Global Change Biology (2008) 14, 644–656, doi: 10.1111/j.1365-2486.2007.01532.x
Increased night temperature reduces the stimulatory
effect of elevated carbon dioxide concentration on
methane emission from rice paddy soil
W E I G U O C H E N G *, H I D E M I T S U S A K A I *, A N N E H A R T L E Y w, K A Z U Y U K I Y A G I * and
T O S H I H I R O H A S E G AWA *
*Agro-Meterology Division, National Institute for Agro-Environmental Sciences, Kannondai 3-1-3, Tsukuba, Ibaraki, 305-8604
Japan, wDepartment of Marine and Ecological Sciences, Florida Gulf Coast University, 10501 FGCU Boulevard South, Fort Myers,
FL 33965, USA
Abstract
To determine how elevated night temperature interacts with carbon dioxide concentration ([CO2]) to affect methane (CH4) emission from rice paddy soil, we conducted a pot
experiment using four controlled-environment chambers and imposed a combination of
two [CO2] levels (ambient: 380 ppm; elevated: 680 ppm) and two night temperatures
(22 and 32 1C). The day temperature was maintained at 32 1C. Rice (cv. IR72) plants were
grown outside until the early-reproductive growth stage and then transferred to the
chambers. After onset of the treatment, day and night CH4 fluxes were measured every
week. The CH4 fluxes changed significantly with the growth stage, with the largest fluxes
occurring around the heading stage in all treatments. The total CH4 emission during the
treatment period was significantly increased by both elevated [CO2] (P 5 0.03) and
elevated night temperature (Po0.01). Elevated [CO2] increased CH4 emission by 3.5%
and 32.2% under high and low night temperature conditions, respectively. Elevated [CO2]
increased the net dry weight of rice plants by 12.7% and 38.4% under high and low night
temperature conditions, respectively. These results imply that increasing night temperature reduces the stimulatory effect of elevated [CO2] on both CH4 emission and rice
growth. The CH4 emission during the day was larger than at night even under the highnight-temperature treatment (i.e. a constant temperature all day). This difference became
larger after the heading stage. We observed significant correlations between the night
respiration and daily CH4 flux (Po0.01). These results suggest that net plant photosynthesis contributes greatly to CH4 emission and that increasing night temperature
reduces the stimulatory effect of elevated [CO2] on CH4 emission from rice paddy soil.
Keywords: conductance, elevated carbon dioxide concentration, interaction, methane, night respiration, night temperature, rice, soil solution, solar radiation
Received 8 June 2007; revised version received 25 September 2007 and accepted 12 October 2007
Introduction
Anthropogenic emissions of key atmospheric trace
gases that absorb infrared radiation, such as carbon
dioxide (CO2) and methane (CH4), will likely lead to
an increase in global mean surface temperature, with
the potential to bring about climate changes. Depending
on various population growth and energy-use scenarios, atmospheric carbon dioxide concentration ([CO2]) is
expected to rise from 379 ppm currently to between 485
Correspondence: Weiguo Cheng, tel. 1 81 29 838 8205, fax 1 81 29
838 8211, e-mail: [email protected]
644
and 1000 ppm by 2100. After CO2, CH4 is the most
important greenhouse gas, responsible for approximately 20% of the anthropogenic global warming effect
[Intergovernmental Panel on Climate Change (IPCC),
2001]. During the industrial era, the concentration of
atmospheric CH4 increased at about 1% per year,
but the rate of increase has declined since the 1990s
(Dlugokencky et al., 2003). However, recent studies
have suggested that the decline in human-induced
CH4 emissions in the 1990s was only transitory, and
atmospheric CH4 might rise again (Bousquet et al., 2006;
Lelieveld, 2006). Furthermore, the enhanced greenhouse effects of CO2, CH4, and other greenhouse gases
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are predicted to cause an average global warming of
1.1–6.4 1C by 2100 (IPCC, 2007). Of the major sources of
CH4, natural wetlands and rice paddies are the largest,
together accounting for 34% of the total flux of CH4 to
the atmosphere (Bousquet et al., 2006).
In submerged rice paddies, CH4 is an end product of
the anaerobic decomposition of organic matter, mostly
by acetate fermentation and CO2 reduction (Takai,
1970). The sources of organic matter in flooded rice
paddy soil are from older matter (e.g. native soil organic
matter, incorporated organic material such as straw and
manure) and new matter from plant growth (e.g. root
exudates and plant debris; Yagi & Minami, 1990; Minoda et al., 1996). In addition, plant-mediated transport is
a very important pathway for CH4 emission from
cultivated rice soil (Inubushi et al., 1989; Schutz et al.,
1989; Nouchi et al., 1990; Wassmann et al., 1996).
Elevated [CO2] increases rice biomass (above- and
belowground) production and grain yield (Baker &
Allen, 1993; Ziska et al., 1997; Kim et al., 2003; Baker,
2004; Sakai et al., 2006; Yang et al., 2006). Many studies
have also demonstrated a positive effect of elevated
[CO2] on CH4 emission from rice paddies (Ziska et al.,
1998; Allen et al., 2003; Inubushi et al., 2003; Cheng et al.,
2006; Zheng et al., 2006). One mechanism by which CH4
emission increases under elevated [CO2] is that increased tiller number results in a greater CH4 conductance through the rice plant. This mechanism represents
an indirect effect of elevated [CO2] at the early stages of
rice growth. The other mechanism is that elevated [CO2]
increases soil microbial carbon and accelerates the turnover rate of soil organic carbon during the middle and
later parts of the rice growth season (Cheng et al., 2001,
2005; Hoque et al., 2001), which serves as a source of
CH4 production. However, it remains unclear how
much each mechanism contributes to the enhancement
of CH4 under elevated [CO2].
CH4 emissions are also highly sensitive to temperature. On the microbial level, methanogenesis is optimum between 30 and 40 1C. High soil temperatures
enhance CH4 production by increasing methanogen
populations as well as the activity of other bacteria that
mediate methanogenic fermentation. The latter seem to
be more sensitive than methanogens to temperature
variations (Le Mer & Roger, 2001). Ziska et al. (1998)
measured CH4 emission using open-top chambers under elevated [CO2] and temperatures in a paddy field in
the tropics of the Philippines and showed that CH4
emission was increased by elevated [CO2] (300 mL L1
above ambient) and decreased by elevated air temperature (1 4 1C above ambient). In their experiment, the soil
temperature was increased only marginally (o0.5 1C)
and the biomass production decreased due to the
elevated air temperature (Ziska et al., 1998). In contrast,
645
Allen et al. (2003) showed that the total seasonal CH4
emission was fourfold greater under high [CO2]
(660 mL L1) and high temperature (38/29 1C for day/
night) than under the low [CO2] (330 mL L1) and low
temperature (32/23 1C for day/night), probably due to
more root sloughing or exudates. The discrepancy
between these studies may be partly due to different
experimental conditions, including different soil types
and environmental modifications.
There are still uncertainties in the predictions of
global temperature, but for the past 100 years, the daily
minimum (i.e. night) temperature increased at a faster
rate than daily maximum (daytime) temperature in
association with a steady increase in atmospheric greenhouse gas concentrations (Kukla & Karl, 1993; Easterling et al., 1997). Correlation analyses showed that
grain yield and aboveground biomass declined with
increasing night temperature in Los Baños, the Philippines, from 1979 to 2003 (Peng et al., 2004). However,
neither the effect of night-time temperature alone on
CH4 emission nor its combined effect with elevated
[CO2] have been tested experimentally.
To estimate accurately the feedback effect of global
warming and elevated [CO2] on CH4 emissions from
the paddy field, we need to understand the combined
effects of these two parameters on CH4 emission from
flooded rice soil. We were also interested in testing
whether elevated [CO2] stimulates CH4 emission without an apparent increase in tiller number. In this study,
we grew rice under two [CO2] and two night air
temperature conditions during the plant’s reproductive
stage using four controlled-environment chambers. Our
objective was to determine how CH4 emission responds
to increased [CO2] and night temperature as well as
their interaction.
Materials and methods
Experimental schedule, cultural practice, rice cultivar,
and soil
This research was conducted at the National Institute
for Agro-Environmental Sciences, Tsukuba, Japan
(36101 0 N, 140107 0 E). We used a semidwarf indica-type
rice cultivar, IR72, which is grown widely in south-east
Asia (Peng et al., 1999). On 5 June 2006, germinated seed
were sown in a seedling tray (three seeds per cell). At 3
weeks after sowing, the seedlings were transplanted to
15 plastic pots (19.5 cm inside diameter, 27 cm height,
0.2 cm thickness) filled with grey sand soil that was
collected from the plough layer (15 cm of the top
layer) of a rice field in Kujukuri, Chiba Prefecture,
Japan. The soil contained 8.1 g kg1 organic carbon
and 0.9 g kg1 total nitrogen, and average soil pH was
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646 W . C H E N G et al.
Stages of rice growth:
Air temp. (°C)
Vegetative growth
Reproductive growth
Before treatment
After treatment
(grown in outdoor water tank)
(grown in chambers)
(Air temp. varied for one day)
High night
temp. (32 °C)
Low night
temp. (22 °C)
30
25
20
0 4 8 12 16 20 24
Day
26-Jun
10-Jul
24-Jul
14
28
7-Aug 21-Aug
4-Sep
18-Sep
Local time (h)
2-Oct
16-Oct
98
112
0
0
Flooding of moist soil;
basic fertilization;
transplanting
42
56
70
84
Days after transplanting
Additional
fertilization
Harvest for highand low-nighttemp. treatments,
respectively
Fig. 1 Experimental schedule and changes in daily average air temperature (before treatment) for rice plants grown in an outdoor
water tank, and daily air temperature variation (after treatment) for rice plants grown in controlled-environment chambers.
6.3. Before rice transplanting, 9.0 kg (7.4 kg dry soil
equivalent) of soil was mixed with 1.53 g NH4Cl and
0.87 g KH2PO4 and was used to fill each pot. The
amounts of nitrogen, phosphorus, and potassium of
the basal fertilizers were 0.40, 0.20, and 0.25 g pot1,
respectively. At 35 and 49 days after transplanting
(DAT), we top-dressed with 0.62 g N, 0.10 g P, and
0.13 g K pot1. The flooding water was maintained at
about 5 cm depth throughout the cultivation period.
We grew the plants outside during the vegetative
growth period. Meteorological data, including daily
temperature and solar radiation, were from the Weather
Data Acquisition System of the National Institute for
Agro-Environmental Sciences. We started the [CO2]
and night-temperature treatments around the panicleformation stage at 59 DAT, when we randomly assigned
three pots to each of the four controlled-environment
chambers and used the remaining three pots for
destructive sampling (Fig. 1). We terminated our highand low-night-temperature treatments for both [CO2]
conditions at 107 and 114 DAT, respectively, depending
on the physiological maturity, at which time we
sampled plants to determine dry weights of each organ
for all the plants used in the experiment.
Experimental design for treatments and controlledenvironment chambers
We performed the [CO2] and night-temperature treatments only during the reproductive growth stage in this
experiment, because the tiller number had already been
determined at this stage, which allowed us to limit
indirect effects on CH4 emission due to differences in
tiller number. We used four controlled-environment
chambers (Shimadzu, Kyoto, Japan) for this experiment
and imposed a combination of two levels of [CO2] and
two levels of night temperature. Each chamber was
4 m 2 m 2 m (length width height) and housed
two stainless-steel containers measuring 1.5 m 1.5 m 0.3 m (length width depth) filled with water into
which the rice pots were placed. We have used similar
chambers to perform elevated [CO2] experiments on
rice plants since 1996. Within each chamber, air temperature and relative humidity were controlled by
using electrical resistance heaters (with a bubbling
system for humidification) and cold-water heat exchangers with proportional-integral-derivative (PID) controllers (DB1000; Chino, Tokyo, Japan). [CO2] was
maintained at a set-point concentration using a computer-controlled pure-CO2 injection system with PID
controller, which give reliable performance between
chamber replicates (Cheng et al., 2001, 2006; Sakai
et al., 2001, 2006). Because there were no chamber
replicates (i.e. true replicates) in this study, we rotated
the treatments among the four chambers every 3 weeks
(changed the environmental settings and moved the
pots so that the pots received the same treatment)
during the treatment period, so as to minimize variation
due to the controlling system. A recent meta-analysis
showed that there was no difference between the use of
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E F F E C T S O F N I G H T T E M P E R AT U R E A N D [ C O 2 ] O N C H 4 E M I S S I O N
Daily CH4 flux and dark respiration (CO2 flux)
measurement
CH4 and CO2 fluxes were collected with a cylindrical,
transparent, acrylic, closed-top chamber (20.5 cm inside
diameter, 100 cm height, 0.3 cm thickness). During the
sampling time of 30 min, we covered each pot with the
chamber to capture gas exchanged between the pots
and the atmosphere. At 0, 15, and 30 min after the
chamber was placed, a gas sample of about 30 mL
was drawn with a 50 mL plastic syringe through a
capillary tube at the top of the chamber and injected
into a 19 mL vacuum bottle with a rubber stopper and
screw cap. The bottles were taken back to the laboratory,
where the amounts of CH4 and CO2 were measured by
gas chromatography (Shimadzu GC-7A, Kyoto, Japan)
with a flame ionization detector (FID) and a thermal
conductivity detector (TCD), respectively. The flux was
calculated from the increase in the gas concentration
inside the chamber per square metre per hour (Cheng
et al., 2006). Before treatment, only daytime CH4 flux
was determined once or twice every 2 weeks while rice
Day
40
Night
(a)
Night
Day
Air T
Day
Soil T
Low night temp.
35
30
25
Temperature (°C)
true replicates (chambers; 20 studies) and pseudoreplicates (plant within chamber, one chamber per treatment; 22 studies) on the results of elevated [CO2] and
temperature experiments (Zvereva & Kozlov, 2006).
The four treatment conditions were as follows: (1)
elevated [CO2] at 680 ppm and high night temperature
at 32 1C (EH); (2) ambient [CO2] at 380 ppm and high
night temperature at 32 1C (AH); (3) elevated [CO2] at
680 ppm and low night temperature at 22 1C (EL); and
(4) ambient [CO2] at 380 ppm and low night temperature at 22 1C (AL). As shown in Fig. 1, for high-nighttemperature treatments we maintained the day and
night air temperatures at a constant 32 1C. For the
low-night-temperature treatments, the day air temperatures were maintained from 08:00 to 16:00 hours and the
night air temperatures from 20:00 to 04:00 hours, with a
linear temperature transition phase of 2.5 1C h1 from
04:00 to 08:00 and 16:00 to 20:00 hours. For both highand low-night-temperature treatments, we checked for
variations in the air and soil (at 10 cm depth) temperatures in the chamber for 3 consecutive days (9–11
September), with data recorded every 10 min by a
Thermo Recorder (TR-71U, T&D Corp., Tokyo, Japan;
see Fig. 2). The actual average air temperatures were
30.3 and 26.5 1C, respectively; and the soil temperatures
were 28.4 and 24.2 1C for high- and low-night-temperature treatments, respectively. The differences of air and
soil temperatures between the high- and low-nighttemperature treatments were 3.8 and 4.2 1C, respectively, close to values predicted in global climate change
scenarios at the end of the 21st century (IPCC, 2007).
647
20
Daily average air temp.: 26.5 °C
Daily average soil temp.: 24.2 °C
15
(b)
Air T
Soil T
High night temp.
35
30
25
Daily average air temp.: 30.3 °C
Daily average soil temp.: 28.4°C
20
15
0
12
24
36
Time (h)
48
60
72
Fig. 2 Variations of air temperature (solid line) and soil temperature at 10 cm (dashed line) over 72 h (recorded each 10 min)
for (a) low- and (b) high-night-temperature treatments between
75 and 78 days after transplanting (9–11 September 2006).
Arrows indicate day and night flux sampling times while the
soil temperature was the same during the day and at night.
grew in an outdoor water tank, and the night respiration measurement was not carried out. After the onset
of the treatment, we measured CH4 fluxes each day at
10:00 and 22:00 hours, when the soil temperatures at
10 cm depth under low night temperatures were similar
( 25 1C; Fig. 2), while the daily CH4 flux was average of
day and night fluxes. The increase in [CO2] in the
chamber in the evening samples was used to calculate
night respiration. In addition, we gathered CH4 flux
data four times on 78 and 86 DAT to estimate daily
variations at a finer scale.
Measurement of dissolved CO2 and CH4 in soil solution
and calculating conductance for CH4 flux
The soil solution in each pot was sampled with a Rhizon
soil-solution sampler (10 Rhizon SMS-MOM; Eijkelkamp Agrisearch Equipment, Giesbeek, the Netherlands).
This sampler consists of a microporous polymer tube
(10 cm length, 2.5 mm outside diameter, 1.5 mm inside
diameter) and a PVC tube (50 cm length, 2.7 mm outside
diameter, 1.0 mm inside diameter). The microporous
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648 W . C H E N G et al.
Before treatment
After treatment
100
CO2(µg C mL–1)
(a)
80
60
Bef
40
EH
EL
AH
AL
EH
EL
AH
AL
8
(b)
CH4 (µg C mL–1)
polymer tube was inserted vertically into the soil at a
depth of 5–15 cm in each pot before transplanting the
rice plants. Before to sampling, about 5 mL of solution
was sucked out of the polymer tube with a 10 mL
vacutainer (Terumo Ltd, Tokyo, Japan) to remove impurities from the tube. Then a 19 mL semivacuum bottle
(filled with pure N2 gas at 0.5 atm) fitted with a rubber
stopper and screw cap was connected to the polymer
tube. About 9.5 mL of soil solution was sucked into the
bottle by the time the pressure in the bottle reached
1 atm. The amount of soil solution collected and
the headspace volume were determined by weighing
the bottle before and after sampling. CO2 and CH4 were
measured in the laboratory with a gas chromatograph
(Shimadzu GC-7A) with TCD and FID detectors,
respectively. Concentrations of CO2 and CH4 dissolved
in the soil solution were calculated by Henry’s law
according to the concentrations of CO2 and CH4 in the
headspace (Cheng et al., 2005).
The conductance for CH4 flux was calculated as follow
(Nouchi et al., 1994): conductance 5 (CH4 flux/concentration of CH4 in soil solution)/number of shoots.
6
4
2
Bef
0
0
Statistical analyses
An analysis of variance (ANOVA) was conducted on the
concentrations of CO2 and CH4 dissolved in the soil
solutions, daily CH4 flux, and night respiration, which
were measured every week during the treatment period; the [CO2] and night temperature were designated as
main-plot factors, and DAT was designated as a splitplot factor. The data gathered on 113 DAT was excluded
in this analysis, because high-night-temperature treatments had been terminated already. Also, a two-way
ANOVA was conducted on the total CH4 emission and the
plant parameters during the treatment period and at
harvest for effects of [CO2], night temperature, and the
[CO2] night temperature interaction. The analyses
were performed using the statistical package SPSS 14
(SPSS Inc., Chicago, IL, USA).
Results
Changes in concentrations of CO2 and CH4 dissolved in
soil solution
The concentration of CO2 dissolved in the soil solution
ranged from 50 to 90 mg C mL1 across the entire rice
growth period (Fig. 3a). The peak of dissolved CO2 in
the soil solution occurred at 5–6 weeks after rice transplanting, which corresponded to the maximum tiller
number stage (data not shown). After the onset of the
treatment, CO2 dissolved in the soil solution differed
significantly between treatments and the difference
14
28
42
56
70
84
Days after transplanting
98
112
Fig. 3 Changes in the concentration of (a) CO2 and (b) CH4
dissolved in the soil solution of potted rice plants grown in a
water tank before treatment and in a controlled chamber after
treatment. Bars indicate standard deviation (n 5 3). EH, elevated
CO2 and high night temperature; AH, ambient CO2 and high
night temperature; EL, elevated CO2 and low night temperature;
AL, ambient CO2 and low night temperature; CO2, carbon
dioxide; CH4, methane.
became progressively larger with time; the AL treatment consistently had the lowest concentration of CO2
in the soil solution. The ANOVA results showed that the
CO2 dissolved in soil solution was significantly affected
by night temperature (P 5 0.03), but not by elevated
[CO2] (P 5 0.17; Table 1). The concentration of CH4
dissolved in the soil solution increased steadily from
rice transplanting to harvest (Fig. 3b). After the onset of
the treatment, CH4 dissolved in soil solution was significantly affected by night temperature (Po0.01) and by
elevated [CO2] (P 5 0.03; Table 1). There were no significant interactions between elevated [CO2] and night
temperature in terms of their effect on dissolved CO2 or
CH4 in soil solution (P 5 0.09 and 0.21, respectively).
Changes in daily CH4 flux and night respiration
Before the treatment period, the CH4 flux increased
after about 7 weeks (i.e. at the maximum tiller stage)
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649
Table 1 The F and P values from analysis of variance (ANOVA) of main-plot factors of CO2 concentration ([CO2]) and night
temperature (Temp), split-plot factor of days after transplanting (DAT) on CH4 and CO2 dissolved in soil solutions, daily CH4 flux,
and night respiration CO2 throughout treatment season
CH4 dissolved
in soil solution
CO2 dissolved
in soil solution
Daily CH4 flux
Night respiration
(night CO2 flux)
F
F
P
F
P
Source
df
F
P
P
[CO2]
Temp
[CO2] Temp
Main-plot error
DAT
DAT [CO2]
DAT Temp
DAT [CO2] Temp
Split-plot error
1
1
1
8
6
6
6
6
48
7.6
104.8
1.9
0.03
o0.01
0.21
2.3
6.6
3.6
0.17
0.03
0.09
6.0
94.5
2.4
0.04
o0.01
0.16
36.8
150.1
2.1
o0.01
o0.01
0.19
234.9
3.0
7.9
6.9
o0.01
0.02
o0.01
o0.01
10.2
4.5
18.8
1.1
o0.01
o0.01
o0.01
0.37
59.3
4.2
14.6
3.3
o0.01
o0.01
o0.01
o0.01
145.3
0.3
11.8
1.4
o0.01
0.95
o0.01
0.25
CH4, methane; CO2, carbon dioxide.
Before treatment
After treatment
Daily CH4 flux (mg C m–2 h–1)
40
EH
EL
AH
AL
30
20
Bef
10
0
0
14
28
42
56
70
84
Days after transplanting
98
112
Fig. 4 Changes in the daily CH4 flux from potted rice plants
grown in a water tank before treatment and in a controlled
chamber after treatment. EH, elevated CO2 and high night
temperature; AH, ambient CO2 and high night temperature;
EL, elevated CO2 and low night temperature; AL, ambient CO2
and low night temperature. Arrows indicate heading days for
each treatment. CO2, carbon dioxide; CH4, methane.
and varied with changes in air temperature (Figs 1
and 4). After the onset of the treatment, the CH4 fluxes
continued to increase for 3–4 weeks and then decreased
as the plants reached maturity despite air temperatures
being kept the same during the treatment period (32/32
and 32/22 1C day/night for the respective temperature
treatments). The largest fluxes coincided with the heading stage for all the treatments. After the heading stage,
the CH4 emitted during the day was larger than that at
night for all treatments (Fig. 5). The difference between
night-temperature treatments became apparent immediately after the start of the treatment, while the effect of
[CO2] became evident at 2 weeks after the start of the
treatment and only under low temperature. The daily
CH4 fluxes and accumulated CH4 emissions during the
treatment period were significantly increased by elevated [CO2] (P 5 0.03 and 0.04, respectively) and high
night temperature (both Po0.01; Tables 1 and 2). Elevated [CO2] caused CH4 emission to increase by 3.5%
and 32.2% under high and low night temperature conditions, respectively, while the 3.5% increase by elevated [CO2] under high night temperature condition
was not statistically significant (Table 2). Daily CH4 flux
varied weakly on days with low solar radiation,
whereas fluctuations were stronger on days with high
solar radiation (Fig. 6).
Night respiration ranged from 132 to 540 mg C m2 h1
during the entire treatment period, and this parameter
varied significantly with growth stage among the four
treatments and daytime solar radiation (Fig. 7). Nighttime CO2 respiration was significantly affected by elevated [CO2], as well as high night temperature (ANOVA,
both Po0.01; Table 1). There was no significant interaction between elevated [CO2] and night temperature in
terms of their effect on daily CH4 flux and night
respiration (P 5 0.16 and 0.19, respectively; Table 1).
Relationships between CH4 flux, CH4 concentration in
soil solution, and night respiration
Significant positive correlations were found between
CH4 flux and CH4 concentration in the soil solution
before the heading stage (r2 5 0.91, Po0.01), but from
then onwards the CH4 fluxes decreased with increasing
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650 W . C H E N G et al.
70
84
Days after transplanting
98
112
70
84
98
112
40
CH4 flux (mg C m–2 h–1)
(a)
40
(b) AH
EH
30
30
20
20
10
10
Day
40
(c)
40
Night
EL
(d) AL
30
30
20
20
10
10
0
CH4 flux (mg C m–2 h–1)
56
0
56
70
84
98
112
70
84
98
112
Days after transplanting
Fig. 5 The difference in CH4 flux between daytime and night-time from potted rice plants grown in controlled chambers during
treatment. Bars indicate standard deviation (n 5 3). (a) EH, elevated CO2 and high night temperature; (b) AH, ambient CO2 and high
night temperature; (c) EL, elevated CO2 and low night temperature; (d) AL, ambient CO2 and low night temperature. CO2, carbon
dioxide; CH4, methane.
Table 2 Effects of elevated [CO2] and night temperature on the CH4 emission and net dry weight increase by rice plant during the
treatment period, at total and stem dry weight at harvest
Night temperature
CO2 (abbrev.)
Total CH4
emission (g C hill1)
High (32 1C)
Elevated (EH)
Ambient (AH)
% change by e[CO2]
Elevated (EL)
Ambient (AL)
% change by e[CO2]
1.00a*
0.96a
3.5
0.74b
0.56c
32.2
Low (22 1C)
Net total dry
weight increase
(g hill1)
Total dry weight
at harvest (g hill1)
Stem dry weight
at harvest (g hill1)
60.9a
54.0a
12.7
57.6a
41.6b
38.4
122.2a
115.4a
5.9
119.0a
103.0b
15.5
50.5a
46.9a
7.7
41.5a
33.0b
25.9
*Different letters at same column indicated significantly different among four treatments at the 0.05 probability level.
CH4, methane; CO2, carbon dioxide.
CH4 concentration in the soil solution (Fig. 8). Significant positive correlations were found between the night
respiration and daily CH4 flux (r2 5 0.42, n 5 30,
Po0.01), but the relationship differed depending on
the measurement day (Fig. 9). The CH4 and night
respiration were measured eight times and the resulting
data can be divided into two groups. Group A was
composed of the first, second, and fourth measurements, which were made on days with higher solar
radiation (420 MJ m2 day1; Figs 4 and 7), and plants
were in the growth stage before the grain stage. Group
B was composed of the third and the fifth to eighth
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Journal compilation r 2008 Blackwell Publishing Ltd, Global Change Biology, 14, 644–656
E F F E C T S O F N I G H T T E M P E R AT U R E A N D [ C O 2 ] O N C H 4 E M I S S I O N
EH
CH4 flux (mg C m–2 h–1)
40
EL
AH
Night
Day
AL
Night
Day
(a)
651
40
(b)
30
30
20
20
10
10
Low solar radiation
(rainy day)
High solar radiation
(sunny day)
0
0
6
12
18
24
6
12
18
24
Local time (h)
Fig. 6 Effect of solar radiation on diurnal CH4 flux variations among the four treatments: (a) on a rainy day (78 days after
transplanting); (b) on a sunny day (86 days after rice transplanting). Bars indicate standard deviation (n 5 3). EH, elevated CO2 and
high night temperature; AH, ambient CO2 and high night temperature; EL, elevated CO2 and low night temperature; AL, ambient CO2
and low night temperature; CO2, carbon dioxide; CH4, methane.
measurements, which were made on days with lower
solar radiation (o20 MJ m2 day1; Figs 4 and 7); the
third measurement was made on a rainy day and the
fifth to eighth measurements were made after the plants
had reached the grain stage (Fig. 9). These results
suggest that both the rice growth stage as well as solar
radiation affect CH4 emission and night respiration.
Additionally, the conductance for CH4 flux (calculated by parameters of CH4 flux, concentration of CH4
in soil solution, and number of shoots) had different
change patterns among the four treatments, even
though the soil temperatures were kept at 28.4 1C for
high-night-temperature treatments and at 25.1 1C for
low-night-temperature treatments during the experimental period (Fig. 10).
Discussion
CH4 emissions influenced by elevated [CO2] and night
temperature
Many studies have demonstrated a positive effect of
elevated [CO2] on CH4 emission from natural wetlands
(Dacey et al., 1994; Hutchin et al., 1995; Megonigal &
Schlesinger, 1997; Saarnio & Silvola, 1999; Vann &
Megonigal, 2003) and rice paddies (Ziska et al., 1998;
Allen et al., 2003; Inubushi et al., 2003; Cheng et al., 2006;
Zheng et al., 2006). The rate of CH4 emission increase
due to elevated [CO2] varied widely, ranging from 20%
to 600%. Two free-air CO2 enrichment experiments
performed in Japan and China showed that the average
increase in CH4 emission from rice paddies due to
elevated [CO2] was 58.2% with normal management
(Inubushi et al., 2003; Zheng et al., 2006). The increased
CH4 emission in response to elevated [CO2] was attributed to accelerated CH4 production as a result of
increased root exudates and root autolysis products
and to increased plant-mediated CH4 emission because
of the higher rice tiller numbers under elevated [CO2]
conditions (Inubushi et al., 2003; Cheng et al., 2005;
Zheng et al., 2006). In this experiment, we imposed the
high [CO2] treatment only in the second half of the rice
growth period, after panicle formation (Fig. 1), so that
there was no difference among treatments in tiller
number and rice root biomass that would increase
plant-mediated CH4 emission and root autolysis products (W. Cheng, H. Sakai, K. Yagi, T. Hasegawa,
unpublished results). Nevertheless, elevated [CO2]
caused the total CH4 emissions to increase significantly
(by 32.2%) under the low-night-temperature condition,
suggesting that increased photosynthesis, and possibly
increased root exudates (from photosynthesis) and their
decomposition, can substantially promote CH4 emission.
In contrast, elevated [CO2] did not increase the total
CH4 emissions under the high-night-temperature condition (Fig. 4; Table 2), suggesting that increased night
temperature reduces the stimulatory effect of elevated
[CO2] on CH4 emission. This result was consistent with
the net total dry weight increase (i.e. difference in dry
weight before and after treatments) (Table 2). Thus,
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Journal compilation r 2008 Blackwell Publishing Ltd, Global Change Biology, 14, 644–656
652 W . C H E N G et al.
500
EH
EL
AH
AL
400
300
After heading
EH
AH
30
EL
AL
20
10
0
200
0
1
2
3
4
5
6
CH4 dissolved in the soil solution (µg C mL–1)
7
Fig. 8 Relationship between daily CH4 flux and CH4 concentration in the soil solution among the four treatments while rice
plants were grown in controlled chambers. EH, elevated CO2
and high night temperature; AH, ambient CO2 and high night
temperature; EL, elevated CO2 and low night temperature; AL,
ambient CO2 and low night temperature; CH4, methane; CO2,
carbon dioxide.
100
30
Solar radiation
(MJ m–2 day–1)
Before heading
40
Daily CH4flux (mg C m–2 h–1)
Night respiration (night CO2 emission)
( mg C m–2 h–1)
600
20
10
0
70
84
98
Days after transplanting
112
Fig. 7 Changes in dark respiration (night CO2 emission) of rice
plants grown in controlled chambers during the treatment. Bars
indicate standard deviation (n 5 3). EH, elevated CO2 and high
night temperature; AH, ambient CO2 and high night temperature; EL, elevated CO2 and low night temperature; AL, ambient
CO2 and low night temperature. The solar radiation on each
sampling day is shown in the lower portion of the figure. CO2,
carbon dioxide.
increased night temperature reduces the stimulatory
effect of elevated [CO2] on both CH4 emission and rice
growth (total biomass increase) simultaneously. This
finding confirms that CH4 emission is highly dependent
on rice carbon gain due to net photosynthesis. We
cannot explain why the high night temperature reduces
the stimulatory effect of elevated [CO2] on rice biomass
increase; however, a possible reason is that the increased plant respiration at high night temperature
reduced the difference in C accumulation between
elevated and ambient [CO2] conditions.
Many previous studies reported that CH4 emissions
were linearly related to photosynthetic CO2 uptake rate
or total and root biomass productions in natural wetlands and rice paddies (Whiting & Chanton, 1993; Sass
& Fisher, 1995; Huang et al., 1997; Olszyk et al., 1999;
Allen et al., 2003). Our results imply that in order to
estimate the CH4 emission from rice paddies under
40
Daily CH4 flux (mg C m–2 h–1)
56
30
EH
yB = 0.078xB–3.97
AH
r2=0.69**
n=18
3
3
EL
AL
6
67
7
20
4 4
22
5
3
5
4
5
12 1
6
7 3
10
8
8
7
6
1
5
4
2
1
yA=0.083xA–17.03
r 2 =0.86**
n=12
0
0
200
400
600
Night respiration, CO2 flux (mg C m–2 h–1)
Fig. 9 Relationship between daily CH4 flux and night respiration among four treatments during the rice plants grown
in controlled chambers. EH, elevated CO2 and high night
temperature; AH, ambient CO2 and high night temperature;
EL, elevated CO2 and low night temperature; AL, ambient
CO2 and low night temperature. The numbers (1–8) within
symbols on the graph indicate the sampling times after treatments began. Data fell within two groups: Group A was composed of the first, second, and fourth samples; Group B was
composed of the third and the fifth to eighth samples. CH4,
methane; CO2, carbon dioxide.
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E F F E C T S O F N I G H T T E M P E R AT U R E A N D [ C O 2 ] O N C H 4 E M I S S I O N
Conductance (cm3 h–1 shoot–1)
15
EH
AH
EL
70
84
98
AL
10
5
0
56
112
Days after transplanting
Fig. 10 Changes in conductance of CH4 flux among treatments
while rice plants were grown in controlled chambers. EH,
elevated CO2 and high night temperature; AH, ambient CO2
and high night temperature; EL, elevated CO2 and low night
temperature; AL, ambient CO2 and low night temperature; CH4,
methane; CO2, carbon dioxide.
elevated [CO2] and air temperature (including elevated
night temperature), the crop and soil model must be
capable of simulating these interactive effects on crop
growth. Although many studies have shown that elevated air temperature modifies the effect of elevated
[CO2] on rice growth and yield (Baker & Allen, 1993;
Kim et al., 1996; Ziska et al., 1997; Moya et al., 1998),
more studies should be performed to confirm our
results regarding the combined effects of elevated
[CO2] and night temperature. Again, the tiller number
and root biomass (not shown) were similar among the
four treatments, as these tissues were formed during the
vegetative growth stage before we initiated the [CO2]
and night-temperature treatments. Therefore, the increased CH4 emissions can be attributed to accelerated
CH4 production as a result of increased root exudates.
Seasonal and daily variation of CH4 flux influenced by
elevated [CO2] and night temperature
Seasonal variation of CH4 flux follows rice plant development, with or without apparent seasonal temperature
dependence in the fields (Schutz et al., 1990; Sass &
Fisher, 1997; Khalil et al., 1998). For paddy soils flooded
continuously without organic matter addition, CH4 flux
gradually increases during the vegetative stage with
increasing plant biomass and reaches the maximum
value during the reproductive stage (Nouchi et al.,
1994; Sass & Fisher, 1997; Wassmann et al., 2000;
653
Le Mer & Roger, 2001). Our results showed that CH4
and CO2 fluxes had significant seasonal variations even
though the same air temperatures were maintained for
each treatment during the entire treatment period (Figs
4 and 7; Table 1). The peak CH4 flux occurred around
the heading stage in all four treatments and then
decreased until harvest (Fig. 4). Sakai et al. (2001)
reported that rice canopy respiration and photosynthesis decreased after the heading stage in both elevated
and ambient [CO2] treatments. Thus, the CH4 flux
decrease after the heading stage observed in the present
study could be partly attributed to decreased photosynthesis rate and carbohydrate accumulation. Decreased night respiration also provided evidence that
seasonal variation of CH4 flux influenced by elevated
[CO2] was due to changes in photosynthesis, because
significant relationships were reported between night
respiration and gross or net rice photosynthesis rates
under both elevated and ambient [CO2] conditions
(Sakai et al., 2001). The relationship between night
respiration and CH4 flux is not well understood, and
to our knowledge, this study is the first to report a
significant correlation between night respiration and
daily CH4 flux. In addition, our findings suggest that
variations in night respiration are more sensitive to
daytime solar radiation than are variations in CH4 flux
(Figs 7 and 9).
Daily variation of CH4 flux is largely due to temperature variation. The highest rice CH4 fluxes usually occur
in the late afternoon and the lowest occur in the early
morning, which coincides with the temperature variation in the upper soil layer (Holzapfel-Pschorn et al.,
1986; Wassmann et al., 1994; Yagi et al., 1996; Hosono &
Nouchi, 1998). Our results showed, however, that CH4
fluxes during the day were markedly larger than those
at night, even though the air and soil temperatures were
similar between day and night. Interestingly, the day–
night difference in CH4 fluxes expanded after the heading stage in the high-night-temperature treatments
(Fig. 5). The reason for this is unclear, but this finding
implies that the daily variation in CH4 fluxes depended
not only on soil temperature, but also on the rice plants’
physiological metabolism or physiological age. It is also
interesting to note that diurnal variation was more
pronounced on a sunny day than on a cloudy day
(Fig. 6), which also suggests the dependence of CH4
on daytime carbon gain.
Conductance for CH4 flux influenced by elevated [CO2]
and night temperature
Plant-mediated transport is the dominant pathway for
CH4 flux from flooded rice paddies, where CH4 is
produced by methanogens under anaerobic conditions
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654 W . C H E N G et al.
(Schutz et al., 1989; Nouchi et al., 1990; Wassmann et al.,
1996). Many studies reported that the concentration of
CH4 dissolved in the soil solution has a strong relationship with CH4 flux (Nouchi et al., 1990; Wassmann et al.,
1996; Ziska et al., 1998; Lu et al., 2000), because dissolved
CH4 diffuses into the cell-wall water of root cells,
gasifies in the aerenchyma channel of the root cortex,
and then diffuses from roots into the leaf sheaths
(Nouchi et al., 1990). Our results showed that there
was a significant positive relationship between CH4
flux and CH4 concentration in the soil solution before
the heading stage (Po0.01), but the CH4 fluxes decreased with increased CH4 concentration in the soil
solution after the heading stage (Figs 3, 4, and 8). The
decline of CH4 fluxes would be due to the decrease of
the conductance for CH4 flux, which is an index of gas
transport capacity (Nouchi et al., 1994; Lu et al., 2000).
Conductance for CH4 flux in rice paddies is strongly
affected by soil temperature and rice cultivar properties
(Hosono & Nouchi, 1997; Yao et al., 2000). As shown in
Fig. 10, the conductance for CH4 flux varied during the
experimental period among the four treatments, even
though the soil temperatures were kept at 28.4 1C for
high-night-temperature treatments and at 25.1 1C for
low-night-temperature treatments at the time of CH4
flux measurements. On average, high-night-temperature treatments had higher conductance for CH4 flux
than the low-night-temperature treatments. This finding is consistent with the results reported by Nouchi
et al. (1994) and Hosono & Nouchi (1997). In addition,
elevated [CO2] also affected the conductance for CH4
flux, but this was evident only under low night temperatures. Yao et al. (2000) reported that the conductance for CH4 flux was positively correlated with
parameters of plant size, and most strongly with stem
intercellular volume. Thus, the different effects of elevated [CO2] on conductance for CH4 flux between the
high- and low-night-temperature treatments are likely
due to differences in plant size. In addition, the dry
weight of stem at harvest was significantly increased
(by 26%) by elevated [CO2] under low night temperature, but dry weight was not significantly increased
(7.7%) under high night temperature (Table 2). Finally,
the decrease in CH4 conductance with crop age is
another reason for the decreased CH4 emission after
the heading stage.
Conclusions
The results of this study provide convincing evidence
that both elevated [CO2] and high night temperature
cause significantly increased CH4 emissions from rice
paddy soils, although the elevated [CO2] high night
temperature interaction was not significant (P 5 0.11).
Elevated [CO2] increased CH4 emission by 3.5% under
high temperature conditions, but this increase was
32.2% under low night temperature conditions. In addition, elevated [CO2] affected the carbohydrate assimilation, measured as net dry weight increase, and stem dry
weight, which represents the size of the CH4 pathway,
under high- and low-night-temperature conditions,
showing trends similar to those for CH4 emission. The
CH4 emission during the daytime was larger than at
night, even in the high-night-temperature treatment (i.e.
a constant temperature all day). We observed significant
correlations between the dark respiration and daily
CH4 flux (Po0.01). These results suggest that net plant
photosynthesis contributes greatly to CH4 emission,
and increasing night temperature reduces the stimulatory effect of elevated [CO2] on CH4 emission from rice
paddy soil. It should be noted, however, that our results
are based on a chamber experiment, and the daily
temperature variations did not match those in the field.
And the 10 1C difference between high and low night
temperature was out the scenario of climate change in
future. Therefore, to better understand the effects of
predicted climate warming, field studies on the interactive effects of elevated [CO2] and night temperature
should be performed.
Acknowledgements
This research was funded by Global Environment Research
Program, Ministry of the Environment, Japan. We thank Drs
M. Yoshimoto and M. Fukuoka of the National Institute for
Agro-Environmental Sciences (NIAES) for their helpful comments and discussions, and Drs S. Sudo and K. Minamikawa
of NIAES for their assistance of CO2 and CH4 analyses.
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