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Diurnal variation of methane emission from a paddy field in Brazilian Southeast/Variacao diurna da emissao de metano em arroz irrigado no Sudeste do Brasil.


The lowland flood-irrigated rice is a cropping system that promotes methane (C[H.sub.4]) emission, an important greenhouse gas that strongly influences the atmosphere photochemistry. The C[H.sub.4] shows a potential global heating capacity 28-fold higher than carbon dioxide (C[O.sub.2]) over a 100-year time horizon (MYHRE et al., 2013). Local measurements of C[H.sub.4] emissions are essential for the improvement of national and regional gas emission inventories. In order to optimize efforts for gas measurements it is important to know the time representing the average daily emission for a given producing area, as well as the influence of some key environmental parameters associated with the emission fluxes, for example, soil, air and water temperatures. A number of studies reported positive correlations between C[H.sub.4] diurnal emission variations and soil temperature in paddy fields under different climate conditions (SCHuTZ et al., 1990; YAGI & MINAMI, 1990; SASS et al., 1991; COSTA et al., 2008). WANG et al. (1997) argued that diel patterns of C[H.sub.4] emissions are determined by the interaction of the soil temperature and the partial pressure of C[H.sub.4].

NEUE et al. (1997) observed fast C[H.sub.4] emission increase after sunrise reaching a maximum after midday, decreasing until minimum at night. Other authors also reported one C[H.sub.4] emission peak during the day (SATPATHY et al., 1997; WANG et al., 1999), but there are reports about the occurrence of two peaks (WANG et al. 1993). SASS et al. (1991) observed diurnal maximum emission values between 7 and 9p.m. in rice fields in Texas. Peaks at night could be probably caused by a lower [O.sub.2] transport to the rhizosphere, causing lower C[H.sub.4] oxidation and higher net emissions (SCHUTZ et al., 1989). According to SCHuTz et al. (1990), the diurnal C[H.sub.4] emission rhythm may increase with the increasing diurnal rhythm of root exudates, resulting in higher apparent activation energy ([E.sub.a]). [E.sub.a] represents the microbial community response to temperature, which is responsible for the C[H.sub.4] production and release to the atmosphere. SASS et al. (1991) showed that the solar radiation and the photosynthetic activity of rice plant are correlated with the C[H.sub.4] production and with the grain yield. DENIER VAN DER GON et al. (1996) also reported that temperature and solar radiation may affect C[H.sub.4] emission due to their effect in the net primary production and in the root exudation. By using the eddy covariance technique, HATALA et al. (2012) argued that the gross photosynthesis, more than the soil temperature and other abiotic factors, is the primary causes of the diurnal pattern in rice paddy C[H.sub.4] flux. On the same line, KNOX et al. (2016) concluded that photosynthesis is the dominant factor influencing the diurnal pattern in C[H.sub.4] flux, although, soil temperature significantly influences the amplitude of diurnal C[H.sub.4] fluctuations. Most part of the studies has been carried out in temperate and subtropical climate regions and scarce information is available for tropical soils. The Paraiba Valley, located in the Southeast of Brazil, under tropical climate, has just over 7,000 hectares of irrigated rice, about 69% of the total area of rice production in the state of Sao Paulo. It became the remaining region of rice production in the state, since the upland and rainfed rice was strongly reduced over the last few decades. The objective of this study was to investigate the diurnal variation of C[H.sub.4] emission in a flooded-irrigated rice system in specific days of different plant development stages, under tropical climate, and three growth seasons in order to determine the appropriate time period for gas sampling in that region. It aimed also to verify correlations between C[H.sub.4] flux and air, water and soil temperatures, and solar radiation. This information will support studies focused on C[H.sub.4] emission quantification in paddy fields and to contribute with the improvement of gas emission inventories for the Southeast region of Brazil.


The study was carried out in an experimental paddy field at Pindamonhangaba, State of Sao Paulo, in the Agencia Paulista de Tecnologia dos Agronegocios (APTA), Polo Regional Vale do Paraiba (APTA), located at 22[degrees]55' S Latitude, 45[degrees]30' W Longitude, with 560 meters of average altitude. The soil is classified as a Haplic Gleysols (EMBRAPA, 2013) with clayey or loamy-clayey texture. The organic carbon (OC) content was estimated in 20.2 [+ or -] 2.6g [kg.sup.-1] at 0-10cm depth and 14.8 [+ or -] 2.4g [kg.sup.-1] at 10-20cm depth, and total nitrogen (N) content in 1.3g [kg.sup.-1] and 1.2g [kg.sup.-1] at 0-10cm and 10-20cm, respectively. The climate is type Cwa (tropical climate of altitude), according to the Koeppen classification, with average highest temperature above 22[degrees]C and average lowest temperature below 18[degrees]C, warm and moist summer and dry winter. The average annual rainfall is 1,334mm (VILLELA & FURLANI JUNIOR, 1996). The experiment consisted of a single water management (continuous), with plots of approximately 500 square meters with two repetitions. The IAC 103 rice variety was used in the three growth seasons (GS). It is characterized as a medium cycle variety with average plant height of 95cm and average grain yield of 5,056kg [ha.sup.-1]. Seedlings were manually transplanted, spaced 30cm between rows and 20cm between plants. After seedling regeneration, the field was flooded under 15cm of water, on average. The field was fertilized with urea. Campaigns of 24-hour gas sampling every 3h were performed in the GS of 2003/2004, 2004/2005 and of 2005/2006. In the 1st GS (2003/2004), rice was transplanted in Dec 31st, 2003, and two sampling campaigns were carried out: (C1) March 15th, 2004, in the booting stage in the reproductive phase (stage R2, according to COUNCE (2000)); (C2) April 26th, 2004, in the ripening stage (in the transition of the stages R7-R8), 37 days after panicle exertion and 16 days after soil drainage. We adopted this later sampling campaign to observe the diurnal C[H.sub.4] fluxes near the harvest. Also, only at 37 days after the panicle exertion the plant was completely mature, with a very slow soil drainage due to the frequent rain events occurred in that specific period and to the own physiographic condition of the study area. In this first GS soil, pH varied from 6.3 to 6.4, and Eh from -177 (C1) to -192 (C2). In the 2nd GS (2004/2005) rice was transplanted in Dec 21st, 2004 and three campaigns were performed: (C1) March 9th, 2005, in the rice plant booting stage (R2, according to COUNCE, 2000), 5 days before panicle exertion; (C2) March 23th, 2005, in the stage R5, 9 days after panicle exertion; (C3) april 13th, 2005, at the stage R7, 30 days after panicle exertion. The drainage of the fields occurred at Apr 20th, 2005. The pH soil values varied from 6.7 to 6.6 and Eh were -318 (C1), -292 (C2) and -233 (C3). In the 3th GS (2005/2006), rice was transplanted in Jan 1st, 2006 and three campaigns were performed: (C1) February 6th, 2006, in the V10 vegetative stage; (C2) March 20th, 2006, in the booting stage (R2), 3 days before flowering; (C3) April 10th, 2006, in the ripening stage (in the transition of the stages R6-R7). Fields drainage occurred seven days later. In that GS, soil pH were 6.5 (C1), 6.6 (C2) and 6.8 (C3), while Eh values were -202 (C1), -233 (C2), -221 (C3).

Methane Flux Measurements

Air samples were collected using the method of closed chamber (SASS et al., 1991). Chambers (60x60cm) were made with aluminum and composed by permanent anchors, extensors and lids equipped with temperature sensor, fans and a septum for air sampling. Each chamber was settled 5cm depth into the soil soon after the flooding, and remained in the same place during the entire growing season. Air samples were collected from the chamber lids at 3-hour interval, using 60mL polystyrene syringes (DA Becton, Dickinson and Company--BD). Each flux value was obtained from a series of five samples taken from each box at 5min intervals (SASS et al., 2002). Zero-minute samples were taken outside the chamber, 1 meter over the surface of the rice paddy. Samples were analyzed in a Agilent model GC 6890 gas chromatograph, equipped with 6-way valves, split mode injector, 0.5cc stainless-steel loop, HP-Plot Al/M megabore column (0.53mm diameter x 30m length) and flame ionization detector (FID). A standard curve of C[H.sub.4] was prepared with 5, 10 and 20ppm of C[H.sub.4] Methane fluxes were calculated by the equation f = H[[mu]P/RT][[DELTA]C/[DELTA]t] where f is C[H.sub.4] flux, P is the mean air pressure in the chamber ([approximately equal to]1atm), [mu] is the gas molecular weight of C[H.sub.4] (16.123g/mol), R is the universal gas constant (8.31441 J/mol x K), T is the temperature within the chamber at sampling (K), H is the height (m) of the chamber at sampling, [DELTA]C/[DELTA]t is the change in C[H.sub.4] concentration during the incubation time ([DELTA]t).

Environmental parameters

Average air temperature and solar radiation data were obtained from the meteorological station of "APTA--Vale do Paraiba", at Pindamonhangaba. Temperatures of floodwater and soil (at 2, 5 and 10cm depth) were registered with a Full Gauge thermometer of five edges. Air temperature inside the chambers were registered at each gas sampling time with a digital thermometer. Soil pH and Eh data were registered using a Digimed digital pHmeter.

Data analysis

A second-degree polynomial nonparametric local-regression model was used to fit a smooth curve to the C[H.sub.4] diurnal emission data. The adjusted curves were used to estimate the average diurnal C[H.sub.4] emission over each 24h-campaign and the respective time for these emissions. The 95% confidence interval of adjusted curve was used to calculate the error emissions. Correlation coefficients between C[H.sub.4] emission and other variables were estimated using the method of Pearson (p [less than or equal to] 0.05). We calculated the activation energy, Ea (kJ [mol.sup.-1]), using the linearized equation of Arrhenius (SASS et al., 1991) ln(f) = ln(a)--[[E.sub.a]/R[T.sub.s2] where f is the C[H.sub.4] emission, a is the Arrhenius constant, R is the gas universal constant (J/mol x K) and [T.sub.s2] is the temperature of the soil at 2cm depth (K). The parameters were estimated by carrying out linear regression. Data were analyzed using the R software (R CORE TEAM, 2015).


Diurnal variation of C[H.sub.4] emission in the 24h-campaigns in the three rice growth stages

Emission peaks were mostly observed in the afternoon and lower fluxes were recorded in the early morning (Figure 1), as also observed by other authors (WASSMANN et al., 1994; SATPATHY et al., 1997; WANG et al., 1997; YANG & CHANG, 1999; TSENG et al., 2010). Average C[H.sub.4] flux rate at the R2 stage (C1) of the first GS (7.58 [+ or -] 1.05mg C[H.sub.4] m-2 h-1) was lower compared with the following GS (11.74 [+ or -] 1.87 and 13.22 [+ or -] 2.61 in 2004/2005 and 2005/2006, respectively). These lower emissions might be partially explained by climatic conditions with lower average air temperature in the (C1) campaign (23.6[degrees]C, in a range of 17.3 -31.7[degrees]C) when compared with the campaigns performed in the R2 stage in the two following GS (28.0 and 28.4[degrees]C in the 2004/2005 and 2005/2006 GS, respectively) (Table 1). According to YOSHIDA (1981), the optimum rice crop growth occurs under air temperatures between 20 and 35[degrees]C, flowering, 30 and 33[degrees]C, and ripening, 20 and 25[degrees]C. Temperature is an important factor in photosynthetic process due to the effect on enzymes that catalyze the reactions. In turn, the air temperature is indirectly dependent on solar radiation. Diurnal accumulated solar radiation registered in the 24h-campaigns performed in the first GS (100.4cal.[cm.sup.-2].[dia.sup.-1] at C1 and 119.5cal.[cm.sup.-2].[dia.sup.- 1] at C2) was lower than those of the following ones (129.1 to 239.0cal.[cm.sup.-2].[dia.sup.-1] in the GS of 2004/2005 and of 188.8 to 217.5cal.[cm.sup.-2].[dia.sup.-1] in 2005/2006), which could have affected the efficiency of the photosynthetic process and exudates production with consequent lower C[H.sub.4] emission rates. Lower C[H.sub.4] emission rates observed in the latest campaigns, at the maturity, might be attributable to the decrease of the capacity of C[H.sub.4] transportation caused by the blocking of aerenchymal channels (AULAKH et al., 2001) and to the increase of C[H.sub.4] oxidation in the soils (SCHUTZ et al., 1989). In the second 24h-campaign (Apr 26th) of the first GS, after 16 days of the soil drainage, when there was not a water blade, C[H.sub.4] fluxes were recorded probably due to several rain events, favoring some anoxic condition in the soil, with a Eh equivalent to -192. Higher C[H.sub.4] emission rates were observed between the R2 and R5 stages in the second and third GS, in a range of 11.7 to 13.2mg C[H.sub.4] [m.sup.-2] [h.sup.-1], then decreasing in later stages, when the grains are being filled and the physiologic maturity is achieved. Based on the daily C[H.sub.4] average flux over each 24h-campaign, the most appropriate local time for gas sampling in the studied area was estimated at 12:11:15a.m. [+ or -] 01:14:16 (mean [+ or -] standard deviation) and 09:05:49p.m. [+ or -] 01:29:04.

Correlation between parameters and C[H.sub.4] emissions

A modest but significant correlation was reported between C[H.sub.4] emission and air temperature in the reproductive and in the ripening stages ([r.sup.2]=0.55 and [r.sup.2]=0.53, respectively, p [less than or equal to] 0.05), while a higher correlation was reported between C[H.sub.4] emission and water temperature (Table 2) in the same stages ([r.sup.2]=0.82 and [r.sup.2]=0.72 respectively, p [less than or equal to] 0.05). Similarly, SATPATHY et al. (1997) reported a high correlation between C[H.sub.4] emission and water and air temperature at the rice tillering and ripening stages. MEIJIDE et al. (2011) associated higher C[H.sub.4] emissions in the late evening with higher water temperature in a rice paddy field in Italy.

Methane emission and soil temperature was highly correlated (Table 2), as also reported by other authors (YAGI & MINAMI (1990), SASS et al. (1991), WANG et al. (1999)). That correlation was significant for the 24h-campaigns performed in the vegetative and reproductive stages in the depths of 2, 5 and 10cm, but also in the ripening stage at 2cm of depth. The C[H.sub.4] emission rates over each 24h-campaign were fit to Arrhenius equation as a function of soil temperature at 2cm of depth to calculate the activation energy ([E.sub.a]) an [E.sub.a] of 93.68 [+ or -] 11.17 kJ [mol.sup.-1] ([r.sup.2]=0.81, p. value <0.05) was obtained for the 24h-campaign at the R2 stage, while values of 61.74 [+ or -] 27.51kJ [mol.sup.-1] ([r.sup.2]=0.14) and 42.69 [+ or -] 15.02kJ [mol.sup.-1] ([r.sup.2]=0.54, p. value <0.05) were registered for the 24h-campaign in the ripening and vegetative stages, respectively. These values are near to the range of 50 to 130kJ [mol.sup.-1] reported by NEUE & SASS (1994). COSTA et al. (2008) reported Ea values in the range of 59 to 341kJ [mol.sup.-1] in a conventional planting system in South of Brazil, under subtropical climate. The occurrence of maximum Ea values in the campaigns performed in the R2 stage might be probably due to the increased amounts of root exudates as carbon source for C[H.sub.4] formation (LINDAU et al., 1991; MINODA & KIMURA, 1994). Solar radiation was weakly correlated with the C[H.sub.4] emission rates throughout the day. According to MEIJIDE et al. (2011), pressure gradients in the plant, which are driven by diurnal variation in light availability, may produce variation on the C[H.sub.4] emissions according to the solar radiation. Solar radiation may have an indirect effect on C[H.sub.4] emissions since it affects temperature and light intensity, which are important parameters for the development of the plant. Other variables should be also considered to better explain C[H.sub.4] diurnal fluxes, for example, the gross photosynthesis and the soil microbiological dynamics.


Higher C[H.sub.4] emission rates occur in the afternoon and lower in the early morning in the studied area. Soil temperature at 2cm of depth is highly associated to the C[H.sub.4] fluxes in all studied stages, so that it is a key parameter to be considered in gas flux measurements in paddy fields. The C[H.sub.4] emission activation energy in response to this parameter was higher in the stage R2. Also, all the environmental parameters presented correlation with the C[H.sub.4] fluxes in the stage R2, when methane emission is typically high along the flooded rice growth season and possibly making such correlations more evident. Based on the daily C[H.sub.4] average flux over each 24h-campaign, the most appropriated average time for gas collection in the region is at 12:11:15a.m. [+ or -] 01:14:16 (mean [+ or -] standard deviation) and 09:05:49p.m. [+ or -] 01:29:04.


The authors are grateful to the Ministry of Science and Technology (MCT) for the financial aid and to the Experiment Station of APTA for the support during the experiments.


The authors declare no conflict of interests.


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Magda Aparecida de Lima (1) * (iO) Ricardo Antonio Almeida Pazianotto (1) (iO) Omar Vieira Villela (2) (iO) Lourival Costa Paraiba (1) (iO)

(1) Emprapa Meio Ambiente, Rodovia SP-340, 13820-000, Jaguariuna, SP, Brasil. E- mail: * Corresponding author.

(2) Agencia Paulista de Tecnologia dos Agronegocios (APTA), Polo regional Vale do Paraiba, Pindamonhangaba, SP, Brasil.

Caption: Figure 1--Methane emission fluxes (mg C[H.sub.4] [m.sup.-2] [h.sup.-1]) determined in each 24h-campaign in a paddy field in three rice-cropping seasons (2003/2004, 2004/2005, 2005/2006), and the curve adjusted by local regression model with confidence interval of 95%. Dotted line indicates the average diurnal emission and dashed line the best local time for gas sampling.
Table 1--Average and ranges of air, water and soil temperatures at 2
cm, 5 cm and 10 cm of depth, and average methane emission rates
observed in the 24h-campaigns in three growing seasons of flood-
irrigated rice cropping, calculated by a curve fit to local
regression model. The error corresponds to 95% confidence interval
of the adjusted curve.

                     Plant stage     Air Temp.          Water
                         (*)        [degrees]C     Temp. [degrees]C

                                   1st Growing season (2003/2004)

C1: Mar 15th, 2004       R2            23.6              24.1
                                   (17.3 -31.7)      (21.6-25.4)
C2: Apr 26th, 2004      R7-R8          20.5               1

                                   2nd Growing season (2005/2006)

C1: Mar 9th, 2005        R2            28.0              25.6
                                    (18.4-36.7)      (22.2-29.5)
C2: Mar 23rd, 2005       R5            26.5              25.5
                                    (21.9-34.1)      (24.2-28.2)
C3: Apr 13th, 2005       R7            25.4              23.8
                                    (16.5-38.2)      (21.2-27.0)

                                   3rd Growing season (2005/2006)

C1: Feb 6th, 2006        V10           28.4              28.9
                                    (21.4-41.1)      (25.2-37.4)
C2: Mar 20th, 2006       R2            25.0              26.0
                                    (21.2-36.7)      (24.0-30.2)
C3: Apr 10th, 2006      R6-R7          24.0              24.1
                                    (18.5-34.8)      (22.4-26.7)

                       Soil Temp,       Soil Temp.
                     2cm [degrees]C   5 cm [degrees]C

                     1st Growing season (2003/2004)

C1: Mar 15th, 2004        22.9             22.9
                      (21.7-23.7)       (22.1-23.5)
C2: Apr 26th, 2004        20.0             20.4
                      (19.1-20.8)       (19.6-21.1)

                     2nd Growing season (2005/2006)

C1: Mar 9th, 2005         25.5             25.5
                      (23.0-28.5)       (23.9-27.5)
C2: Mar 23rd, 2005        25.3             25.2
                      (24.1-26.5)       (24.2-26.2)
C3: Apr 13th, 2005        23.6             23.7
                      (22.2-25.0)       (22.6-24.6)

                     3rd Growing season (2005/2006)

C1: Feb 6th, 2006         28.0             28.1
                      (25.7-30.7)       (26.3-30.3)
C2: Mar 20th, 2006        25.9             25.8
                      (24.8-27.2)       (24.9-26.6)
C3: Apr 10th, 2006        24.1             24.2
                      (23.4-24.9)       (23.6-25.4)

                                              Average CH4
                       Soil Temp.               diurnal
                     10cm [degrees]C         emission rate
                                       (mg [m.sup.-2] [h.sup.-1])

                     1st Growing season (2003/2004)

C1: Mar 15th, 2004        23.0             7,58 [+ or -] 1,05
C2: Apr 26th, 2004        20.7             7.8 [+ or -] 2.04

                     2nd Growing season (2005/2006)

C1: Mar 9th, 2005         25.6            11.74 [+ or -] 1.87
C2: Mar 23rd, 2005        25.0            12.59 [+ or -] 3.51
C3: Apr 13th, 2005        23.9             6.75 [+ or -] 2.94

                     3rd Growing season (2005/2006)

C1: Feb 6th, 2006         28.0             5.52 [+ or -] 0.35
C2: Mar 20th, 2006        25.6            13.22 [+ or -] 2.61
C3: Apr 10th, 2006        24.4             6.18 [+ or -] 1.70

(*) according to Counce (2000); V10: vegetative stage, where there
is a collar formation on leaf 10 on the main stem; R2: booting
stage, with the flag leaf collar; R5: at least one caryopsis on the
main stem panicle is elongating to the end of the hull; R6: at least
one caryopsis on the main stem panicle has elongated to the end of
the hull; R7: grain drying: at least one grain of the main stem
presents yellow pericarp; R8: grain maturity, where at least one
grain of the main stem presents brown pericarp; (1) drained soil.

Table 2--Correlation coefficients between CH4 flux and solar
radiation, air, water and soil temperatures in a rice cropping area
under continuous flood-irrigation management system.

                              Pearson's coefficients of correlation
                                   (degrees of freedom)

Environmental parameters                 Rice growth stages

                               V10           R2         R5-R8 (1)

Solar radiation             -0,41 (7)    0,34 (24) *    0,24 (33)
Air temperature (2)         -0,18 (7)    0,55 (24) *   0,53 (33) *
Water temperature            0.31 (7)    0.82 (17) *   0.72 (23) *
Soil temperature            0.75 (7) *   0.89 (16) *   0.40 (30) *
  (2cm depth)
Soil temperature            0.78 (7) *   0.84 (16) *    0.33 (30)
  (5cm depth)
Soil temperature            0.75 (7) *   0.75 (16) *    0.25 (30)
  (10cm depth)

(1) intermediate stage; (2) data registered by the local
meteorological station. * p-value [less than or equal to] 0.05.
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Title Annotation:SOIL SCIENCE
Author:de Lima, Magda Aparecida; Pazianotto, Ricardo Antonio Almeida; Villela, Omar Vieira; Paraiba, Louriv
Publication:Ciencia Rural
Date:Apr 1, 2018
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