and winter of 1996 and the winter of 1997

Date	Diffusion coefficients			Relaxation depth			Fluxes
in 1996/97	cm^2s^−1			cm			mBqm^2s^−1	mgCm^2h^−1	µgNm^2h^−1	µgCm^2h^−1
(mm-dd)	CO2	N2O	CH4	CO2	N2O	CH4	^222Rn	CO2	N2O	−CH4*
06-22	0.043	0.016	0.047	143	87	149	4.3	43.3	7.6	10.6
07-05	0.078	0.032	0.062	193	123	172	5.7	16.9	4.5	2.0
07-12	0.055	0.022	0.067	162	102	178	7.3	36.2	3.9	8.4
07-21	0.078	0.046	0.083	193	148	199	10.5	46.1	4.4	6.6
08-29	0.086	0.041	0.073	202	140	186	15.7	73.5	2.7	3.0
08-31	0.046	0.026	0.066	148	111	177	5.9	49.6	2.5	4.6
09-20	0.043	NM	0.075	143	NM	189	4.5	40.1	NM	17.6
09-26	0.035	0.019	0.045	129	95	146	4.1	19.8	7.6	6.8
Mean	0.058	0.029	0.065	164	115	175	7.3	40.7	4.8	7.5
12-24	0.021	0.007	0.002	100	240	31	4.1	11.4	7.3	0.35
01-26	0.008	0.002	0.017	62	856	90	5.9	0.8	9.1	0.04
Mean	0.015	0.005	0.010	81	548	61	5.0	6.1	8.2	0.20

NM indicates not measured.

*–CH4 flux denotes the CH₄ uptake to the soil from the atmosphere.

4.5 CO₂, N₂O and CH₄ fluxes by the two methods

CO₂, N₂O and CH₄ fluxes determined by the ²²²Rn method were compared with those estimated by the chamber method over grassland soils, and the ratios showing these comparisons are listed in Table 2. The ratios of CO₂, N₂O and CH₄ fluxes during the summer season were somewhat higher than during the winter season. Ratios ranged from 0.84 to 1.64 for CO₂, 0.70 to 1.20 for N₂O and 0.57 to 1.44 for CH₄ flux, respectively. CO₂, N₂O and CH₄ fluxes calculated using both methods fluctuated temporally in the aerated grassland soil throughout the seasons. The magnitudes of temporal variation in CO₂, N₂O and CH₄ fluxes were 20, 14 and 28% for the ²²²Rn method, and 21, 12 and 22% for the chamber method, respectively. The factor of temporal variation is used to quantify temporal variability in each flux throughout the year. Seasonal variations in CO₂, N₂O and CH₄ from the two methods are related to fluctuations in environmental factors such as soil temperature, soil organic carbon, soil moisture, grain size and so on. Interestingly, there was no distinct difference in the ratio between summer and early winter, except for the data obtained for January 26, 1997. This may be due to the frozen ground during the winter season. Additional study will be required to estimate these fluxes, including for the winter season, for better understanding of these gases’ transport mechanism(s).

Table 2 The flux ratio of the ²²²Rn method to the chamber method in sandy soil, northern Japan

Date	Flux ratio (FRn/Fchamber)
in 1996 (mm-dd)	CO2	N2O	CH4
06-22	1.27	1.00	1.20
07-05	0.97	0.87	0.57
07-12	1.64	0.90	1.19
07-21	0.84	0.80	0.85
08-29	1.13	1.20	1.18
08-31	1.21	0.70	0.89
09-20	0.88	NM	1.44
09-26	0.95	1.10	0.86
average ± SD*	1.11 ± 0.26	0.92 ± 0.16	1.02 ± 0.28
12-24	1.53	1.00	0.91
01-26**	0.67	0.80	0.59
average ± SD*	1.09 ± 0.60	0.89 ± 0.12	0.78 ± 0.16
Total	1.10 ± 0.31	0.91 ± 0.15	0.98 ± 0.27

NM indicates not measured.

*SD denotes standard deviation.

**The date is January 26, 1997.

5. DISCUSSION

5.1 Comparison of CO₂, N₂O and CH₄ fluxes by the two methods

CO₂ flux estimated by the ²²²Rn method was slightly higher than that from the chamber method, suggesting that it may be due to some amount of soil moisture occurring during observation (Dörr and Münnich 1990; Dueñas et al. 1999). Unfortunately, the profile of soil moisture was not observed through this study, owing to the disturbance. Dorr and Munnich (1990) and Dueñas et al. (1999) also reported that CO₂ and CH₄ flux values measured by the ²²²Rn method tended to be higher than those measured by the chamber method, as observed in this study. On the other hand, N₂O flux measured here by the chamber method is slightly higher than from the ²²²Rn method, which is due possibly to different soil types and environmental factors. A regression analysis in this study revealed that the differences between the two methods were not significant (p < 0.001). The validities of both flux measurement methods for CO₂, N₂O and CH₄ were effectively confirmed. Specifically, CO₂, N₂O and CH₄ fluxes estimated by the ²²²Rn method elucidated 89, 91 and 90% of the variability in CO₂, N₂O and CH₄ flux measurements, respectively, from the chamber method within the aerated soil of site H-1. As a result, we found the ²²²Rn method analogous to the static chamber method for flux estimation of these greenhouse gases in this grassland of northern Japan.

Flux measurements of CO₂, N₂O and CH₄, meanwhile, could be not represented due to the heterogeneity of the point-to-point site within grassland soils (Sommerfeld et al. 1996). To accurately estimate CO₂, N₂O and CH₄ fluxes in heterogeneous systems, multiple CO₂, N₂O and CH₄ flux measurements are needed to cover the target study site more widely. During winter, N₂O fluxes estimated using both methods were much higher than those estimated during summer, suggesting that winter N₂O flux may be attributed to the denitrification process from a deficiency of soil oxygen (Williams et al. 1992; Kim and Tanaka 2002), as well as an increase in soil moisture (Williams et al. 1992).

Concentrations of CO₂, N₂O and CH₄ in the chamber varied linearly with time (R² ≧ 0.99), suggesting that the results of these chamber measurements are indeed reliable (Livingston and Hutchinson 1995). Small concentration changes with a short sampling interval would not lead to large errors in flux determination. The static chamber method is well suited to easily estimate trace gas fluxes over a short period; however, this method can sufficiently explain neither the process of soil-originated CO₂ and N₂O production (Kim and Tanaka 2002), nor the depth-dependence distribution of the source-strength of CO₂ and N₂O within the soil.

5.2 Environmental factors regulating CO₂, N₂O and CH₄ fluxes

Temperature and soil moisture are well-known environmental factors affecting CO₂, N₂O and CH₄ fluxes in different soils. The relationships between temperature in air and soil at 5 cm depth and CO₂, N₂O and CH₄ fluxes from the ²²²Rn and chamber methods are shown exponentially in Fig. 2. The correlation coefficients (R²) between air temperature and CO₂ and CH₄ fluxes by ²²²Rn and chamber methods were 0.73 and 0.77 for CO₂ flux and 0.71 and 0.76 for CH₄ flux, respectively, suggesting that air temperature accounts for > 70% of the variability in both CO₂ and CH₄ fluxes. Coefficients for soil temperature were 0.64 and 0.69 for CO₂ flux, and 0.64 and 0.68 for CH₄ flux, estimated by the ²²²Rn and chamber methods. On the other hand, N₂O flux had an inversely exponential relationship to both air temperature (R²: 0.52 and 0.49) and soil temperature (R²: 0.54 and 0.50), as shown in Fig. 2b and 2e. This indicates that N₂O flux magnitude is dependent on both soil moisture content (Williams et al. 1992) and soil oxygen concentration (Goreau et al. 1980; Williams et al. 1992; Kim and Tanaka 2002). As we measured neither soil moisture content nor oxygen concentration in the soil, it was difficult to figure the environmental factors affecting N₂O flux in this study. However, Keeney et al. (1979) and Zhou et al. (2005) reported that N₂O flux occurs in an inverse relationship with temperature, and Schimel et al. (1993) described temperature as a strong controller of microbially mediated production and consumption of trace gases. Other factors, such as substrate and moisture availability, could also often be limiting, to the extent that the temperature effect was not expressed. As a result, our findings suggest an inversely exponential relationship between N₂O flux and temperature in this study.

Figure 2 Responses from fluxes measured by the ²²²Rn and chamber methods to air temperature (a, b, and c) and soil temperature at 5-cm depth (d, e and f) in aerated grassland soil. Negative CH₄ denotes the oxidation of atmospheric CH₄ to the soil. Solid and dotted lines denote exponential curves for ²²²Rn and chamber methods, respectively. Air and soil temperatures were significant, key factors in determining CO₂ and CH₄ fluxes, measured by ²²²Rn and the chamber method; however, N₂O flux did not depend on temperature.

The Q₁₀ value represents a temperature sensitivity of CO₂, N₂O and CH₄ fluxes, and is defined as the ratio of reaction rate at an interval of 10°C, Q₁₀ = exp (10 × β), where β is constant. The Q₁₀ for air temperature was 2.98 and 2.79 for CO₂, 0.73 and 0.74 for N₂O and 4.58 and 4.21 for CH₄, according to the ²²²Rn and chamber methods, respectively. Correspondingly, Q₁₀ for soil temperature was 3.14 and 2.99 for CO₂, 0.54 and 0.50 for N₂O and 5.09 and 4.66 for CH₄ for the ²²²Rn and chamber methods, respectively. Remarkably, Q₁₀ for CH₄ flux on soil temperature was much higher than for air temperature. Whalen and Reeburgh (1990) suggested that CH₄ oxidation rates can be measured by adding ¹⁴CH₄ to a sample in a sealed incubation jar, supporting a decrease in ¹⁴CH₄ and the increase in ¹⁴CO₂. Our findings demonstrate that soil temperature has greater effect than air temperature in regulating the fluxes of CO₂ and CH₄, as well as also affecting the magnitude of soil microbial activity that controls the flux strengths of CO₂ and CH₄ in aerated grassland soils (Nazaroff 1992). Although the ²²²Rn and chamber methods were effective for the flux measuements of greenhouse gases, additional study is needed to better understand the production mechanism of CO₂, N₂O and CH₄ oxidation in soil by using stable isotopes.

Seasonal fluxes of CO₂, N₂O and CH₄ were 200 ± 22 and 19 ± 9.2 g C m² season⁻¹, 28 ± 2.8 and 30 ± 4.6 mg N m² season⁻¹ and –37 ± 5.2 and −0.8 ± 0.3 mg C m² season⁻¹, respectively, during the 215-d summer and 150-d winter in the aerated grassland soil of Northern Japan. The winter fluxes of CO₂, N₂O and CH₄ represent 9, 51 and 3% of the annual fluxes, reflecting higher winter N₂O production due to the constraint of soil oxygen (Kim and Tanaka 2002).

6. CONCLUSION AND FUTURE WORK

Flux measurements of CO₂, N₂O and CH₄ estimated by the ²²²Rn and chamber methods were compared in cold-temperate grassland soil of northern Japan. From the results of the ²²²Rn method, average diffusion coefficients and relaxation depths of CO₂ and CH₄ were similar to previous values in aerated sandy soils (Dörr and Münnich 1990; Trumbore, 1990; Dueñas et al. 1999; Kim and Tanaka 2002). There are yet few reports for a diffusion coefficient and relaxation depth of N₂O and, as a result, we first report here on these factors for our aerated grassland soil site. There is no significant difference between the CO₂, N₂O and CH₄ fluxes measured by the ²²²Rn method and those by the chamber method, with a 95% confidence level. Soil temperature was a much more important factor than air temperature in determining fluxes of CO₂ and CH₄, and to a greater extent N₂O flux, in aerated grassland soils.

The winter contributions from CO₂, N₂O and CH₄ fluxes corresponds to 9%, 51 and 3% of total annual fluxes for CO₂, N₂O and CH₄. Although there are few reports for winter N₂O emission and observation frequency through the year of this study, emission should not be overlooked in estimations of regional nitrogen budget, due to higher winter N₂O contribution to the atmosphere (Kim and Tanaka 2002).

ACKNOWLEDGMENTS

We appreciate our colleagues in the Laboratory of Marine and Atmospheric Geochemistry (MAG), Hokkaido University, for their cooperation throughout this study. We thank Dr. H. Narita at Tokai University for ²²²Rn analysis, and Nate Bauer (IARC), University of Alaska Fairbanks, for constructive editorial revisions of the manuscript.