This is a self-archiving file for Tokida et al. 2012 published in Plant and Soil, DOI: 10.1007/s11104-012-1356-7. The final
publication is available at http://www.springerlink.com/content/x508n4701m5l1215/?MUD=MP.
1
The contribution of entrapped gas bubbles to the soil methane pool
and their role in methane emission from rice paddy soil in free-air
[CO2] enrichment and soil warming experiments
Takeshi Tokida, Weiguo Cheng, Minaco Adachi, Toshinori Matsunami, Hirofumi Nakamura,
Masumi Okada, Toshihiro Hasegawa

Abstract
 Purpose We attempted to determine the contribution of
entrapped gas bubbles to the soil methane (CH 4) pool and
their role in CH4 emissions in rice paddies open to the
atmosphere.
 Methods We buried pots with soil and rice in four
treatments
comprising
two
atmospheric
CO 2
concentrations (ambient and ambient +200 μmol mol–1) and
two soil temperatures (ambient and ambient +2°C). Pots
were retrieved for destructive measurements of rice growth
and the gaseous CH4 pool in the soil at three stages of crop
development: panicle formation, heading, and grain filling.
Methane flux was measured before pot retrieval.
 Results Bubbles that contained CH4 accounted for a
substantial fraction of the total CH 4 pool in the soil:
26–45% at panicle formation and 60–68% at the heading
and grain filling stages. At panicle formation, a higher CH 4
mixing ratio in the bubbles was accompanied by a greater
volume of bubbles, but at heading and grain filling, the
volume of bubbles plateaued and contained ~35% CH4. The
bubble-borne CH4 pool was closely related to the putative
rice-mediated CH4 emissions measured at each stage across
the CO2 concentration and temperature treatments.
However, much unexplained variation remained between
the different growth stages, presumably because the CH 4
transport capacity of rice plants also affected the emission
rate.
 Conclusions The gas phase needs to be considered for
accurate quantification of the soil CH4 pool. Not only
ebullition but also plant-mediated emission depends on the
gaseous-CH4 pool and the transport capacity of the rice
plants.
Keywords rice paddy, methane, entrapped bubbles, free-air
CO2 enrichment, soil warming, climate change
Abbreviations
FACE free air CO2 enrichment
[CO2]
CO2 concentration
Received: 18 April 2012 / Accepted: 28 June 2012.
Responsible Editor: Tim Moore
T. Tokida (corresponding author)•T. Hasegawa
National Institute for Agro-Environmental Sciences,
3-1-3 Kannondai,
Tsukuba, Ibaraki 305-8604, Japan
email: tokida@affrc.go.jp
T. Matsunami
Akita Prefectural Agriculture, Forestry and Fisheries
Research Center,
34-1 Yuwaaikawa-aza-genpachizawa,
Akita 010-1231, Japan
W. Cheng
Faculty of Agriculture,Yamagata University,
1-23 Wakaba-cho,
Tsuruoka, Yamagata 997-8555, Japan
H. Nakamura
Taiyo Keiki Co., Ltd, Tokyo,
114-0032, 1-12-3 Nakajujo,
Kita-ku, Tokyo 114-0032, Japan
M. Adachi
National Institute for Environmental Studies,
16-2 Onogawa,
Tsukuba, Ibaraki 305-8506, Japan
M. Okada
Faculty of Agriculture, Iwate University,
3-18-8 Ueda,
Morioka, Iwate 020-8550, Japan
This is a self-archiving file for Tokida et al. 2012 published in Plant and Soil, DOI: 10.1007/s11104-012-1356-7. The final
publication is available at http://www.springerlink.com/content/x508n4701m5l1215/?MUD=MP.
INTRODUCTION
Rice-paddies are one of the largest anthropogenic sources of
atmospheric methane (CH4), a potent greenhouse gas. The
estimated radiative forcing (global warming potential; Shine et
al. 1990) of CH4 relative to the same mass of CO2 over a
100-year forward prediction has steadily increased with
successive estimates, from 21 in the mid-1990s (Schimel et al.
1995) to 23 (Ramaswamy et al. 2001), 25 (Forster et al. 2007),
and ~30 (Shindell et al. 2009) through the 2000s. This increase
has been influenced by an improved understanding of the
importance of the indirect effects of CH4, especially its role in
the production of ozone in the troposphere and water in the
stratosphere, both of which are potent greenhouse gases
(Hansen et al. 2005; Shindell et al. 2005). If these indirect
effects are taken into account, atmospheric methane contributes
almost half as much radiative forcing as atmospheric CO2
(Shindell et al. 2009). To reduce CH4 production would be an
economically effective way of mitigating global warming over
the next several decades because of its strong radiative forcing
and short residence time in the atmosphere (Shindell et al.
2012).
Aside from the greenhouse effect, CH4 plays an important
ecological role as an end point for the “final disposal” of carbon
compounds in rice-paddy ecosystems. In anoxic water-logged
soils, fermentative decomposition dominates dissimilatory
processes, yielding various organic acids (Stams 1994; Schink
1997). Without the completion of these biochemical pathways
that lead to CH4 production, these organic acids may remain in
the soil and negatively affect rice growth, either directly
(Armstrong and Armstrong 2001) or indirectly by increasing
the concentration of Fe(II), a substance toxic to rice plants
(Becker and Asch 2005).
Because of its low solubility and lack of an ionic form, CH 4
escapes rapidly from the dissolved state in soil solution into the
gas phase to form bubbles within the soil that eventually escape
to the atmosphere. The solubility of CH4 is less than
one-twentieth that of CO2 within the temperature range of
20–40°C (Wilhelm et al. 1977; Clever and Young 1987).
Therefore, the concentration of dissolved CH4 in soil solution
was found to be an order of magnitude smaller than that of CO2,
even during the methanogenic phase, when equal molar
amounts of CH4 and CO2 were being produced from organic
compounds (Tokida et al. 2011). By contrast, many studies
have shown a very high CH4 mixing ratio (defined as the
number of molecules divided by the sum of the total number of
gas molecules, i.e. mole fraction) in the bubbles (over 50% in
some cases) in rice-paddy soils (Holzapfel-Pschorn et al. 1986;
Uzaki et al. 1991; Watanabe et al. 1994; Byrnes et al. 1995;
Rothfuss and Conrad 1998; Watanabe and Kimura 1998;
Cheng et al. 2005; Han et al. 2005; Cheng et al. 2008a). As a
corollary of these two tendencies, a major portion of the soil
CH4 pool may exist in the gas phase (i.e., in trapped bubbles)
even in water-logged soils (Wassmann et al. 1996; Bosse and
Frenzel 1998; Cheng et al. 2005), presenting a sharp contrast to
CO2, almost all of which exists in dissolved form (Tokida et al.
2
2009).
Despite these facts, we presently have limited knowledge
about the role of entrapped bubbles in CH4 retention in the soil
and the transfer of CH4 to the atmosphere. For example, in most
studies involving CH4 inventory, the authors have assumed that
the dissolved form is the sole CH4 reservoir, neglecting the
bubble form. Plant-mediated transport of CH4 has attracted
much attention (Nouchi et al. 1990; Wang et al. 1997), whereas
the release of CH4 in bubbles (often termed “ebullition”) has
rarely been quantified, although a few studies have revealed
that ebullition can be important during the early growing season
(Wassmann et al. 1996). Although rice plants might act as a
conduit between the bubble-borne CH4 reservoir and the
atmosphere, we are aware of only a few studies of the role of
the bubble-borne CH4 reservoir in rice-mediated CH4 emissions
(Hosono and Nouchi 1997; Bazhin, 2010).
We conducted a field study in a Japanese rice paddy to improve
our understanding of the role of entrapped bubbles in the
retention of CH4 in the soil, the overall soil pool size of CH4,
and the emission of CH4 into the atmosphere. We hypothesized
that entrapped bubbles would represent a major proportion of
the CH4 inventory, even in apparently water-saturated soil, and
that they may be an important factor controlling CH 4 emission
over the course of rice crop development. We also investigated
how an increase in the atmospheric CO2 concentration ([CO2])
and elevated soil temperature would affect the CH4 pool in the
soil and the flux of CH4 from the soil pool to the atmosphere.
Recent studies have suggested that high [CO2] and soil
warming treatments significantly increase the CH4 emission
from rice paddies (Tokida et al. 2010); however, the effects of
[CO2] and soil warming on CH4 pool size and its relationship to
the emission rate are not well understood. The field study was
conducted at a free-air CO2 enrichment (FACE) facility where
[CO2] can be elevated by 200 μmol mol–1 (ppm equivalent)
above ambient by fumigating with pure CO2 (Okada et al.
2001). Subplots of elevated temperature (+2°C) were nested
within both high and ambient [CO2] plots.
MATERIALS AND METHODS
Study site, CO2 enrichment, and soil-warming treatments
We conducted the study in the 2007 growing season of the
rice-FACE (free-air CO2 enrichment) experiment at
Shizukuishi, Iwate, Japan (39°38′ N, 140°57′ E). Rice
plants were grown in an open field, contained within pots
(described in the section "Preparation of pot cultures") so that
we could accurately quantify the pool size of CH4, especially
the CH4 within gas bubbles entrapped in the soil. We
maintained the environmental conditions as uniform as possible
for the pots and for the surrounding rice plants grown directly in
the soil. We buried the pots into the plowed FACE
experimental fields so that the pots would experience the same
[CO2] and temperature treatments as the surrounding area.
We used the same experimental fields described by Tokida et
al. (2010). Briefly, two paddy fields were assigned to each of
This is a self-archiving file for Tokida et al. 2012 published in Plant and Soil, DOI: 10.1007/s11104-012-1356-7. The final
publication is available at http://www.springerlink.com/content/x508n4701m5l1215/?MUD=MP.
three blocks (replicates for [CO2] treatment); one field had an
ambient [CO2] level and the other field was CO 2-enriched
(FACE). Each FACE ‘ring’ was an octagonal arrangement of
eight 5-m long horizontal emission tubes with a resultant
diameter of 12 m across. The FACE plots had a target
concentration of 200 μmol mol–1 above ambient using a pure
CO2 injection FACE system (Okada et al. 2001). The FACE
system operated only during the daylight hours. The
season-long daytime average [CO2] (measured by LI-820;
LI-COR, Inc., USA) was 568 μmol mol −1 in the FACE plots
and 376 μmol mol−1 in the ambient-[CO2] plots. The fraction of
time that the 1-min average [CO2] deviated by <10% or <20%
from the target [CO2] was used to indicate the performance of
the [CO2] control. Averaged over the season and the three
FACE rings, 68% of the time the deviation was within 10% and
91% of the time it was within 20%.
Our FACE experiment included a split-plot factor for two
levels of soil and ponded-water temperature: an ambient
temperature plot and an elevated temperature plot, with the
latter targeted at 2°C above ambient. The surface soil and water
were warmed using thermostatically controlled heating wires
placed on the soil surface between the rows. The soil and water
temperature of both plots was continuously measured by Pt100
thermometer and recorded in CR10X (Campbell Scientific Inc.,
USA). The temperature of the water and plow-layer soil was
almost uniformly elevated, because the field was kept flooded
(standing water depth was 3−6 cm) and the elevated
temperature plots were enclosed with corrugated boarding to
minimize the lateral movement of water. The elevated
temperature plot was enclosed by corrugated PVC panels to
prevent rapid exchange of paddy water in the plot area with that
from the surrounding area. The warming facility successfully
maintained an increased soil temperature until the middle of the
grain filling stage. The seasonal mean temperature elevation
was 1.9 ± 0.1°C (mean ± SD, n = 6) for the surface soil (0 cm)
and 1.8 ± 0.1°C (mean ± SD, n = 6) at 10-cm depth (Tokida et
al. 2010). All agronomic practices were the same as those of
local farmers with the exception that midseason drainage was
not carried out so that the warming treatments would be
continuous.
Preparation of pot cultures
Soils used for the pot cultivation were collected from the
corresponding fields 1 month before transplanting; we obtained
soils from six paddy fields (two CO2 levels times three blocks).
The soil in the study site was an Andosol (according to World
Reference Base for Soil Resources) with a mean organic C
content of 77.8 ± 15.3 g kg–1 DW (mean ± SD, n = 6) and total
N of 4.8 ± 0.9 g kg–1 DW (mean ± SD, n = 6) (Tokida et al.
2010). The dry bulk density of the pot soil was 0.638 ± 0.057
Mg m–3 (mean ± SD, n = 6, ranging from 0.580 to 0.737 Mg
m–3) and the porosity was 75.5 ± 2.2% (mean ± SD, n = 6,
ranging from 71.7 to 77.7%). Such a low bulk density and high
porosity are typical characteristics of the volcanic ash soils that
are common in Japan (Maeda and Soma 1986).
3
We sowed rice seeds (Oryza sativa L. cv. Akitakomachi) on
23 April 2007 in seedling trays. The seedlings to be
subsequently used for the ambient-[CO2] and FACE plots were
raised in two different chambers, one under ambient [CO2] and
the other under elevated [CO2] (ambient +200 μmol mol–1).
The pots were round (13.5 cm × 16 cm, D × H) with an inner
volume of 2230 mL. On 23 May 2007, 1 week before
transplanting, the soil was puddled and mixed with fertilizer.
All fertilizers were applied as a basal dressing. Nitrogen was
supplied at a rate of 0.96 g N pot–1 (0.16 g N as ammonium
sulfate, 0.32 g N as LP-70, and 0.48 g N as LP-100 [LP-70 and
LP-100 are coated-urea fertilizer, Chisso-asahi Fertilizer Co.,
Ltd., Tokyo, Japan]), potassium at a rate of 1.33 g K pot–1 (0.8 g
K as KCl and 0.53 g K as potassium silicate), and phosphorus at
a rate of 1.39 g P pot–1 as fused magnesium phosphate. These
fertilizer rates supplied the equivalent of 18 g N m–2, 25 g K m–2,
and 26.2 g P m–2.
Seedlings were transplanted from seed trays to pots by hand
at a rate of three seedlings per pot. The pots were then placed
into the field so that the surface of the soil in the pot was at a
level flush with the surrounding soil. Because we conducted
destructive sampling (see the next section), nine pots were
buried in each experimental unit.
Flux measurements
Methane flux was measured using the static chamber method
(Hutchinson and Livingston 2002) on three occasions
corresponding to different growth stages of rice: panicle
formation (48–50 days after transplanting, DAT), heading
(75–77 DAT), and the middle of grain filling (105–106 DAT).
At each growth stage, three pots were measured for CH 4 flux
after which the pots were retrieved for destructive sampling
from each experimental plot. As the pot did not have drainage
hole, the soil was kept wet until soil-bubble collection (see next
section). The flux measurements were made twice, once in the
nighttime (natural, not enforced condition) and once in the
daytime for each pot. Because the number of chambers for the
flux measurements was limited, we needed to carry out three set
of measurements at separate times (one set consisted of
nighttime and daytime measurements). In order to complete the
three sets of measurements as short a time as possible in a
practical way, the daytime flux measurement came first for
some pots followed by the nighttime measurements and the
opposite order was true for the other pots.
An acrylic, cylindrical chamber consisting of a lower (25 ×
60 cm, D × H) and upper (26.7 × 50 cm, D × H) section was
placed over each pot. The upper section of the chamber fitted
over the lower one and was supported by a water-filled groove
surrounding the outer top lip of the lower section, thus
providing an airtight seal between the two sections and the
surrounding atmosphere. After placement of the chamber over
a pot, gas samples were collected at intervals of 0, 10, and 20
min in the daytime and 0, 5, 10, and 15 min in the nighttime.
The samples were injected into pre-evacuated 20 mL bottles
and transported to the laboratory for analysis within a week.
This is a self-archiving file for Tokida et al. 2012 published in Plant and Soil, DOI: 10.1007/s11104-012-1356-7. The final
publication is available at http://www.springerlink.com/content/x508n4701m5l1215/?MUD=MP.
4
The mixing ratio of CH4 was analyzed using a GC system
(GC-14B; Shimazu, Kyoto, Japan). Details of combination of
GC columns used in the present analysis were provided by
(Sudo 2006). The efflux rate of CH4 was calculated from the
increase in the gas mixing ratio, the basal area of the chamber,
and the chamber volume, and the temperature inside the
chamber. We assumed that the air pressure in the chamber was
101.325 kPa (1 atm). For nighttime measurements, we also
calculated CO2 emission rates which represent dark respiration
by rice plants because soil respiration from the flooded soil is
generally small.
Ideally, it is desirable to quantify both non-bubbling and
naturally occurring bubbling emissions; however, it is difficult
to accurately estimate a time-representative value of bubble
release because it may occur episodically (Tokida et al. 2007).
Non-bubbling flux should result in a linear increase in CH4
concentration over time. Therefore, to exclude ebullition flux
we set two arbitrary criteria by which the linearity of increase in
the chamber CH4 concentration could be satisfied, a technique
adopted in many previous studies (e.g. Sass et al. 1990;
Buendia et al. 1998): (i) for daytime measurements, we
assumed that the flux was not influenced by ebullition if the
rates of CH4 concentration increase during the 0–10 min and
10–20 min periods did not differ greater than 50% (equivalent
to R2 > 0.9868); (ii) for nighttime measurements, we first
checked the linearity of CH4 concentration versus time (at 0, 5,
10, and 15 min) and rejected the data if the R 2 value was less
than 0.9800; if the data were not rejected we then applied a
similar test for linearity as for daytime measurements; in this
case, though, we assumed that the change in CH4 concentration
was not influenced by ebullition if the increments during the
0–10 min and 5–15 min periods did not differ greater than 50%.
We also discarded measurements that indicated a negative CH4
flux (only one such measurement was obtained). Methane flux
measurements accompanied by erratic CO2 emission rates
(nighttime measurements only) were also rejected because such
erratic CO2 emission data suggest that errors may have
occurred during pre-evacuation of the sample bottles or in the
gas chromatography analysis (12 measurements).
original level. A portion of the gas (about 30 mL) was
transferred into a 20-mL vacuum bottle for the purpose of
measuring the mixing ratio of CH4 by using a gas
chromatograph (GC-14A; Shimadzu, Kyoto, Japan) equipped
with a flame-ionization detector. After the gas sampling, the
rice roots in the pot were gently and thoroughly washed with
water. The aboveground parts and roots of the rice plants were
oven-dried at 80°C for 72 h to measure dry matter weight.
Sampling of rice plants and soil bubbles
Calculation of the dissolved and gaseous CH4 inventories in the
soil
Within 2 hours after the collection of pots from the field, the
aboveground parts of the rice plant were severed above 3 cm
from the soil surface and removed, and soil bubbles were
collected from each pot using a method described by Uzaki et al.
(1991). Each pot was placed into a large bucket (35 × 50 cm, D
× H) containing 30 L of tap water, and an inverted plastic
funnel (30 cm in diameter) with a rubber cap in the spout was
filled with water up to the level of the stopper and then placed
with its rim below the water and positioned above the pot to
collect any bubbles released when the soil in the bucket was
manually stirred by hand (Fig. 1). Three minutes was enough to
complete the manual ejection of the bubble. The gas space
developed in the cone of the funnel was then extracted with a
60-mL plastic syringe until the water level returned to its
We calculated the amounts of CH4 present in the gaseous phase
and dissolved in the aqueous phase using the volume ratio of
the two phases and the mixing ratio of CH4 in the gas phase
(Tokida et al. 2005). We assumed that CH 4 was in equilibrium
between the two phases (Watanabe and Kimura 1995)
according to Henry’s law (Clever and Young 1987). We also
assumed that the pressure of the gas phase was 101.325 kPa (1
atm) because hydrostatic pressure was relatively small (< 2% of
air pressure). Water temperature at soil-bubble sampling was
measured and assumed to be equal to the temperature of gas and
aqueous phase of the pot.
To evaluate the importance of the gas-phase in the CH4
inventory, we estimated the fraction of gaseous CH4 in the total
syringe
funnel
Rice pot
Fig. 1 Diagram showing how gas bubbles were collected from the rice
pots.
This is a self-archiving file for Tokida et al. 2012 published in Plant and Soil, DOI: 10.1007/s11104-012-1356-7. The final
publication is available at http://www.springerlink.com/content/x508n4701m5l1215/?MUD=MP.
(gas + solution) inventory (r) which can be theoretically
calculated from
r = x / [x + (1/H)],
(1)
where x is the volumetric ratio of gas to water content and H is
the dimensionless Henry’s law constant (Tokida et al. 2009).
Note that H is temperature dependent and can be reasonably
approximated in the range from 0°C to 40°C by
H = –5.742 × 10-5 T3 + 8.91× 10-4 T2 + 0.479 T + 17.4
(2)
where T is the temperature (°C). To estimate x, the solid content
was directly measured in addition to the volume of bubbles, and
the water content was estimated by subtraction.
Statistical analyses
(Littell et al. 2006). Percentage data were arcsine-transformed
to homogenize the variance before statistical analysis (Gomez
and Gomez 1984).
A simple correlation analysis was performed to determine
the most important factors controlling CH4 emissions. The
potential explanatory variables included surface soil
temperature, parameters related to the bubble-borne CH4 pool
(bubble volume, mixing ratio of CH 4, and mass of bubble-borne
CH4), and plant parameters (aboveground and root biomass,
tiller number, and dark respiration from the nighttime
measurement). Methane flux and temperature data were
analyzed separately for the day and night values, but for the
parameters related to the CH4-pool and rice plants, the same
values were used for day and night because they were
determined by destructive sampling.
RESULTS
The effects of high [CO2] and elevated temperature treatments
were analyzed by ANOVA for a split-plot randomized
complete-block experimental design with three replications;
[CO2] was treated as the fixed-effect whole-plot factor and
temperature as the split-plot factor. In addition, growth stage
was treated as a fixed-effect repeated-measures with the
experimental units as subjects. The computations were
performed with PROC MIXED of SAS v9.2 (SAS Institute,
Inc., Cary, NC) by the restricted maximum-likelihood method
to test the main effects and interactions of the fixed effects
Table 1 Effects of [CO2] and soil
temperature on plant growth parameters
at three different growth stages in a
CO2-enrichment and
elevated-temperature growth
experiment with paddy rice.
Stage
Panicle
formation
Heading
Grain
filling
Statistics
Rice growth
Overall, the rice growth parameters responded similarly to the
[CO2] and temperature treatments whether the rice was grown
in the pots or in hills (Tokida et al. 2010). Although not
statistically significant, FACE tended to increase both the
aboveground (P = 0.18) and root biomasses (P = 0.12). Soil
warming stimulated the aboveground biomass significantly (P
< 0.001) but its effect on root biomass depended on the growth
stage of the rice (P < 0.05 for Stage × Temperature): at panicle
formation, there was no discernible difference between the
FACE-ET
FACE-AT
Amb-ET
Amb-AT
FACE-ET
FACE-AT
Amb-ET
Amb-AT
FACE-ET
FACE-AT
Amb-ET
Amb-AT
Aboveground
biomass
(g pot–1)
30.7
26.2
28.2
23.0
62.7
52.2
56.9
49.4
87.2
78.4
80.0
76.7
Root
biomass
(g pot–1)
4.5
4.6
4.6
4.4
5.4
5.4
4.9
5.2
4.8
5.6
4.4
5.1
6.9
5.7
6.2
5.2
11.7
9.7
11.7
9.4
18.1
14.0
18.2
15.1
Tiller
number
(# pot–1)
33.4
34.2
34.6
33.7
28.9
28.6
31.1
30.2
28.1
27.6
26.0
27.3
CO2
ns (P = 0.18)
ns (P = 0.12)
ns
ns
***
**
***
ns
CO2 × T
ns
ns
ns
ns
Stage (S)
***
***
***
***
S × CO2
ns
ns
†
ns
S×T
ns
*
***
ns
S × CO2 × T
ns
ns
ns
ns
Treatment
Temperature (T)
ns, not significant; †, P < 0.1; *, P <
0.05; **, P < 0.01, ***, P < 0.001
Treatment abbreviations: FACE,
free-air CO2 enrichment by 200 μmol
mol–1 above ambient; ET, elevated
temperature by 2°C above ambient; AT,
ambient temperature; Amb, ambient
CO2.
5
Shoot-to-root
ratio
This is a self-archiving file for Tokida et al. 2012 published in Plant and Soil, DOI: 10.1007/s11104-012-1356-7. The final
publication is available at http://www.springerlink.com/content/x508n4701m5l1215/?MUD=MP.
6
Table 2 Attributes of CH4 in bubbles trapped in the soil and the non-bubble flux of CH4 to the atmosphere in different treatment plots at
three growth stages in a CO2-enrichment and elevated-temperature growth experiment with paddy rice
Stage
Panicle
formation
Heading
Grain
filling
Statistics
Treatment
Bubble volume
(mL pot–1)
FACE-ET
FACE-AT
Amb-ET
Amb-AT
FACE-ET
FACE-AT
Amb-ET
Amb-AT
FACE-ET
FACE-AT
Amb-ET
Amb-AT
42.6
29.4
34.4
21.7
92.8
88.0
88.8
83.2
118.1
100.2
112.1
97.7
Mixing ratio
of
CH4 in
bubbles (%)
5.5
2.1
5.2
1.6
13.5
19.5
18.7
18.1
43.5
25.5
44.4
27.7
1.6
0.4
1.1
0.2
6.2
8.8
8.2
7.9
25.8
12.9
24.5
14.8
Fraction of
gas-phase CH4
inventory to the
total (%)
45
36
40
26
61
60
61
60
68
64
67
65
CO2
ns
ns
ns
ns
ns
ns
Temperature (T)
**
***
**
***
*
†
CO2 × T
ns
ns
ns
ns
ns
ns
Stage (S)
***
***
***
***
***
*
S × CO2
ns
ns
ns
*
ns (P = 0.13)
ns
S×T
ns
***
***
**
†
ns
S × CO2 × T
ns
ns
ns
ns
ns
ns
Bubble CH4
storage (mg
C pot–1)
Daytime
CH4 flux
(mg C m–2
h–1)
14.2
7.3
14.6
7.7
25.1
24.4
26.8
28.9
41.4
14.6
21.0
14.0
Nighttime
CH4 flux
(mg C m–2
h–1)
21.1
11.0
18.6
15.3
16.2
15.3
19.0
18.5
12.6
9.1
13.2
12.2
ns, not significant; †, P < 0.1; *, P < 0.05; **, P < 0.01; ***, P < 0.001
Treatment abbreviations: FACE, free-air CO2 enrichment by 200 μmol mol–1 above ambient; ET, elevated temperature by 2°C above
ambient; AT, ambient temperature; Amb, ambient CO2
ambient and elevated temperature treatments, but at heading the
elevated temperature treatment had a significantly reduced root
biomass, and the degree of root-mass reduction was greater at
the grain filling stage (Table 1). Such contrasting effects of
temperature on aboveground and root biomass were reflected in
the shoot (aboveground) to root ratio; it was always larger in the
elevated temperature than ambient temperature treatments (P <
0.001), and the difference became larger at successive growth
stages (P < 0.001 for Stage × Temperature).
Pool size of gas-phase CH4 in the soil
The use of pots enabled us to accurately quantify the CH4 pool
in bubble form in the flooded soil. The volume of the bubbles
increased with growth stage (Table 2). Elevated temperature
significantly increased the volume of bubbles (P < 0.01),
especially at the panicle formation (+51%, averaged over the
[CO2] treatments) and grain filling stages (+16%). Elevated
[CO2] also tended to increase the volume of bubbles, especially
at panicle formation (+28%, averaged over the temperature
treatments), although the difference was not statistically
significant. Gas composition analysis revealed a high mixing
ratio of CH4 in the trapped gas bubbles (Table 2) which
increased over the growing season and exceeded 35% at the
grain filling stage (averaged over the CO2 and temperature
treatments). The soil warming treatment increased the CH4
mixing ratio at panicle formation (+189%) and at grain filling
(+65%), but not at heading. The effect of FACE on the mixing
ratio of gas in bubbles was not obvious at any stage. The
amount of CH4 in bubble form built up over time: 0.8 mg C
pot–1 at panicle formation, 7.8 mg C pot–1 at heading, and 19.5
mg C pot–1 at grain filling (averaged over the four treatments)
(Table 2). The warming treatment dramatically increased the
storage of CH4 in gas form at panicle formation (+379%) and at
the grain filling stage (+81%), but not at heading. A significant
FACE effect was seen only at panicle formation (+55%).
The presence of entrapped bubbles allowed the gas-phase
CH4 to be a major component of the soil CH4 pool (Table 2).
The proportion of the total CH4 (gaseous + dissolved form)
present in bubbles was 37% at panicle formation, 61% at
heading, and 66% at grain filling (averaged over the four
treatments). Elevated temperature increased the gas-phase
fraction at all stages (P < 0.001), but more at panicle formation
This is a self-archiving file for Tokida et al. 2012 published in Plant and Soil, DOI: 10.1007/s11104-012-1356-7. The final
publication is available at http://www.springerlink.com/content/x508n4701m5l1215/?MUD=MP.
than at the other stages, as indicated by the significant “stage ×
temperature” interaction. Elevated [CO2] also appeared to
increase the gas-phase CH4 at panicle formation.
The mixing ratio of CH4 in trapped bubbles was well
approximated by a bounded function using the volume of
trapped bubbles as the explanatory variable across the three
growth stages (Fig. 2). At panicle formation, the mixing ratio of
CH4 was relatively low, but within that range of values a higher
mixing ratio of CH4 was associated with a linear increase in gas
volume. Results from the heading and grain filling stages also
showed an increasing bubble volume with a higher mixing
ratio, but the relative increase in volume was less at these
higher mixing ratios.
120
100
4
80
3
60
2
40
1
PF
HD
GF
20
0
Bubble volume (mL pot–1)
Volumetric gas content (y, %)
140
R2 = 0.88
5
0
0
20
40
60
Mixing ratio of CH4 (x, %)
Flux of CH4 into the atmosphere
At panicle formation and heading, the CH4 concentration in the
flux-measurement chamber showed a linear build-up with time
in most measurements, both during the day and at night (Table
3). However, at grain filling, only about half the samples met
the criteria for non-bubbling emissions. The flux results
presented hereafter refer only to non-bubbling measurements
a: negative flux at any sampling
interval or erratic CO2 flux
90
PF-day
80
PF-night
70
HD-day
60
HD-night
50
GF-day
GF-night
40
30
20
10
Fig. 2 Relationship between the mixing ratio of CH4 in soil gas bubbles
and the volume of gas bubbles expressed either as volumetric gas
content (left y axis) or bubble volume per pot (right y axis). PF =
measurements at panicle formation; HD = measurements at heading;
GF = measurements at grain filling.
Table 3 Number of CH4 concentration
measurements that could be
categorized as non-bubbling,
influenced by bubbling, or flawed.
Correlation between explanatory variables and the CH 4 flux
and CH4 pool
Methane flux (mg C m–2 h–1)
y = –4.85 exp(–0.0701x) + 5.39
6
unless otherwise noted.
The absolute emission rate and its response to elevated [CO2]
and soil temperature in this experiment were similar to those
observed from rice hills without pots (Tokida et al. 2010). The
effect of FACE on CH4 flux was not statistically significant in
the current study, whereas elevated temperature significantly
increased the CH4 flux at panicle formation (+84% averaged
over the four treatment plots) and grain filling stages (+99%)
(Table 2), but not at heading.
For all of the measurements combined (three growth stages and
daytime and nighttime), temperature exhibited the highest
correlation with CH4 flux (r = 0.60, P < 0.001, Fig. 3), followed
by trapped-bubble volume (r = 0.51, P < 0.001, Table 4).
160
7
0
20
22
24
26
28
30
Soil temperature at 0 cm depth ( C)
Fig. 3 Relationship between daytime (day) and nighttime (night) CH4
flux and soil temperature (0 cm). A covariance analysis (soil
temperature as covariate) indicated that daytime CH4 flux was
significantly higher than the nighttime flux at the heading stage (P <
0.001) and marginally significantly higher at the grain filling stage (P
= 0.08). PF = measurements at panicle formation; HD = measurements
at heading; GF = measurements at grain filling.
Examining each growth stage separately, at the panicle
formation and heading stages the mass of CH4 in the form of
bubbles (“Bubble-CH4” in Table 4) produced the highest
Pearson’s correlation coefficient of all possible variables both
Category
Non-bubbling
Bubbling
Flawed with
other artificial
errorsa
7
Panicle formation
Day
Night
34
29
2
0
–
7
Stage
Heading
Day
Night
30
30
5
4
1
2
Grain filling
Day
Night
16
18
20
15
–
3
This is a self-archiving file for Tokida et al. 2012 published in Plant and Soil, DOI: 10.1007/s11104-012-1356-7. The final
publication is available at http://www.springerlink.com/content/x508n4701m5l1215/?MUD=MP.
8
Table 4 Pearson’s correlation coefficient between CH4 flux and potential explanatory variables at different stages of rice crop development
Stage
Panicle formation
Variables
Day
Temp
0.49**
Vb
Night
All data
Heading
Grain filling
Day
Night
Day
Night
0.73***
0.28
0.23
0.63**
0.26
0.60***
0.86***
0.68***
0.47**
0.44*
0.46†
0.62**
0.51***
Mb
0.69***
0.35†
0.47**
0.52**
0.53*
0.43†
0.38***
Bubble-CH4
0.90***
0.83***
0.64***
0.59***
0.62*
0.50*
0.35***
AGB
0.57***
0.35†
0.27
0.17
0.30
0.03
0.29***
RB
0.12
–0.01
0.30
0.23
–0.20
–0.40
Till
0.01
0.01
0.31†
0.23
0.34
–0.39
CO2
–
0.81***
–
0.27
–
–0.14
0.16*
–0.06
–
Gas bubbles as a major pool of CH4 in paddy soil
In our results, CH4 in the gas phase accounted for a significant
fraction (26–45%) of the total soil pool of CH4 at the panicle
formation stage and came to dominate the inventory at the
heading and grain filling stages (Table 2). Clearly, the size of
the gas-phase CH4 pool was larger than that of the dissolved
form. These results showed a sharp contrast to the conventional
wisdom that CH4 occurs in dissolved, not gaseous, form in rice
paddy soil (e.g. Bossio et al. 1990).
We estimated the ratio of gaseous CH4 to the total (gas +
solution) inventory as a function of the mixing ratio of CH4 in
the gas phase at 25°C (Fig. 4), using the relationship shown in
Fig. 2 and Eq. (1). Our calculations suggest that even if the
mixing ratio of CH4 is as low as 4% (with a corresponding gas
content of only 1.7%), >40% of CH4 occurs in the form of gas
bubbles. As the mixing ratio increases, the fraction in the gas
phase also increases progressively, but the amount of trapped
gas plateaus at a volumetric gas content of ~5% at a CH4
mixing ratio of ~40%, and the fraction of gaseous CH4
inventory correspondingly plateaus at ~68% (Fig. 4).
40
3
30
2
Fraction in gas phase
20
Volumetric gas content
Volumetric gas content (%)
DISCUSSION
Fraction of CH4 in gase phase to total (%)
†,daytime
P < 0.10;and
*, Pnighttime
< 0.05; **,fluxes.
P < 0.01;
P <filling,
0.001 the mass of
for
At***,
grain
Temp: soil temperature (at 0 cm depth), Vb: bubble volume per pot as volumetric gas content (m3 m–3), Mb: mixing ratio of CH4 in bubbles,
CH4 in the form of bubbles produced a significant correlation
Bubble-CH4: mass of CH4 in the form of bubbles, AGB: above ground biomass,
80 RB: root biomass, Till: tiller number, CO 2: CO2 efflux (dark
6
with
both ofdaytime
respiration
rice plant).and nighttime CH4 flux, whereas
temperature exhibited a high correlation with the daytime flux.
70
5
The volume of gas bubbles (Vb) showed the best correlation for
nighttime measurements. In most cases, rice growth parameters
60
did not have a significant correlation with CH4 flux except for
4
50
aboveground biomass at panicle formation (Table 4).
1
10
0
0
0
10
20
30
40
50
60
Mixing ratio of CH4 in gas phase (%)
Fig. 4 Fraction of CH4 in gas-form to the total (gas form + solution
form) inventory as a function of the mixing ratio of CH4 in the gas
phase at 25°C. The relationship shown in Fig. 2 and Eq.1 was used for
computation of these curves.
How does the gas pool size affect the rate of CH4 emission?
The results of the present study clearly demonstrate a close
relationship between the size of the gas pool and the flux of
CH4 in rice fields (Table 4). Enhanced CH4 emissions in the
warming treatment at the panicle formation and grain filling
stages accompanied a larger CH4 pool in bubble form (Table 2),
indicating a consistent relationship between the gas pool and
CH4 flux under different temperature regimes.
This is a self-archiving file for Tokida et al. 2012 published in Plant and Soil, DOI: 10.1007/s11104-012-1356-7. The final
publication is available at http://www.springerlink.com/content/x508n4701m5l1215/?MUD=MP.
Because we omitted bubbling emissions from the flux
measurements, the size of the CH4 pool in entrapped bubbles
influenced the flux measurements mainly through
plant-mediated CH4 emission (Nouchi et al. 1990; Wang et al.
1997), which is driven by molecular diffusion (Denier Van Der
Gon and Van Breemen 1993). Because diffusion is controlled
by a difference in concentration gradient, not by pool size, the
CH4 mixing ratio (Mb in Table 4) ought to be the bubble-related
parameter most closely related to CH4 flux. However, the
volume of bubbles (Vb) had a similar, or in most cases better,
correlation with CH4 flux than the CH4 mixing ratio.
The volume of bubbles can affect the rate of plant-mediated
CH4 emission by enhancing the diffusive (passive) uptake of
CH4 by the rice root. When solution-phase CH4 comes in
contact with rice roots, a boundary layer exists in the soil in the
vicinity of the root surface where CH4 transport is limited by
the diffusion of the gas in the soil water. A mechanistic
diffusion model would give us clear exposition in this regard;
the diffusion of CH4 within the soil is by far the slowest process
in the soil–plant system if the soil is saturated with water (Van
Bodegom et al. 2001). The CH4-rich bubbles in contact with the
roots would allow for much faster CH4 movement into the roots
because the coefficient of diffusion is about four orders of
magnitude greater for gases that are in the gas phase compared
to that in the dissolved state (Himmelblau 1964). The greater
the bubble volume, the larger would be the area of direct
contact between the roots and the bubbles, leading to a lower
resistance for CH4 transport. These interpretations are
consistent with previous findings that the removal of gas
bubbles by brief evacuation resulted in an immediate reduction
of the CH4 emission rate, indicating enhanced plant-mediated
transport in the presence of bubble reservoirs
(Holzapfel-Pschorn et al. 1986).
Although our results indicate that the gaseous CH4 pool plays
an important role in controlling CH4 emission, considerable
unexplained variation in the CH4 flux remains. The largest
variation is that between the growth stages of rice; the
bubble-borne CH4 pool at grain filling was more than double
that at heading, but the flux did not increase proportionally
(Table 2). The accumulation of CH4-containing bubbles (and of
CH4 dissolved in the soil water) appears not to have contributed
to commensurately larger CH4 emission at grain filling; the
CH4 transport capacity of rice at this stage might have been
lower due to senescence (Nouchi et al. 1994). Cheng et al.
(2008b) observed a positive relationship between CH4 flux and
CH4 concentration in soil solution before heading, but
afterwards the CH4 emission decreased with increased CH4
concentration. The results of both studies strongly indicate a
need to understand the change in CH4 transport capacity with
rice growth and senescence, because the plant-mediated release
may be limited by transport capacity rather than by pool size in
the soil in the later growth stages. The absence of a stimulatory
effect of soil warming on CH4 emissions at heading (Table 2)
may also be linked to rice phenology, as elevated temperature
accelerated the day of heading by 4 days (Tokida et al. 2010).
Another large source of unexplained variation is the
9
difference between day and night CH4 flux (Table 4). Several
studies have shown that the diurnal variation in CH4 flux is
associated
with
a
change
in
soil
temperature
(Holzapfel-Pschorn and Seiler 1986; Sass et al. 1991; Schütz et
al. 1989; Wang et al. 1999). However, covariance analysis with
temperature as the covariate suggested that CH4 fluxes from
daytime measurements were significantly higher than those
from nighttime at the heading stage (P < 0.001) and marginally
significantly higher at the grain filling stage (P = 0.08) even at
the same temperature (Fig. 3).
We speculate that the bubble volume might increase during
daylight hours, which in turn increases the daytime CH 4
emission, though it was not possible to directly quantify the
diurnal change in bubble volume in the present study.
Theoretically, a rise in temperature directly leads to a greater
bubble volume by gas expansion (Charles's law) and also by
degassing from the aqueous to the gas phase (due to smaller
solubility), with the latter making the greater contribution
(Tokida et al. 2009). Consequently, the warming temperature
phase (i.e., during daylight hours) would bring about a greater
volume and larger emissions. On the other hand, the subsequent
cooling phase (nighttime) would result in smaller volume and
flux even at the same temperature as a result of hysteresis; the
greater CH4 emission during the ascending temperature trend
might result in smaller pool size of CH4 during the descending
trend. Additionally or alternatively, bubble-induced mass flow
might contribute to the diurnal fluctuation in CH4 flux. Hosono
and Nouchi (1997) observed that entrapped gas bubbles formed
in direct contact with the base of the stem of rice plants at a
shallow depth in the soil (e.g., 1 cm). Their laboratory
experiment further suggested that a small increase in gas
pressure (1 kPa, equivalent to ~10 cm head of H2O) around the
base of the stem can cause a three-fold increase in CH4
emission through the rice plant, indicating the presence of
convective rather than diffusive flow through the soil–plant
system.
Implications for ebullition and modeling
We did not investigate bubbling CH 4 release (ebullition) from
the paddy soil in this study, but the relationship between bubble
volume and the mixing ratio of CH4 in Fig. 2 indicates the
presence of a “threshold volume” beyond which gas bubbles
escape into the atmosphere as the soil–root matrix cannot hold
them any longer (Fig. 2). The greater frequency of non-linear
CH4 accumulation in the chamber during flux measurements at
grain filling also highlighted the potential importance of
ebullition after the heading stage (Table 3).
Our results provide some insights for models of CH 4
emission from rice paddies. Most existing models do not
account for the bubble-borne CH4 pool in soil; in most cases
they assume either (i) that there is no CH4 pool in the soil as a
result of instantaneous CH4 emission from net CH4 production
(production–consumption) (Cao et al. 1995; Sass et al. 2000),
or (ii) that soil CH4 exists only in the dissolved state (Fumoto et
al. 2007). Some models simulate CH4 release via bubbling, the
This is a self-archiving file for Tokida et al. 2012 published in Plant and Soil, DOI: 10.1007/s11104-012-1356-7. The final
publication is available at http://www.springerlink.com/content/x508n4701m5l1215/?MUD=MP.
rate of which is determined by the rate of CH4 production in
combination with some thresholds above which the produced
CH4 is emitted instantaneously to the atmosphere (Huang et al.
2004; Xu et al. 2007).
Omission of the bubble-borne CH4 pool might be a
reasonable simplification, but would limit the model's
suitability under several situations when bubbling release is
important, such as release associated with seasonal (Bosse and
Frenzel 1998; Wassmann et al. 1996) and diurnal variation
(Byrnes et al. 1995; Denier Van Der Gon and Neue 1995) and
drainage events (Denier Van Der Gon et al. 1996; Han et al.
2005; Watanabe et al. 1994). As indicated in the present study,
the amount of gaseous CH4 in the soil may also affect the rate of
CH4 emission through rice plants. Although the relationship
found in this study (Fig. 2 and 3) is still empirical, we suggest
that its utilization in existing CH4-emission models may be a
simple method of explicitly incorporating the bubble-borne
CH4 pool in soil without violating mass conservation
constraints.
REFERENCES
[1]
[2]
[3]
[4]
[5]
[6]
[7]
[8]
[9]
[10]
CONCLUSIONS
The results obtained in this study clearly show that entrapped
bubbles represent a major CH4 inventory, even in soil that is
regarded as water-saturated. The gaseous CH4 pool showed a
good correlation with rice-mediated emissions obtained at each
growth stage across both the ambient and elevated [CO2] (+200
μmol mol–1) and warming (+2°C) treatments. However, the
pool size alone could not explain the variation across different
rice growth stages, indicating that the transport capacity of rice
plants can also limit the rate of plant-mediated emissions. Our
hypothesis based on the present results is that a greater bubble
volume may lead to faster CH4 transfer from the soil to the roots
because gas diffusion is about four orders of magnitude greater
in the gas phase than in the liquid phase. We propose that
incorporation of the relationship between the CH4 mixing ratio
(which can be estimated from the dissolved CH4 concentration)
and the bubble volume into existing CH4-emission models may
be a simple approach if the models need to explicitly define the
bubble-borne CH4 pool and its relation to emissions.
[11]
[12]
[13]
[14]
[15]
[16]
[17]
[18]
ACKNOWLEDGMENT
We thank Mr. H. Iino and Mr. H. Kamimura of the Field
Management Division of the National Institute for
Agro-Environmental Sciences (NIAES) for technical
assistance with pot preparation. We also acknowledge Ms. M.
Kajiura and Dr. N. Katayanagi of NIAES and Dr. M.
Matsushima of Chiba University for help with flux
measurements and Drs. S. Sudo and K. Minamikawa of NIAES
for assistance with the GC analysis. This research was
financially supported by the Global Environment Research
Program, Ministry of the Environment, Japan, and a
Grant-in-Aid for Scientific Research (PD 19-7010) from the
Japan Society for the Promotion of Science.
10
[19]
[20]
[21]
[22]
[23]
[24]
Armstrong J, Armstrong W (2001) Rice and Phragmites: Effects of
organic acids on growth, root permeability, and radial oxygen loss to the
rhizosphere. Am J Bot 88:1359–1370
Bazhin N (2010) Theory of methane emission from wetlands. Energy
Environ Sci 3:1057–1072
Becker M, Asch F (2005) Iron toxicity in rice—conditions and
management concepts. J Plant Nutr Soil Sci 168:558–573
Bosse U, Frenzel P (1998) Methane emissions from rice microcosms: The
balance of production, accumulation and oxidation. Biogeochemistry
41:199–214
Buendia LV, Neue HU, Wassmann R et al (1998) An efficient sampling
strategy for estimating methane emission from rice field. Chemosphere
36:395–407
Bossio DA, Horwath WR, Mutters RG, van Kessel C (1999) Methane
pool and flux dynamics in a rice field following straw incorporation. Soil
Biol Biochem 31: 1313–1322
Byrnes BH, Austin ER, Tays BK (1995) Methane emissions from flooded
rice soils and plants under controlled conditions. Soil Biol Biochem
27:331–339
Cao M, Dent J, Heal O (1995) Modeling methane emissions from rice
paddies. Global Biogeochem Cycles 9:183–195
Cheng W, Inubushi K, Hoque MM et al (2008a) Effect of elevated [CO2]
on soil bubble and CH4 emission from a rice paddy: A test by 13C
pulse-labeling under free-air CO2 enrichment. Geomicrobiol J
25:396–403
Cheng W, Sakai H, Hartley AE, Yagi K, Hasegawa T (2008b) Increased
night temperature reduces the stimulatory effect of elevated carbon
dioxide concentration on methane emission from rice paddy soil. Global
Change Biol 14:644–656
Cheng W, Yagi K, Xu H, Sakai H, Kobayashi K (2005) Influence of
elevated concentrations of atmospheric CO2 on CH4 and CO2 entrapped in
rice-paddy soil. Chem Geol 218:15–24
Clever HL, Young CL (1987) IUPAC solubility data series, vol27/28,
methane. Pergamon, Oxford, UK.
Denier Van Der Gon HAC, Neue HU (1995) Influence of organic-matter
incorporation on the methane emission from a wetland rice field. Global
Biogeochem Cycles 9:11–22
Denier Van Der Gon HAC, Van Breemen N (1993) Diffusion-controlled
transport of methane from soil to atmosphere as mediated by rice plants.
Biogeochemistry 21:177–190
Denier Van Der Gon HAC, Van Breemen N, Neue HU et al (1996)
Release of entrapped methane from wetland rice fields upon soil drying.
Global Biogeochem Cycles 10:1–7
Forster P, Ramaswamy V, Artaxo P et al (2007) Changes in atmospheric
constituents and in radiative forcing. In Solomon S, Qin D, Manning M et
al (eds). Climate change 2007: The physical science basis, contribution of
working group I to the fourth assessment report of the intergovernmental
panel on climate change. pp 129–234. Cambridge University Press,
Cambridge, United Kingdom and New York, NY, USA.
Fumoto T, Kobayashi K, Li C, Yagi K, Hasegawa T (2007) Revising a
process-based biogeochemistry model (DNDC) to simulate methane
emission from rice paddy fields under various residue management and
fertilizer regimes. Global Change Biol 14:382–402
Gomez KA, Gomez AA (1984) Statistical procedures for agricultural
research. John Wiley & Sons, New York.
Han GH, Yoshikoshi H, Nagai H et al (2005) Concentration and carbon
isotope profiles of CH4 in paddy rice canopy: Isotopic evidence for
changes in CH4 emission pathways upon drainage. Chem Geol 218:25–40
Hansen J, Sato M, Ruedy R et al (2005) Efficacy of climate forcings. J
Geophys Res 110:D18104
Himmelblau DM (1964) Diffusion of dissolved gases in liquids. Chem
Rev 64:527–550
Holzapfel-Pschorn A, Conrad R, Seiler W (1986) Effects of vegetation on
the emission of methane from submerged paddy soil. Plant Soil
92:223–233
Holzapfel-Pschorn A, Seiler W (1986) Methane emission during a
cultivation period from an italian rice paddy. J Geophys Res
91:11803–11814
Hosono T, Nouchi I (1997) Effect of gas pressure in the root and stem
base zone on methane transport through rice bodies. Plant Soil 195:65–87
This is a self-archiving file for Tokida et al. 2012 published in Plant and Soil, DOI: 10.1007/s11104-012-1356-7. The final
publication is available at http://www.springerlink.com/content/x508n4701m5l1215/?MUD=MP.
[25] Huang Y, Zhang W, Zheng X, Li J, Yu Y (2004) Modeling methane
emission from rice paddies with various agricultural practices. J Geophys
Res 109:D08113
[26] Hutchinson GL, Livingston GP (2002) Soil-atmosphere gas exchange. In
Dane JH and Topp C (eds). Method of soil analysis part 4 physical
method. pp 1159–1182. Soil Science Society of America, Inc., Madison.
[27] Littell RC, Milliken GA, Stroup WW, Wolfinger RD, Schabenberber O
(2006) Sas® for mixed models, Cary, NC.
[28] Maeda T, Soma K (1986) Physical properties. In Wada K (eds). Ando
soils in Japan. pp 99–114. Kyushu University Press, Fukuoka, Japan.
[29] Nouchi I, Hosono T, Aoki K, Minami K (1994) Seasonal variation in
methane flux from rice paddies associated with methane concentration in
soil water, rice biomass and temperature, and its modeling. Plant Soil
161:195–208
[30] Nouchi I, Mariko S, Aoki K (1990) Mechanism of methane transport
from the rhizosphere to the atmosphere through rice plants. Plant Physiol
94:59–66
[31] Okada M, Lieffering M, Nakamura H et al (2001) Free-air CO2
enrichment (FACE) using pure CO2 injection: System description. New
Phytol 150:251–260
[32] Ramaswamy V, Boucher O, Haigh J et al (2001) Radiative forcing of
climate change. In Houghton JT, Ding Y, Griggs DJ et al (eds). Climate
change 2001: The scientific basis contribution of working group i to the
third assessment report of the intergovernmental panel on climate change.
pp 349–416. Cambridge University Press, Cambridge, United Kingdom
and New York, NY, USA.
[33] Rothfuss F, Conrad R (1998) Effect of gas bubbles on the diffusive flux of
methane in anoxic paddy soil. Limnol Oceanogr 43:1511–1518
[34] Sass RL, Fisher FM, Harcombe PA, Turner FT (1990) Methane
production and emission in a texas rice field. Global Biogeochem Cycles
4:47–68
[35] Sass RL, Fisher FM, Jr., Huang Y (2000) A process-based model for
methane emissions from irrigated rice fields: Experimental basis and
assumptions. Nutr Cycl Agroecosys 58:249–258
[36] Sass RL, Fisher FM, Turner FT, Jund MF (1991) Methane emission from
rice fields as influenced by solar radiation, temperature, and straw
incorporation. Global Biogeochem Cycles 5:335–350
[37] Schütz H, Holzapfel-Pschorn A, Conrad R, Rennenberg H, Seiler W
(1989) A 3-year continuous record on the influence of daytime, season,
and fertilizer treatment on methane emission rates from an italian rice
paddy. J Geophys Res 94:16405–16416
[38] Schimel D, Alves D, Enting I et al (1995) Radiative forcing of climate
change. In Houghton JT, Meira Filho LG, Callander BA et al (eds).
Climate change 1995: The science of climate change, contribution of WG
I to the second assessment report of the intergovernmental panel on
climate change. pp 65–132. Cambridge University Press, Cambridge,
United Kingdom and New York, NY, USA.
[39] Schink B (1997) Energetics of syntrophic cooperation in methanogenic
degradation. Microbiol Mol Biol Rev 61:262–280
[40] Shindell D, Kuylenstierna JCI, Vignati E et al (2012) Simultaneously
mitigating near-term climate change and improving human health and
food security. Science 335:183–189
[41] Shindell DT, Faluvegi G, Bell N, Schmidt GA (2005) An
emissions-based view of climate forcing by methane and tropospheric
ozone. Geophys Res Lett 32:L04803
[42] Shindell DT, Faluvegi G, Koch DM et al (2009) Improved attribution of
climate forcing to emissions. Science 326:716–718
[43] Shine KP, Derwent RG, Wuebbles DJ, Morcrette J-J (1990) Radiative
forcing of climate change. In Houghton JT, Jenkins GJ and Ephraums JJ
(eds). Climate change: The IPCC scientific assessment. pp 41–68.
Cambridge University Press, Cambridge, United Kingdom and New
York, NY, USA.
[44] Stams AJM (1994) Metabolic interactions between anaerobic-bacteria in
methanogenic environments. Antonie Van Leeuwenhoek 66:271–294
[45] Sudo S (2006) Method and instrument for measuring atmospheric gas,
patent publication number 2006-275844. National Institute for
Agro-Environmental Sciences, Japan.
[46] Tokida T, Adachi M, Cheng W et al (2011) Methane and soil CO2
production from current-season photosynthates in a rice paddy exposed to
elevated CO2 concentration and soil temperature. Global Change Biol
17:3327–3337
[47] Tokida T, Fumoto T, Cheng W et al (2010) Effects of free-air CO2
enrichment (FACE) and soil warming on CH4 emission from a rice paddy
[48]
[49]
[50]
[51]
[52]
[53]
[54]
[55]
[56]
[57]
[58]
[59]
[60]
11
field: Impact assessment and stoichiometric evaluation. Biogeosciences
7:2639–2653
Tokida T, Miyazaki T, Mizoguchi M (2009) Physical controls on
ebullition losses of methane from peatlands. In Baird A, Belyea L, Comas
X, Reeve A and Slater L (eds). Northern peatlands and carbon cycling.
American Geophysical Union, Washington, DC., USA.
Tokida T, Miyazaki T, Mizoguchi M et al (2007) Falling atmospheric
pressure as a trigger for methane ebullition from peatland. Global
Biogeochem Cycles 21:GB2003
Tokida T, Miyazaki T, Mizoguchi M, Seki K (2005) In situ accumulation
of methane bubbles in a natural wetland soil. Eur J Soil Sci 56:389–395
Uzaki M, Mizutani H, Wada E (1991) Carbon isotope composition of CH4
from rice paddies in Japan. Biogeochemistry 13:159–175
Van Bodegom PM, Groot T, Van Den Hout B, Leffelaar PA, Goudriaan J
(2001) Diffusive gas transport through flooded rice systems. J Geophys
Res 106:20861–20873
Wang B, Neue HU, Samonte HP (1997) Role of rice in mediating
methane emission. Plant Soil 189:107–115
Wang B, Neue HU, Samonte HP (1999) Factors controlling diel patterns
of methane emission via rice. Nutr Cycl Agroecosys 53:229–235
Wassmann R, Neue HU, Alberto MCR et al (1996) Fluxes and pools of
methane in wetland rice soil with varying organic inputs. Environ Monit
Assess 42:163–173
Watanabe A, Kimura M (1995) Methane production and its fate in paddy
fields. VIII. Seasonal variation of methane retained in soil. Soil Sci Plant
Nutr 41:225–233
Watanabe A, Kimura M (1998) Factors affecting variation in CH4
emission from paddy soils grown with different rice cultivars: A pot
experiment. J Geophys Res 103:18947–18952
Watanabe A, Murase J, Katoh K, Kimura M (1994) Methane production
and its fate in paddy fields. V. Fate of methane remaining in paddy soil at
harvesting stage. Soil Sci Plant Nutr 40:221–230
Wilhelm E, Battino R, Wilcock RJ (1977) Low-pressure solubility of
gases in liquid water. Chem Rev 52:219–262
Xu S, Jaffé PR, Mauzerall DL (2007) A process-based model for methane
emission from flooded rice paddy systems. Ecol Model 205:475–491G.
O. Young, “Synthetic structure of industrial plastics (Book style with
paper title and editor),” in Plastics, 2nd ed. vol. 3, J. Peters, Ed. New
York: McGraw-Hill, 1964, pp. 15–64.