Soil Science Society of America Journal 64:2180-2186 (2000)
© 2000 Soil Science Society of America
DIVISION S-10-WETLAND SOILS
Methane and Nitrous Oxide Emissions from a Rice Field in Relation to Soil Redox and Microbiological Processes
A.X. Houa,
G.X. Chena,
Z.P. Wangb,
O. Van Cleemputc and
W.H. Patrick, Jr.b
a Laboratory of Ecological Process of Trace Substances in Terrestrial Ecosystem, Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang 110015, People's Republic of China
b Jr., Wetland Biogeochemistry Institute, Louisiana State Univ., Baton Rouge, LA 70803, USA
c Faculty of Agriculture and Applied Biological Sciences, Univ. of Ghent, Coupure 653, Ghent B-9000, Belgium
bpatrick{at}premier.net
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ABSTRACT
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Paddy rice fields provide an environment for production of two important greenhouse gases, CH4 and N2O, because of variations in soil characteristics, moisture content, and microbial activity during the cropping season. Emissions of CH4 and N2O from a paddy rice field in northern China were measured in situ by static chamber technique during March to December in 1995 and 1996. Factors affecting gas emission, including soil temperature, pH, and redox potential (Eh), were measured as well. Emissions of CH4 and N2O were strongly correlated with changes in soil redox potential. Significant CH4 emission occurred only at soil redox potential lower than approximately -100 mV, while the emission of N2O was not significant below +200 mV. A significant inverse relationship between CH4 and N2O emissions was observed (r = -0.49, n = 16, 5% confidence level). The results suggest the possibility of using management practices to maintain the redox potential in a range where both N2O and CH4 emissions are low. The activities of six related bacteria groups (zymogenic bacteria, acetic acid and hydrogen-producers, methanogens, CH4 oxidizers, and nitrifiers and denitrifiers) in the soil were also measured in an effort to explain the relationship between gas emission and soil microbiological processes. Methane emission was significantly related to the logarithm number of zymogenic bacteria (r = 0.76, n = 12, 1% confidence level), as well as to soil redox potential (r = -0.72, n = 12, 1% confidence level). Both zymogenic bacteria number and soil redox potential appear to be predicators of CH4 emission potential.
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INTRODUCTION
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METHANE AND NITROUS OXIDE are two important greenhouse gases emitted mostly from soil biotic sources (Duxbury et al., 1993). Methane is produced in anaerobic environments by obligate anaerobic microorganisms through either CO2 reduction or transmethylation processes. Most of the N2O produced in agricultural ecosystems is produced from denitrification under anaerobic conditions, although nitrification under aerobic conditions is also a contributor (Williams et al., 1992; Rice and Rogers, 1993). Flooded rice fields are considered one of the most important sources of atmospheric CH4 and possibly an important source of N2O (Mosier et al., 1990). The soil microbiological processes that produce these gases, methanogenesis, nitrification and denitrification, are affected by many physical and biochemical factors, such as soil pH, redox potential, temperature, and soil moisture content, etc. The content of soil oxidants (O2, NO-3, Mn4+, Fe3+, SO2-4, and CO2) used as electron acceptors for organic matter degradation contributes significantly to these processes. The reduction of various oxidants in homogeneous soil suspensions occurs sequentially at corresponding soil redox potential (Ponnamperuma, 1972; Patrick and DeLaune, 1977). Methane production rate is ordinarily high in flooded soils with high organic carbon content. Temporarily flooded soils are producers of N2O because of the availability of mineral N and the temporary oxidized condition which enables nitrification to take place (Byrnes et al., 1993). Reduced flooding duration increases N2O production, whereas continuous flooding maintains anaerobic conditions and, hence, enhances CH4 production (Neue, 1993). It is obvious that the factors affecting CH4 and N2O emissions are complicated and interrelated. An inverse relationship between CH4 and N2O emissions from a flooded rice field has been reported (Chen et al., 1997). A better understanding of the relationship between these two important greenhouse gases and the factors that govern their production is needed to identify agricultural practices such as improved management of organic matter, increasing frequency of drainage, and changing fertilization method that will mitigate the emission of the gases. The objective of this study was to understand how soil redox potential and microbiological processes interact to control the emissions of CH4 and N2O.
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Materials and methods
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Experimental Site
The field experiment was conducted at Shenyang Experimental Station of Ecology, Chinese Academy of Sciences (41°32' N, 122°23' E) in 1995 and again in 1996. The soil type is locally described as meadow brown. The main soil physico-chemical characteristics are shown in Table 1
(Chen et al., 1995).
Local field management procedures were followed in both years. Rice was irrigated with a shallow layer of water of 5 to 10 cm deep during flooded period (late May to middle of September). The size of the experimental plot was 4 by 6 m. Each plot received 90 kg of organic manure (organic matter 250 g kg-1, total N 4–5 g kg-1, P2O5 2 g kg-1, and K2O 6 g kg-1) and 0.32 kg urea 2 d before transplanting (late May). Additionally 0.32 and 0.26 kg urea were broadcast on each plot at tillering (late June) and heading (middle August), respectively. Rice was harvested the middle of October.
Gas Sampling, Analysis and Calculation
Methane and N2O were collected in a standard static chamber (0.8 by 0.8 by 1.0 m) from 1000 to 1100 h (Chen et al., 1995). This sampling time was based on the diurnal variation patterns of gas emission, assuming this pattern remained the same the whole season. The gas flux measurement was replicated four times at a frequency of 1 or 2 wk. Methane concentrations were analyzed with a SP-2305E gas chromatograph (Beijing Instrumental Factory, China) equipped with a FID detector. Nitrous oxide analyses were carried out on a Shimadzu 14A gas chromatograph with an ECD detector (Shimadzu Scientific Instruments Inc., Columbia, MD). Standard gas of CH4 and N2O was provided by National Research Institute of Standard Material, China.
Methane and N2O fluxes were calculated as follows:
is the density of gas at the absolute temperature of the chamber headspace, 
m and c are the mass and mixed ratio concentration of gas increased (or decreased) in the static chamber during t, respectively. V, A, and h are the volume of effective space, area of bottom and height of the chamber, respectively.
In Situ Soil Measurements
Air temperature and soil temperature at 5-cm depth were measured in duplicate while measuring gas emission. Soil samples of the 0- 10-cm depth were also randomly collected to determine soil physical and chemical characteristics along with microbiological activity. Soil pH was measured immediately by Orion 250A portable pH meter (Orion Research, Boston, MA) in the laboratory after the sampling. Soil NO-3-N and NH+4-N were measured in triplicate by distillation in presence of MgO and Devarda's alloy. Soil total organic acids was measured in triplicate by the improved Montgomery method with 1% (w/v) NaCl as the extractant (Wang, 1993). Soil redox potential was measured in the field by Orion 250A portable redox meter. Platinum electrodes (six replicates) which had been permanently installed at the 5-cm depth before transplanting were used, together with a calomel reference electrode.
Microbial Activity
Thirteen fresh soil samples were collected at each flux measurement day during March to October. Soil samples were incubated on media immediately after sampling to isolate six related bacteria groups and measure the activity of bacteria. Zymogenic bacteria, acetic acid and hydrogen producers, and methanogens were separated and cultivated by following the procedures described by Qian (1986). A slight modification for using soil extracts instead of fermentation solutions was adopted. Soil extracts were prepared as follows: 1000 mL distilled water was added to 1 kg fresh paddy soil. The mixture was mixed thoroughly for 30 min, and then was left overnight. Clear liquor was obtained by filtering repeatedly through 1-µm filter paper (Xinhua Paper Production Company, China). The liquor was sterilized at 121°C for 30 min and stored at 4°C. The following media were used to separate and cultivate the other three microbial groups.
CH4 oxidizers. NaNO3, 1.0 g; NH4Cl, 0.25 g; KH2PO4, 0.26 g; K2HPO4·3H2O, 0.74 g; MgSO4·7H2O, 1.0 g; CaCl2, 0.2 g; FeSO4·7H2O, 0.004 g; EDTA 0.01 g; trace element solution, 10 mL; soil extract, 100 mL; agar, 18 g; and distilled water 890 mL, pH 7.2. Three milliliter pure CH4 was injected into an 18-mL Hungate tube as a carbon source after tube rolling.
Nitrifiers. (NH4)2SO4, 2 g; K2HPO4, 1 g; MgSO4·7H2O, 0.5 g; NaCl, 2 g; FeSO4, 0.4 g; CaCO3, 5 g; H2O, 1000 mL, natural pH.
Denitrifiers. KNO3, 2 g; MgSO4·7H2O, 0.2 g; K2HPO4, 0.6 g; KNa (C4H4O6)·4H2O, 20 g; H2O, 1000 mL, pH 7.2. Durham tubes were placed in medium to observe gas production.
The most probable number (MPN) was used to enumerate the bacteria. Parameters measured and methods used for different bacteria are shown in Table 2
. The above-described in situ soil and gas emission measurements and measurements of microbial activity were carried out in 1995. In 1996, only redox potential and emissions of CH4 and N2O were measured.
Statistical Analysis
The SPSS 6.0 software package (SPSS Inc., 1996) was used to calculate regression coefficients between different variables. Confidence level of significance was determined by student t-test.
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Results and discussion
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Diurnal and Seasonal Variation of CH4 and N2O Emission
Methane emission rate was lower in the early morning and started to increase after sunrise (Fig. 1a)
. Nitrous oxide emission rate increased until 1300 h, then started to decrease (Fig. 1b). The maximum emission rates were found during 1000 to 1300 h for both CH4 and N2O. This result may be related to temperature changes as well as to the activities of the rice plant itself.
Both CH4 and N2O emissions were measured from 29 March to 7 December (Fig. 2)
. Methane emission did not occur until 3 to 4 wk after the field was flooded (late May). Methane emission rate started to increase and reached a maximum in early July (maximum tillering period). Two other emission peaks were also observed in the middle of August (heading-flowering period) and the beginning of September (maturation period). Methane emission rate decreased in the later growth period and was not detectable after the maturing of rice. This seasonal emission pattern was similar to that found in south China (Wang, 1990), Japan (Minami, 1994), and the USA (Cicerone et al., 1983). This pattern is related to temperature change, soil moisture pattern, soil reducing conditions, as well as rice growth stage.
Figure 2 also shows N2O emission pattern during the observation season. The major emission occurred only during non-flooded periods (before transplanting in latter May and after field drainage in the middle of September).
Changes in Soil Parameters during Growing Season
Temperature
The air and soil temperature change patterns were similar during the growing season (Fig. 3a)
. Soil temperature (5-cm depth) was in the range of 2 to 8.5°C in March. Soil temperature increased gradually from the end of March and reached a maximum in July. Methane emission rate reached a maximum in July as well. The soil temperature remained in the range of 17.5 to 24°C during July to mid-September and then decreased to around 0°C at the beginning of December.
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Fig. 3 Dynamics of impacting factors on gas emissions (1995): (a) temperature, (b) soil pH, (c) mineral N, (d) total organic acid, (e) redox potential
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Nitrous oxide emissions mostly occurred during the non-irrigated periods when the soil temperature was relatively low (Fig. 2). The emission rate of N2O in the drainage period (the end of September to the end of November) increased although soil temperature decreased gradually. This suggests that soil temperature was not a critical factor in N2O formation and emission in this study. The temperature effect might be masked due to existence of other factors.
Soil pH
Soil pH remained constant during the whole season (Fig. 3b), ranging from 6.9 to 7.0. This pH range is favorable for both CH4 and N2O production. Although the hydrolysis of urea after fertilization probably caused a temporary increase in soil pH which might have affected methanogenesis, nitrification, and denitrification, this effect did not last long enough to be detected within our sampling periods.
Soil Mineral Nitrogen
Soil mineral N showed a significant increase following the application of urea and organic manure in May because of lower plant uptake at beginning of season. No obvious accumulation of mineral N was detected after broadcasting urea in June and August because plant assimilation was high and soil samples for mineral N analysis were not collected immediately after urea fertilization (Fig. 3c). No significant correlation was found between soil mineral N and CH4 emission during the growing season; however, basal fertilization in May and broadcasting in August were followed by an increase in N2O emission (Fig. 2), probably as a result of more inorganic N being available for both nitrification and denitrification.
Soil Organic Acid
The majority of organic acids in flooded soil are volatile, low molecular weight, saturated fatty acids in the sequence of formic acid, acetic acid, propionic acid, and butyric acid. Total soil organic acid was measured during the whole season (Fig. 3d). A significant correlation between CH4 emission and the total amount of the organic acids was observed during June 14 to Sept. 22 (r = 0.83, n = 7, 5% confidence level). The maximum amount of organic acids was found on July 4 (6.8 µmol 100 g-1 dry soil) when CH4 emission rate was also the highest. This observation reflects the effect of lower redox potential on soil organic acid production that in turn stimulates CH4 formation.
Soil Redox Potential
Soil redox potential was above +300 mV before field irrigation in late May (Fig. 3e). Redox value decreased sharply after the field was flooded by 5 to 10 cm of water, and reached a level lower than -200 mV within about 30 d. This low value was maintained for 
2 mo during which a large amount of CH4 was emitted. Soil redox potential increased rapidly following the drainage of the field during the maturation period. The value rose to +145 mV 3 days after drainage, and then continued to move up although it fluctuated due to rainfall. Significant N2O emission only occurred above approximately +200 mV. As soil redox potential decreased, less N2O was emitted. This was probably related to the reduction of N2O to N2 under low redox potential conditions.
Interrelationship between CH4 and N2O Emissions in Relation to Redox Potential
An examination of the CH4 and N2O emission patterns in relation to redox potential shows that CH4 emission was highest when redox potential was lowest and that N2O emission was at a minimum at the same time. At high redox values, N2O emission was high with no CH4 emission (Fig. 4)
. These findings suggest that production of both gases is a function of soil redox potential. The critical soil redox potential for CH4 and N2O production has been demonstrated in laboratory studies to be below about -150 mV for CH4 and above about +250 mV for N2O (Wang et al., 1993; Masscheleyn et al., 1993). These critical soil redox potentials suggest that CH4 and N2O production rarely occur at the same time. When soil redox potential is relatively high, soil nitrification takes place which results in N2O production. Nitrous oxide is mostly produced through nitrate reduction when the soil becomes moderately reducing or when the nitrate diffuses into a zone that is less oxidized than the zone in which it is formed. Soil redox potential becomes lower if there is sufficient soil organic carbon. This lower potential enables CH4 formation to occur. Our field experiment showed a significant negative correlation between CH4 and N2O emissions (r = -0.49, n = 16, 5% confidence level), suggesting that there is a risk of increasing N2O emission by manipulating water management to raise the redox potential in order to reduce CH4 emission. These results also suggest that if the redox potential of the soil is kept above the level necessary to support CH4 formation and kept below the moderately reducing condition where N2O is formed, production of both gases could be minimized. This favorable redox potential range appears to be between approximately -100mV and +200 mV. In this range the redox potential is too high to support CH4 production but low enough to favor N2 production over N2O production during the denitrification process. Earlier laboratory studies support this conclusion (Wang et al., 1993; Masscheleyn et al., 1993).
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Fig. 4 Relationship between CH4 and N2O emissions and redox potential in rice field throughout the season (1996)
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Methane and N2O Emission in Relation to Soil Microbiological Activities
The production of CH4 is the result of the activity of different groups of microorganisms including zymogenic bacteria, acetic acid and hydrogen-producers, and methanogens. The metabolism of these different microbial groups completes the degradation of organic carbon from large molecules to the most reduced status i.e. CH4. Most of the CH4 produced in paddy soils is oxidized by CH4 oxidizers before being released into the atmosphere (Conrad and Rothfuss, 1991). Thus, the emission of CH4 is the balanced result of both production and oxidation. Similarly N2O production is the balanced result of two important microbiological processes—nitrification and denitrification.
Our result shows that the numbers of nitrifiers, denitrifiers, zymogenic bacteria, and CH4 oxidizers increased with an increase in temperature before submergence of the field (Fig. 3a, Fig. 5 and 6) ; however, the acetic acid and hydrogen producers as well as methanogens were present in small numbers suggesting that the activities of zymogenic bacteria provided energy for nitrifiers and denitrifiers. Nitrous oxide was significantly produced before field submergence. Apparently the O2 in the soil system was not depleted at this time and the strongly reducing conditions favoring N2 production had not yet developed. After submergence, the numbers of zymogenic bacteria, acetic acid and hydrogen producers, and methanogens increased substantially and reached the highest numbers sequentially. The number of zymogenic bacteria increased from 2.5 x 104 to 7.5 x 106 colony forming units per gram dry soil, acetic acid and hydrogen producers from 2.5 x 104 to 1.5 x 106, and methanogens 3.2 x 103 to 1.8 x 107. Although there was no significant change in the numbers of nitrifiers, CH4 oxidizers and denitrifiers, the enzyme activities of nitrifier and CH4 oxidizer such as ammonia-monooxygenase and methanomonooxygenase might be inhibited because of lack of available O2. The dominant end product of denitrification was likely N2 because of the low soil redox potential which favored N2 over N2O. Methane was the main greenhouse gas produced during the flooded period with almost no N2O production observed. After drainage at the end of the growing season, the acetic acid and hydrogen producers started to decrease. Although the number of methanogens remained high, the reductase system responsible for CH4 production was inhibited due to presence of oxidants such as O2, while CH4 oxidation activity was enhanced. Nitrous oxide emissions increased during the nonflooded season. As soil redox potential increased, soil conditions became more favorable for N2O production first through denitrification, and then by nitrification following O2 entering into the soil.
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Fig. 6 Relationship between N2O emission and related bacterial groups in rice field - (Denitrifiers 1: NO-2 was used as the indicator to determine the activity of denitrifiers; Denitrifiers 2: N2O + N2 was used as the indicator)
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Regression Analysis
Methane and N2O emissions from paddy rice fields are the end result of microbiological processes which are affected by soil physical and chemical characteristics. The relationships among gas emissions, related bacteria, and impacting factors can be quantitatively expressed by adoption of multiple regression analysis based on the simultaneous measurements of these different variables.
Methane and N2O Emission and the Number of Related Bacteria
A significant correlation between the logarithm number of zymogenic bacteria and CH4 emission rate was observed (r = 0.76, n = 12, 1% confidence level).
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No significant correlation between CH4 emission and the number of acetic acid and hydrogen producers, methanogens, and CH4 oxidizers was shown. A correlation between the numbers of nitrifiers and denitrifiers and N2O emission was not found either. Because of the involvement of soil enzymes in these processes, we believe that the nonsignificant correlation between gas emissions and the number of some related bacteria does not necessarily indicate a lack of relationship between these variables. In some cases, the direct effect of soil enzyme is more important than bacteria from which the enzyme was produced. The significant correlation between the logarithm of zymogenic bacteria number and CH4 emission shows the direct effect of this microorganism on CH4 production. As mentioned above, CH4 is the end product of a series of processes of organic carbon degradation in anaerobic soil environments. Zymogens are the first group of bacteria which are involved in this chain reaction. Therefore, the production rate of CH4 is likely to be restricted by the rate of fermentation, which is stimulated by zymogenic bacteria. This result helps to explain the observation of previous studies by Yagi and Minami (1990) and Wang et al. (1993) who indicated a significant correlation between CH4 production rate and easily degradable carbon. It also suggests the possibility of using the number of zymogenic bacteria as an index to predict the CH4 emission potential of the soil. The activity of zymogenic bacteria may reflect the comprehensive influence of soil environmental factors including soil organic carbon, moisture content, pH, etc. on the chain reaction of anaerobic carbon decomposition which indicates the potential rate of CH4 production.
In addition, the number of zymogenic bacteria was significantly correlated to soil redox potential (r = -0.78, n = 12, 1% confidence level).
This inverse relationship indicates the demand of zymogenic bacteria for an anaerobic environment. Low soil redox potential indicates a favorable growth condition for zymogenic bacteria.
Emission of CH4 in Relation to Soil Redox Processes
A significant correlation was found between soil redox potential and CH4 emission (r = -0.72, n = 12, 1% confidence level).
Our result agrees with the result of Yagi et al. (1995), although we did not obtain an exponential relationship between soil redox potential and CH4 emission as observed by Wang et al. (1993) in a homogeneous soil suspension. This might be due to the more complicated field environment.
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Conclusions
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The dynamics of CH4 and N2O emission in a paddy rice field are closely related to soil redox potential and microbial activity. The inverse relationship between CH4 and N2O emissions with changes in soil redox potential was identified in field experiments. This inverse relation indicates the risk of promoting N2O production when eliminating CH4 production by increasing soil redox potential (e.g., drainage). It also demonstrates the difficulty of controlling N2O emission by simply keeping the soil reduced enough to favor N2 production over N2O production during the denitrification process. Water management and organic matter practices should be developed to maintain the soil redox potential at an intermediate range (around -100 to +200 mV). This range is high enough to prevent CH4 production, but low enough to encourage N2O reduction to N2 and minimize the emissions of both of these greenhouse gases.
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ACKNOWLEDGMENTS
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This study was funded in part by Chinese Academy of Sciences, USDA, Louisiana Board of Regents, and University of Ghent, Belgium.
Received for publication June 12, 1998.
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ABSTRACT
INTRODUCTION
