Methane production, oxidation and mitigation: A ...

Science of the Total Environment 572 (2016) 874–896

Contents lists available at ScienceDirect

Science of the Total Environment journal homepage: www.elsevier.com/locate/scitotenv

Review

Methane production, oxidation and mitigation: A mechanistic understanding and comprehensive evaluation of influencing factors Sandeep K. Malyan a, Arti Bhatia a,⁎, Amit Kumar a, Dipak Kumar Gupta b, Renu Singh a, Smita S. Kumar c, Ritu Tomer a, Om Kumar a, Niveta Jain a a b c

Centre for Environment Science and Climate Resilient Agriculture, ICAR-Indian Agricultural Research Institute, New Delhi, 110012, India ICAR-Central Arid Zone Research Institute, Regional Research Station, Pali-Marwar, Rajasthan 342003, India Department of Environmental Science and Engineering, Guru Jambheshwar University of Science and Technology, Hisar, Haryana 125001, India

H I G H L I G H T S

G R A P H I C A L

A B S T R A C T

• Water management (controlled irrigation and midseason drying) is the best CH4 mitigating option in irrigated rice field. • Ammonium based fertilizer having up to 60% CH4 mitigation potential. • Biofertilizer (Azolla and Cynobacteria) are best for sustainable rice cultivation. • Microbial fuel cells are the least explore mitigation option in flooded rice field.

a r t i c l e

i n f o

Article history: Received 20 January 2016 Received in revised form 2 July 2016 Accepted 25 July 2016 Available online 27 August 2016 Editor: Ajit Sarmah Keywords: Methane emission Measurement Mitigation Rice

a b s t r a c t Methane is one of the critical greenhouse gases, which absorb long wavelength radiation, affects the chemistry of atmosphere and contributes to global climate change. Rice ecosystem is one of the major anthropogenic sources of methane. The anaerobic waterlogged soil in rice field provides an ideal environment to methanogens for methanogenesis. However, the rate of methanogenesis differs according to rice cultivation regions due to a number of biological, environmental and physical factors like carbon sources, pH, Eh, temperature etc. The interplay between the different conditions and factors may also convert the rice fields into sink from source temporarily. Mechanistic understanding and comprehensive evaluation of these variations and responsible factors are urgently required for designing new mitigation options and evaluation of reported option in different climatic conditions. The objective of this review paper is to develop conclusive understanding on the methane production, oxidation, and emission and methane measurement techniques from rice field along with its mitigation/abatement mechanism to explore the possible reduction techniques from rice ecosystem. © 2016 Elsevier B.V. All rights reserved.

⁎ Corresponding author. E-mail addresses: abensc@gmail.com, artibhatia.iari@gmail.com (A. Bhatia).

http://dx.doi.org/10.1016/j.scitotenv.2016.07.182 0048-9697/© 2016 Elsevier B.V. All rights reserved.

S.K. Malyan et al. / Science of the Total Environment 572 (2016) 874–896

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Contents 1. 2.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . Production of methane in rice soil . . . . . . . . . . . . . . . 2.1. Hydrolysis . . . . . . . . . . . . . . . . . . . . . . 2.2. Acidogensis . . . . . . . . . . . . . . . . . . . . . . 2.3. Acetogenesis . . . . . . . . . . . . . . . . . . . . . 2.4. Methanogenesis . . . . . . . . . . . . . . . . . . . . 3. Methanogens . . . . . . . . . . . . . . . . . . . . . . . . 4. Pathways of methane emission . . . . . . . . . . . . . . . . 4.1. Diffusion . . . . . . . . . . . . . . . . . . . . . . . 4.2. Ebullition . . . . . . . . . . . . . . . . . . . . . . . 4.3. Plant-mediated transport . . . . . . . . . . . . . . . 5. Methane oxidation . . . . . . . . . . . . . . . . . . . . . . 5.1. Aerobic methane oxidation . . . . . . . . . . . . . . . 5.2. Anaerobic methane oxidation . . . . . . . . . . . . . 6. Factors affecting methane production/oxidation . . . . . . . . 6.1. Soil organic matter . . . . . . . . . . . . . . . . . . 6.2. pH and soil texture . . . . . . . . . . . . . . . . . . 6.3. Soil redox potential (Eh) . . . . . . . . . . . . . . . . 6.4. Oxygen availability . . . . . . . . . . . . . . . . . . 6.5. Soil temperature . . . . . . . . . . . . . . . . . . . 6.6. Plant growth stage . . . . . . . . . . . . . . . . . . 6.7. Diurnal and seasonal variation . . . . . . . . . . . . . 6.8. Effect of elevated CO2 concentration . . . . . . . . . . . 6.9. Rice cultivar . . . . . . . . . . . . . . . . . . . . . 6.10. Fertilizer . . . . . . . . . . . . . . . . . . . . . . 6.11. Pesticide application . . . . . . . . . . . . . . . . . 7. Method for methane flux measurements . . . . . . . . . . . . 7.1. Manual close-chamber method . . . . . . . . . . . . . 7.2. Automated close-chamber method . . . . . . . . . . . 7.3. Micrometeorological method (Eddy Covariance technique) 8. Mitigation of methane emission . . . . . . . . . . . . . . . . 8.1. Water management . . . . . . . . . . . . . . . . . . 8.1.1. Midseason drainage . . . . . . . . . . . . . . 8.1.2. Intermittent drainage . . . . . . . . . . . . . 8.1.3. Alternate drying and wetting . . . . . . . . . . 8.2. Plantation methods . . . . . . . . . . . . . . . . . . 8.3. Rice varietal selection . . . . . . . . . . . . . . . . . 8.4. Fertilization and nitrification inhibitors . . . . . . . . . 8.5. Other interventions for mitigation of methane in rice . . . 9. Concluding remarks . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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1. Introduction Methane (CH4) is a colorless, odorless greenhouse gas (GHG) which burns with a blue flame and was discovered by Allessandro Volta in 1778. CH4 also has some unique physical properties like boiling point of − 162.6 °C, density of 0.4240, C\\H and H\\H bond length of 1.1068 and 1.8118 Å respectively which make it different from other alkanes (Crabtree, 1995). Due to H\\C\\H, CH4 has tetrahedral geometry and its bond angle is equal to 109.5° (Fig. 1a). Geophysical properties of CH4 such as its atmospheric residence time of 12.4 years and instantaneous forcing of 1.37 × 105 W/m2/ppb make it an important greenhouse gases (IPCC, 2014) contributing 20% to anthropogenic greenhouse effect (Cheng-Fang et al., 2012). Greenhouse effect (GHE) in the atmosphere plays a vital role in existence of life on earth as it prominently influences the temperature regime of many ecosystems including rice (Oryza sativa L.) ecosystem. Masters and Ela (2010) reported that the mean temperature of earth would be ‐19 °C without GHE, which would be limiting factor for life existences on earth. Most of the vital activities such as physiochemical reaction in plants are controlled by the temperature, which vary with ecosystems. The global earth surface temperature has increased by 0.88 °C due to enhanced GHE in the late nineteenth century (ChengFang et al., 2012). IPCC (2013) projected 1.5 to 4.5 °C rise in global

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mean annual temperature by the end of twenty-first century.CH4 is second most potent greenhouse gas on the basis of global warming potential (a quantification of the averaged relative radiative forcing impacts of a particular GHG as set 1 for CO2). In the duration of last two decades different scientific reports reveal different global warming potential (GWP) of CH4 which range from 15 to 34 (Table 1) as compared to CO2. Atmospheric concentration of CH4 has increased from a preindustrial 715 to 1774 ppb (Khosa et al., 2011).

Fig. 1. a. Methane tetrahedral geometry shape. b. Ammonium ion tetrahedral geometry shape.

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Table 1 Global warming potential (GWP) of methane on 100 year's time horizon. GWP

Reference

15 21 23 25 28 31 34

Bronson and Mosier (1994) Majumdar (2003); Karakurt et al. (2012) Lascano and Cardenas (2010) Nazaries et al. (2013); Kim et al. (2014a); Maris et al. (2015) Ghosh et al. (2015); Finn et al. (2015) Yamulki (2006) Wang et al. (2015); Gupta et al. (2015)

ecosystem is considered as a sources of CH4 (Toriyama et al., 2005). When the balance between production and consumption is negative, it is considered as CH4 sink such as upland rice. Other than the soil regimes, atmosphere is also the primary sink of CH4 (Prinn, 2003). Primary sinks of CH4 in the atmosphere are hydroxyl radical (OH) and (Cl−1) (Prinn, 2003; Prinn et al., 1995) and OH radical removes about 90% of total emitted tropospheric CH4 (Prinn, 2003). In the atmosphere OH and Cl− radicals remove CH4 respectively as follows (Masters and Ela, 2010 and Le Mer and Roger, 2001): CH4 + OH + 9O2 → CO2 + 0.5 H2 + 2H2O + 5O3

CH4 concentration has been increasing at the rate of 0.5–1% per year on an average (Tamai et al., 2007). Whalen (2005) estimated the cumulative annual CH4 emission at approximately 600 Tg CH4 yr−1 (anthropogenic and natural sources), of which 20% was contributed by rice fields. Out of total atmospheric CH4 about 70–80% is biogenic (Jhala et al., 2014). The total anthropogenic GHGs emissions rose from 27 to 49 gigatones (Gt) CO2 equivalents in four decades (1970 to 2010) at global scenario (Fig. 2a). From 2000 to 2010 GHGs emissions grew on an average by 2.2% per year as compared to 1.3% per year over the entire period from 1970 to 2000 (IPCC, 2014). IPCC (2014) reported that CH4 contributed 16% to total anthropogenic GHG emission in 2010 (Fig. 2b). Agriculture sector alone contributes more than half (50.63%) of the anthropogenic CH4 emissions at the global level (Fig. 2c) out of which rice paddy fields contribute about 20% (Ke et al., 2014). Rice is an artificial managed ecosystem and is cultivated in four different water regimes. The irrigated rice ecosystems (51%) have complete control of the water regime; rainfed rice ecosystem (27%) can be floodprone or drought-prone; upland rice ecosystem (11%) which have no standing water and deepwater rice ecosystems (10%) are characterized by intense inundation (Wassmann et al. 2000b) at the global level. About 80% of the rice is grown under flooded condition in Asia (Toriyama et al. 2005). Rice can be grown successfully in saturated water without no standing water (such as in direct seeded rice). Generally 5–10 cm standing water is considered best for paddy growth (Tuong and Bouman, 2003) but this standing water creates anaerobic environment which favors the CH4 production (Lo et al., 2016). Whenever in any ecosystem there is a positive balance between production of CH4 by methanogenic bacteria and consumption by methanotrophic bacteria that kind of

CH4 + Cl− → HCl + CH3 Apart from hydroxyl radical, methanotrophs (CH4 oxidation bacteria) which are present in rhizospheric zone and upper aerobic surface layer of rice fields are the biological sink for CH4 (Bodelier et al., 2000). About 60–80% of the CH4 emitted during a paddy growing season may be oxidized by methanotrophs before it reaches the atmosphere (Singh et al., 2010).These bacteria are aerobic, gram-negative that use CH4 as C (carbon)/energy sources (Bodelier et al., 2000) and assimilate it into cellular biomass and convert CH4 into CO2. Therefore understanding of factors responsible for production and consumption of methane may help in formulating methane mitigation strategies from the rice fields.The objective of this paper is to review information on CH4 life cycle including production, oxidation, emission, and its measurement in different rice ecosystems along with the different factors contributing to CH4 mitigation CH4 in rice. 2. Production of methane in rice soil Under anaerobic condition of flooded rice ecosystem, CH4 is produced due to bacterial degradation of complex organic matter (Penning and Conrad, 2007). This process is known as methanogenesis and the bacteria/archaea involved are known as methanogens. The weeds (terrestrial and aquatic), roots of weed and rice, rhizodeposition by weeds and rice, algal biomass, litter of rice plants, rice stubbles, microbial biomass, aquatic animals and organic fertilizers are the sources of complex organic matters (Kimura et al., 2004; Lu et al. 2003; Conrad, 2002; Kuzyakov and Domanski, 2000; Kimura, 2000; Liesack

Fig. 2. a — Total annual anthropogenic GHGs emissions at global level from 1970 to 2010 (IPCC, 2014), b — percentage contribution of various anthropogenic GHG emissions at global level in 2010 (IPCC, 2014), c — contributions of various sectors in global CH4 emissions (Karakurt et al., 2012). ⁎FOLU — forestry and other land use; F — fluorinated gases.


877

Fig. 3. The amounts of organic matter supplied annually to the paddy field (Source: Kimura et al., 2004).

et al., 2000; Brune et al., 2000). The annual input of different organic matter in a rice field is given in Fig. 3. This organic matter is converted into the first preferred food form (acetate) or alcohols (preferred after acetate) which is readily available to the methanogens as a direct food (Dubey, 2005) through the following processes.

Conrad, 2011). The temperature of rice fields lie in this range across all geographical region globally.

2.1. Hydrolysis

Methanogenesis is an anaerobic process (Thauer, 1998). In this process, methanogens use carbon from formic acid (formate), methanol, methylamines, dimethyl sulfide, methanethiol, acetate, alcohols, methylated sulfides, CO2/H2) as substrates for the production of CH4 (Nazaries et al., 2013; Dubey, 2005; Le Mer and Roger, 2001).The acetate or CO2/H2 is the immediate precursor for methanogenesis in rice soils (Mitra et al., 2012). Methanogenesis is initiated due to reduction of nonmethanogenic electron acceptor (oxygen, nitrate, manganese (IV), iron (III) and sulfate) and change in thermodynamic condition (Conrad, 1996).

The organic matter in rice fields are composed of humus (biodegradable resistant) and humic (non-biodegradable) components. The humus is a mixture of particulate matter and and water soluble substances. Particulate matter (cellulose, hemicelluloses, lignins and proteins) directly come from the biotic components and water soluble substances (amino acids, sugars and nucleotides come from either the degradation of the particulate matter by extracellular enzyme hydrolysis (Brune et al., 2000; Conrad, 1999, 2002; Kimura, 2000; Liesack et al., 2000) or rizodeposition (Kimura et al., 2004). Hydrolysis may take place in different environments like aerobic to strictly anaerobic (Kimura et al., 2004; Reddy et al., 2000). 2.2. Acidogensis During acidogensis the products of hydrolysis (monomers) are converted into volatile fatty acid (acetate, propionate, butyrate and lactate), ammonia, organic acids, alcohols (ethanol and methanol), hydrogen and carbon di-oxide (Cairo and Paris 1988). Monomers formed during hydrolysis are fermented into acids by fermentative bacteria. These fermentative bacteria can either be strictly anaerobic or may be facultative aerobic in nature. 2.3. Acetogenesis Acetogenesis is a biological reaction in which volatile fatty acids are converted into acetic acid, carbon dioxide and hydrogen by acetogens. Acetogens are obligatory anaerobic bacteria present in rice paddy soils (Rosencrantz et al., 1999). They use the reductive acetyl-CoA or Wood–Ljungdahl pathway (Matschiavelli et al., 2012) for synthesis of acetyl-CoA and cell carbon from CO2 (Muller et al., 2004; Drake et al., 1994). In this process, carbon dioxide is reduced to carbon monoxide by the enzymatic reaction of CO dehydrogenase and formic acid or directly into a formyl group, the formyl group is reduced to a methyl group and then combined with the carbon monoxide and Coenzyme A to produce acetyl-CoA by acetyl-CoA synthase (Lindahl, 2009; Ragsdale, 2006). Basically, acetogens support to enhance the biodegradation of organic compounds by coupling the oxidation of H2 to the reduction of CO2 to acetate (Ragsdale and Pierce, 2008). Acetate formation from the previous metabolites (acids) is done by homoacetogenic/ syntrophic bacteria with the temperature range of 15 to 50 °C (Liu and

2.4. Methanogenesis

3. Methanogens Methanogens are strictly anaerobic obligate (Conrad, 2007), belonging to the domain Archaea of phylum Euryarchaeota (Fazli et al., 2013). Methanogens are classified into three classes, six order, twelve families and thirty five genera (Table 2). Unique feature of all of the methanogens is to gain their energy by producing CH4 from simple substrates like formate, ethanol, acetate and H2 and CO2 (Conrad, 2007). Most of methanogens are mesophilic, able to produce CH4 in temperature ranging from 20 °C to 40 °C (Dubey, 2005). Few genera of methanogens can be found in extreme environments like as hypersaline sediments, hot springs and geothermal sediments where they may thrive at temperatures above 100 °C (Nazaries et al., 2013; Dubey, 2005). They depends on environmental conditions and other organisms for producing reduced condition and suitable substrate, therefore they can function only as members of a microbial community (SerranoSilva et al., 2014). On the basis of the substrate they utilize, methanogens are categorized into five groups (Table 3). Methanogens which mainly use acetate as a C source contribute about 80% to the CH4 production (Chin and Conrad, 1995) while other methanogens which use substrates like formate and H2/ CO2 contribute 10% to 30% (Palmer and Reeve, 1993). All methanogens use ammonium ion (NH+ 4 ) as nitrogen source, although the ability to fix molecular nitrogen and the nitrogen fixation gene (nif) is present in four orders of methanogens, i.e., Methanococcales, Methanomicrobiales, Methanobacteriales and Methanomicrobiales (Serrano-Silva et al., 2014; Dubey, 2005). Methanogens produce CH4 by methanogenesis, and this archaea require some unique coenzymes [ferredoxin (Fd), methanofuran (MFR), tetrahydromethanopterin (H4MPT), coenzyme (F420), coenzyme M (CoM) and coenzyme B (CoB)] to complete this multistep process (Nazaries et al., 2013).

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Table 2 Taxonomy of major methanogens. Domain: Archaea; Kingdom: Archaebacteria; Phylum: Euryarchaeota. Class

Oder

Family

Genus

Remark

Methanobacteria

Methanobacteriales

Methanobacteriaceae

Methanococci

Methanococcales

Methanothermaceae Methanococcaceae

Methanobacterium Methanobrevibacter Methanosphaera Methanothermobactera Methanothermusa Methanococcus Methanothermococcusa Methanocaldococcusa Methanotorrisa Methanomicrobium Methanoculleus Methanofollis Methanogenium Methanolacinia Methanoplanus Methanospirillum Methanocorpusculum Methanocalculus Methanoregula Methanolinae Methanosphaerula Methanocella Methanosarcina Methanococcoides Methanohalobiumb Methanohalophilusb Methanolobusb Methanomethylovorans Methanimicrococcus Methanosalsum Methanosaeta Methanopyrusa

Hyrogenotrophic , methylotrophic Hyrogenotrophic , methylotrophic Hyrogenotrophic , methylotrophic Hyrogenotrophic , methylotrophic Hyrogenotrophic , methylotrophic Hyrogenotrophic , methylotrophic Hyrogenotrophic , methylotrophic Hyrogenotrophic Hyrogenotrophic Hyrogenotrophic Hyrogenotrophic Hyrogenotrophic Hyrogenotrophic Hyrogenotrophic Hyrogenotrophic Hyrogenotrophic Hyrogenotrophic Hyrogenotrophic Hyrogenotrophic Hyrogenotrophic Hyrogenotrophic Hyrogenotrophic Aceticlastic, methylotrophic Aceticlastic, methylotrophic Aceticlastic, methylotrophic Aceticlastic, methylotrophic Methylotrophic Methylotrophic Methylotrophic Methylotrophic Aceticlastic Hyrogenotrophic

Methanocaldococcaceae Methanomicrobiales

Methanomicrobiaceae

Methanospirillaceae Methanocorpusculaceae Methanoregulaceae

Methanopyri

Methanocellales (RC-I)

Methanocellacaea

Methanosarcinales

Methanosarcinaceae

Methanopyrales

Methanosaetaceae Methanopyraceae

Source: Nazaries et al., 2013. a Extreme thermophiles: growth N80 °C. b Extreme halophiles: growth at 4.3 M NaCl.

atmosphere by achieving the threshold level of CH4 partial pressure in the rhizosphere (Denier van der Gon and Breemen, 1993).

4. Pathways of methane emission CH4 is present in the rice fields either as in the gas phase CH4 or as dissolved CH4 (Tokida et al., 2005). Strack and Waddington (2008) estimated that 33–88% of the total sub-surface CH4 is stored in the gasphase. The amount of dissolved CH4 is low due to its low solubility (17 mg/l) at 35 °C in water, and the lack of ionic form (Green, 2013). The regulation of total soil CH4 cycle is governed by the methanogens, methanotrophs and atmospheric-soil CH4 interactions. Generally there are three possible mechanisms for CH4 emission from soil to the atmosphere (Fig. 4).

4.2. Ebullition Ebullition is the process of transportation of methane in the form of bubbles (Green, 2013). This process may be steady or episodic (Rosenberry et al., 2006; Strack et al., 2005; Tokida et al., 2005). It is a faster process than diffusion and it take place when there is high

4.1. Diffusion Mobility of gas in the active layer is known as diffusion. It is a purely physical and slow process of CH4 emission and accounts for very less amount of total CH4 flux from soil due to its low solubility in water (Neue, 1993). The diffusion of CH4 is negligible in clay soil and highest in sandy soil due to differences in pore-space (Neue, 1993). In deepwater rice diffusion is active only in upper water column (Neue, 1993). Diffusion also limits the rate of plant-mediated CH4 transport to the

Table 3 Categorization of methanogenes on the basis of substrate utilization. Substrates

Product formed

Trophic group

4H2 + CO2 4HCOOH Acetate 4CH3OH CH3CHOHCH3 + CO2

CH4 + 2H2O CH4 + 3CO2 + 2H2O CH4 + CO2 3CH4 + CO2 + 2H2O CH4 + 4CH3CHOHCH3 + 2H2O

Hyrogenotrophs Formatotrophs Actetotrophs Methylotrophs Alcoholotrophs

Fig. 4. Flow diagram of methane production, oxidation and emission from rice fields.


production of CH4 particularly during the early period of rice growth and when there is high input of organic matter by different sources. CH4 loss as ebullition from rice soils is a significant and common mechanism; especially in clayey texture soil (IPCC, 1996). Ebullition was thought to contribute between 4 and 100% (seasonal dependency) of the emissions in a rice paddy study in Italy (Schvtz et al., 1989). Bosse and Frenzal (1998) in a rice paddy experiment found that in unplanted and planted microcosms, 85% and 50% of the CH4 was in the form of gas bubbles respectively. Butterbach-Bahl et al. (1997) found that about 10% of the seasonal CH4 emission emitted was attributable to ebullition in the first few weeks. Tokida et al. (2013) determined that a substantial total of the soil CH4 could be attributed to CH4 containing bubbles (i.e., 26–45% at panicle formation and 60–68% at the heading and grain filling stages) and that bubble volume was correlated with growth stage. Tokida et al. (2013) reported that ebullition is not only dependent on the gaseous-CH4 pool but also on the plant-mediated flux capacity. As ebullition is a very fast process for CH4 emission so there is very less or negligible chance for CH4 oxidation to take place. 4.3. Plant-mediated transport This is the primary biological process for CH4 emission in rice, through aerenchymatous tissue (Das and Baruah, 2008; Watanabe et al., 1994; Sass et al., 1990; Nouchi et al., 1990; Seiler et al., 1984; Cicerone et al., 1983). Aerenchyma is modified parenchymatous tissue having air vacuoles to adapt the plant in flooded environment and its main function is the transportation of oxygen for root respiration in rice (Armstrong, 1978; Jensen et al., 1967). Methane is also transported to the atmosphere from rhizosphere through these arenchymatous tissues in rice (Bont de et al., 1978) and this process contributes about 80– 90% of the total CH4 flux emitted to the atmosphere from the rice field (Setyanto et al., 2004; IPCC, 1996; Holzapfel-Pschorn and Seiler, 1986; Holzapfel-Pschorn et al., 1986). CH4 is released primarily through the micropores in the leaf sheath of the lower leaf position and released secondarily through the stomata in the leaf blade (Nouchi et al., 1990). However, Das and Baruah (2008) and Chanton et al. (1997), observed correlation with stomata density and CH4 emissions rates and linked the CH4 emission with transpiration. 5. Methane oxidation CH4 undergoes photochemical and chemical oxidation in the troposphere. Hydroxyl radical plays a crucial role in the oxidation of CH4 in the troposphere (Prinn, 2003). Photochemical oxidation of CH4 in the atmosphere is around 450 Tg y− 1, while biological oxidation at, or near, the production sites is about 700 Tg y−1 (Tate, 2015). However, biological oxidation is done by aerobic and anaerobic methanotrophs. An aerobic methanotrophic bacterium belongs to the Proteobacteria and further classified into two separate groups: Type I and Type II as in Table 4. Type I belongs to the Gammaproteobacteria, family Methylococcaceae and Type II belongs to Alphaproteobacteria, family Methylocystaceae (Conrad, 2007). CH4 oxidation can take place both in aerobic and anaerobic conditions (Nazaries et al., 2013). Methanotrophs generally use CH4 or methanol as a source of energy for their growth (Semrau et al., 2010; Hanson and Hanson, 1996). Aerobic methanotrophs bacteria (obligate methanotrophs) utilize only CH4 as C and energy source (Dedysh and Dunfield, 2011), while bacteria which grow on multi-carbon substrates are known as facultative methanotrophs (Dedysh and Dunfield, 2011). Availability of oxygen is the main limiting factor for aerobic methanotrophy (Bodegom et al., 2001). The majority of aerobic methanotrophs have mesophilic (maximum growth at 20 °C to 40 °C) and neutrophilic (maximum growth at pH 6 to 8) characteristics (Whittenbury et al., 1970). On the basis of affinity for CH4, methanotrophs are classified into two broad groups: high-affinity oxidation and low-affinity oxidation methanotrophs

879

(Nazaries et al., 2013). Methanotrophs which oxidize high concentrations of CH4 (N 100 ppm) are known as low- affinity methanotrophs, while the methanotrophs which have the ability to oxidize CH4 at low levels (1.8 ppm) are known as high-affinity methanotrophs (Bender and Conrad, 1992). The aerobic and anaerobic oxidations by methanotrophs are discussed below: 5.1. Aerobic methane oxidation In aerobic CH4 oxidation, CH4 is converted into CO2 by the sequential activity of the enzymes. In the first step, methane monooxygenase (MMO) enzyme converts CH4 into CH3CHO. CH3CHO is further oxidized to formaldehyde by methanol dehydrogenase, subsequently formaldehyde is oxidized to formate and finally to CO2.The processes of oxidation of CH4 to CO2 is as follows: Monoxygenase

Methanol

Formaldehyde

dehydrogenase

dehydrogenase

CH4 →CH3 CHO →HCHO →HCOOH → CO2 dehydrogenase

Methane monooxygenases (MMO) enzymes catalyze the process of aerobic oxidation of CH4. MMO are classified into two forms: particulate or membrane-bound form (pMMO) and soluble cytoplasmic form (sMMO) (Semrau et al., 2010). Both forms of MMO enzymes require oxygen for the oxidation process (Hakemain and Rosenzweig, 2007). The pMMO enzyme contains iron and copper, while sMMO is a cytoplasmic enzyme containing a unique di-iron site at its catalytic center (Chowdhary and Dick, 2013). The sMMO enzyme is capable of oxidizing wide range of aliphatics, aromatic and alkanes compounds (Colby et al., 1977). The pMMO is present in all methantrophs except Methyloferula and Methylomonas spp. (Vorobev et al., 2011). Methylomonas and Methyloferula species are facultative methanotrophs which use sMMO to grow on CH4. Apart from CH4 this species also grows on other multi-carbon compounds like acetate, ethanol, malate, succinate and pyruvate (Rahman et al. 2011). 5.2. Anaerobic methane oxidation The mechanism of anaerobic oxidation of CH4 (AOM) is carried out by physical association of anaerobic methanotrophic (ANME) Achaea and sulfate-reducing bacteria (SRB) (Nazaries et al., 2013; Serrano-Silva et al., 2014; Chowdhary and Dick 2013). The SRB oxidizes CH4 to CO2 (reversed methanogenesis) by using sulfate as electron acceptor (Caldwell et al., 2008; Thauer and Shima, 2008), so the process is also called sulfate-dependent CH4 oxidation. According to Ettwig et al. (2010), an anaerobic bacterium Methylomirabilis oxyfera, oxidize CH4 which is associated with reduction of nitrite to dinitrogen in pure culture. An unknown enzyme reduces nitric oxide directly to dinitrogen bypassing the formation of N2O (Serrano-Silva et al., 2014). Beal et al. (2009) reported that apart from sulfate and nitrite as electron acceptors, AOM was also found to be dependent on iron and manganese in marine environment. 6. Factors affecting methane production/oxidation CH4 emission in rice soil is a biologically-mediated phenomenon and depends up on the rate of two process (production and oxidation), which are opposite to each other and are controlled by the population of methanogens and methanotrophs in the system. Both of these are controlled by many interplaying factors like soil organic matter content (Das and Adhya, 2014; Zhang et al., 2012), soil pH (Oo et al., 2015; Chowdhary and Dick, 2013; Bharati et al., 2000a), texture of soil (Brye et al., 2013), redox potential of soil (Wang et al., 1993), fertilizers (Yang et al., 2015a; Serrano-Silva et al., 2014) and soil temperature (Schutz et al., 1990). CH4 emission processes are also affected by diurnal variation (Neue et al., 1997), seasonal variation (Datta et al. 2013b; Neue et al., 1997), elevated ozone (Zheng et al., 2011, Bhatia et al.,

880


Table 4 Taxonomy and some characteristics of aerobic methanotrophs. Source: Nazaries et al., 2013. Domain: bacteria/kingdom: eubacteria/phylum: proteobacteria TypeI/class: Gammaproteobacteria

Type II/class: Alphaproteobacteria

Order: Methylococcales/Family: Methylococcaceae Genus

Species

Methylobacter

Methylobacter bovis M. chroococcum M. luteus M. marinus M. psychrophilus M. tundripaludum M. vinelandii

Methylomicrobium

Methylomonas

Methylosarcina

Methylocaldum Methylothermus Methylococcus Methylogaea Crenothrix Clonothrix Methylosoma Methylosphaera Methylovulum Methylomarinum Methylohalobius a b c d e

Order: Rhizobiales/family: Methylocystaceae Remark

Psychrophilesb

Methylomicrobium album M. buryatense M. pelagicum M. agile M. rubra M. scandinavica M. paludis M. koyamae M. lacus, M. fibrate M. quisquiliarum M. gracile M. szegediense M. epidum M. hermalis M. subterraneus M. capsulatus M. thermophilus M. oryae C. polyspora C. fusca M. difficile M. hansonii M. miyakonense M. vadi M. crimeensis

Genus

Methylocystsi

Methylosinus

echinoides heyeri hirsute methanolicus minimus parvus pyriformis rosea bryophila sporium trichosporium

Remark Acidophilesa

Acidophiles

M. palustris M. silvestris M. tundra

Acidophiles Acidophiles Acidophiles

Methylocapsa

M. acidiphila M. aurea

Acidophiles Acidophiles

Methyloferula

M. stellata

Acidophiles

Methylocella Psychrophiles

Thermophilesc Thermophiles Thermophiles Thermophiles Thermophiles Thermophiles Thermophiles

Species M. M. M. M. M. M. M. M. M. M. M.

Halophilesd Psychrophiles Haloalkaliphilese

Acidophiles: growth at pH of 3.8–5.5. Psychrophiles: growth at 5–10 °C but not above 20 °C. Thermophiles: growth N45 °C. Halophiles: growth at 15% NaCl. Haloalkaliphiles: growth at 12% NaCl and at pH of 9–11.

2011) and elevated CO2 (Smith et al., 2010) etc. along with management practice such as rice cultivar (Gutierrez et al., 2013), nutrient application (Das and Adhya, 2014), water management (Liang et al. 2016) and application of pesticides (Jiang et al., 2015) (Table 5). 6.1. Soil organic matter Organic matter (C:N ratio) is an important factor affecting CH4 production in flooded rice soil. In rice cultivation, organic amendments are applied generally in the form of farmyard manure, straw, green manure such as sesbania etc. (Bhatia et al., 2005). Biochar application has also gained importance in the last few years (Kollah et al. 2015a; Parmar et al., 2014; Dong et al., 2013; Karhu et al. 2011) due to its carbon sequential potential (Riya et al., 2014; Khosa et al., 2010). In nonflooded rice, oxidation of organic matter (OM) leads to emission of carbon dioxide by aerobic respiration while under flooded conditions OM is fermented and results in CH4 emission. Organic matter acts as a C source and reduces soil Eh under anaerobic conditions (Ali et al., 2014; Bhattacharyya et al., 2012). Several studies have reported positive increase in CH4 emission after the addition of rice straw (Hou et al., 2013; Agnihotri et al., 1999; Bronson et al., 1997; Yagi and Minami, 1990), green manure (Bronson et al., 1997) and biofertilizer

(Agnihotri et al., 1999) in flooded rice condition. Application of nitrogenous fertilizer along with crop residue in flooded rice enhanced the CH4 emission (Yang et al., 2015a, Das and Adhya, 2014). Yagi and Minami (1990) observed that application of rice straw to rice fields increased methane emission rates by 2 to 4 times as compared to unamended control plots. Bronson et al. (1997) found that organic matter additions as straw (5.5 t ha− 1, dry) and green manure (12 t ha−1, wet) stimulated methane flux several folds. Agnihotri et al. (1999) observed that application of rice straw before flooding and the biofertilizers after flooding enhanced methane efflux from rice fields significantly, while, compost of cowdung and leaves did not stimulate methane production and rather, decreased methane fluxes. Sass et al. (1990) reported a linear relationship between plant biomass and methane emission. Biochar is a slow degrading OM as compared to other sources like crop straw, green manure; cattle manure compost etc. (Fischer and Glaser, 2012). A few recent studies have shown that application of biochar reduces CH4 emission (Zhang et al., 2010) (Table 6). Pandey et al. (2014) observed that biochar application reduced CH4 emission in rice as compared to farm yard manure (56.19 and 60.34%) and straw compost (41.77 and 44.44%) in alternate wetting and drying (AWD) and continuous flooding (CF) respectively. However, higher quantities of biochar application in rice increased CH4 emission


881

Table 5 A comparative evaluation of factors effecting methane emission in rice cultivation. Factors Organic matter content • Farm yard manure • Biochar • Straw compost • Green manure • Cattle manure compost Soil texture and mineralogy Soil pH Soil redox potential (Eh) Soil temperature Climatic factors

Impact on methane production and emission

References

Increases emission Decreases emission over direct straw application Enhances production and emission Increases emission Reduces emission CH4 production increased when the aggregate size of the soil increased The optimum pH for CH4 production was near neutrality Production increases with decrease in Eh (Maximum at Eh −250 mV) Maximum production at 30 °C of soil

Pandey et al. (2014) Feng et al. (2012) Sander et al. (2014) Haque et al. (2013) Pramanik and Kim. (2014) Jackel et al. (2000) Wang et al. (1993) Ali et al. (2008) Lu et al. (2015) Yang and Chang (1988)

CH4 production maximum at 37 oC of air • Temperature • Diurnal variation • Effect of elevated O3 • Effect of elevated CO2 Rice cultivar Method of rice transplanting

Time of transplanting Fertilizer • Urea • Nimin • DMPP • Tablet urea • Ammonium sulphate • Potassium nitrate • MOP • ECC • Thiosulphate • Sodium azide • Silicate • DCD • Hydroquinone • Azolla • Cyanobacteria Water regime management

Pesticide application Fish farming

Maximum production at 12:00 and minimum production at 18:00 Reduces emission (study in Open top chamber) No significant effect on CH4 emission Flux varies from cultivar to cultivar System of rice intensification(SRI) reduces methane emission Direct seeded rice (DSR) reduces methane emission Late transplanting of seedlings mitigate emission than early transplanting of seedlings Enhanced emission (52% more than no nitrogen) Reduces emission by 17% over urea Reduces emission compared to urea Reduces emission by 39% over urea Reduces emission by 21% over urea Enhanced emission Reduces emission by 49% as compared to control(no MOP applied) Reduces methane emission by 25% Enhanced emission by 5% than urea alone Reduces emission by 75% over amendment soil Reduces emission by 36% over control Higher emission compared to urea alone Increase emission by 12% than urea alone Reported to have both increased (Ying et al., 2000) and decreases (Nungkat et al., 2015) emission than control. Reduces production Several water management options like alternate wetting and drying, mid-season drying, controlled irrigation etc. have been reported to minimize CH4 emission as compared with continuous flooded rice Butachlor reduces emission from 15 to 98% than control Enhanced emission by 26% in Fish-rice farming as compared to rice cultivation alone

Zhang et al. (2015) Bhatia et al. (2011) Tokida et al. (2010) Mitra et al. (1999), Jain et al. (2000) Jain et al. (2014) Suryavanshi et al. (2013) Bhatia et al. (2013) Ahmad et al. (2009) Nayak et al. (2006) Ghosh et al. (2003) Rath et al. (1999) Weiske et al. (2001) Wassmann et al. (2000a) Ali et al. (2012) Liou et al. (2003) Babu et al. (2006) Linquist et al. (2012) Malla et al. (2005) Bharati et al. (2000b) Ali et al. (2009b) Datta and Adhya (2014) Malla et al. (2005) Ying et al. (2000) Nungkat et al. (2015) Prasanna et al. (2002) Hussain et al. (2015)

Mohanty et al. (2004) Bhattacharyya et al. (2013)

DMPP-3,4-dimethylpyrazole phosphate; MOP — muriate of potash; ECC — encapsulated calcium carbide; DCD — dicyandiamide.

(Zhang et al., 2012). Beside this, composted manure also reduced CH4 emission by 50% as compared to air dried manure (Kim et al. 2014b). The biogas spent slurry application along with urea (22 kg ha−1) reduced the CH4 emission as compared to farmyard along with urea (49.44 kg ha−1) from rice soil (Debnath et al., 1996). 6.2. pH and soil texture Soil pH plays an important role in methane production with maximum production rates at neutral pH conditions (Pathak et al., 2008; Dunfield et al., 2003; Wang et al., 1993). Methanogens are usually more active in neutral (pH = 6.5–7.5) or slightly alkaline (range) soil and very sensitive to fluctuations in soil pH (IPCC, 1996, Wang et al., 1993). CH4 production above pH 8.8 and below 5.8 in the soil is almost completely inhibited (Pathak et al., 2008). The pH of a flooded soil is usually close to 7.0 regardless of its initial level and thus flooded rice field offer suitable condition for CH4 production (Wassmann et al. 1998). However, optimum pH for CH4 oxidation ranges from 5.0 to 6.5 in pure culture (Le Mer et al., 1996). There are reports of CH4 oxidation at low pH (2) (Islam et al., 2008) and high pH (9.5) (Saari et al. 2004). In soils, with pH b5.0, negligible CH4 oxidation activity has been reported (Chan and Parkin, 2001). Porous coarse sandy soil has been reported to have a higher capacity for CH4 oxidation (10.4 mol of CH4 m−2 day−1) (Kightley et al., 1995).

Type of soil also influences CH4 production. Oxisols, most of the Ultisols, some of the Aridisols, Entisols and Inceptisols are less favorable to methane production when flooded, while Alfisols, Vertisols, and Mollisols are prone to methane production. Methane production in 10 wetland rice soils of Philippines was influenced by the the presence of labile organic substrates and reduction characteristics of the soils (Gaunt et al., 1997). Different paddy soils, respectively, Peat soil, Gley soil, Humic Andosol, and Light-colored Andosol) under similar climatic regions have been reported to emit about 44.8, 27.0, 9.8, and 1.1 g/m2 methane annually (Yagi and Minami, 1990). The higher emission rates from the Peat and Gley soils may be due to the lower percolation rates observed in these soils. Yagi et al. (1998) showed that with increased percolation rates, seasonal methane emission decreased. Inubushi et al., (1992) reported up to 58% reduction in methane emission by increasing percolation rates from essentially zero to approximately 4 mm d−1. Soil texture (percent composition of sand, slit and clay in soil) also inluenced CH4 emission (Le Mer and Roger, 2001), however, reported results are not consistent (Table 7). Neue and Sass (1994) reported higher methane emission from sandy soil as compared to clayey soil. Higher emission of methane from sandy soil has been mainly reported due to poor entrapment of methane in sandy soil as compared to clayey soil (Wang et al., 1993). It may also depend on soil organic C content and the soil redox potential (Hussain et al., 2015). Sass et al. (1994), reported a

882


Table 6 Effect of organic matter incorporation in soil on methane emission from rice soil. Location

Treatment (kg N ha−1)

CH4 emission (kg ha−1)

References

China

Control (0) Urea (240) Urea (120) + pig manure compost (120) Urea ( 219.6) + wheat straw (20.4) Urea (99.6) + Straw (20.4) + pig maure compost (120) Urea (219.6) + straw (20.4) + straw decomposing inoculants (20.7)

85.5 109.1 131.7 271.0 167.2

Yang et al. (2015a)

India

Control (0) Urea (120) Urea (30) + compost (30) Urea (30) + rice straw (30) Urea (30) + poultry manure (30) Urea (220) + rice straw compost (2 t ha−1) Urea (170) + rice straw compost (2 t ha−1) + silicate (300 kg ha−1) Urea(170+ sesbania biomass (2 t ha−1) + silicate(300 kg ha−1) Urea (170)+ Azolla anabaena (2 t ha−1) + (15 kg BGA) + silicate (300 kg ha−1) Urea (170) + cattle manure compost (2 t ha−1) + silicate (300 kg ha−1) Urea (100) + farm yard manure (10 t ha−1) Urea (100) + straw compost (11.21 t ha−1) Urea (100) + biocahr (6.67 t ha−1) Urea (0) + green manure (0 t ha−1) Urea (0) + green manure (9 t ha−1) Urea (0) + green manure (18 t ha−1) Urea (0) + green manure (27 t ha−1) Urea (0) + green manure (36 t ha−1) Control (0) Urea (110) Urea (55)+ Dhaincha (5 t ha-1) Urea (62) + Morning glory(5 t ha−1) Urea (62) + Farmyard manure(5 t ha−1 Urea super granule (40 kg N ha−1) Urea (300) + bio-char (0 t ha−1) Urea (300) + bio-char (10 t ha−1) Urea (300) + bio-char (20 t ha−1) Urea (300) + bio-char (40 t ha−1) Urea (120) Urea (0) + green manure (20 t ha−1) Urea (0) + rice straw compost (10 t ha−1) Urea (0) + farmyard manure (20 t ha−1) Urea (80) Urea (80) + rice straw (1.05 t ha−1) Urea (81) + rice straw (2.19 t ha−1) Urea (0) Urea (120) Urea (90) + FYM (30) Urea (90) + GM (30) Urea (120) + wheat straw (2 t ha−1) Urea (0) + FYM (60) + bioferlizer (30) + wheat straw (30) Urea (0) Urea (60) Azolla (30) + urea (30) Urea (0) + horse dung (3.75 tons ha−1) Urea (0) + horse dung (7.5 tons ha−1) Urea (0) + (148.5 kg of (NH4)HCO3 ha −1) Urea (40) Urea (40) + rice straw (6 tons ha−1) Urea (40) + wheat straw (6 tons ha−1)

Bangladesh

Vietnam

South Korea

India

China

India

Japan

India

Indian

China

Japan

strong linear correlation between seasonal methane emission and the percentage of sand in a sand:clay:silt gradient in Vertisols. Clayey soils may form cracks on drying, and facilitates the release of entrapped CH4 into the atmosphere (Inubushi et al., 1990). Wagner et al. (1999) reported rates of CH4 production in the following sequence: sand b gravel b clayey slit b clay. Thus production might be more in clay soil due to more reduced potential, however, due to higher entrapment of methane in pore space may led to lower emission into the atmosphere. Researchers in different countries have reported CH4 emissions in the range of 153 to 285 kg ha−1, 108 to 441 kg ha−1, 113 to 246.22 kg ha− 1 and 23 to 146 kg ha− 1 from clay loam, silt loam, sandy clay loam and sandy loam soils respectively (Table 7). On comparing, we did not observe any relation between soil texture and

223.7 113.4 149.6 187.2 207.2 185.3 124.78 118.6 121.37 113.60 117.3 353 252 140 205 367 961 1268 1466 139.22 190.55231.87 142.29 258.74 310.17 69.3 67.2 175.1 104.9 21.5 85.6 36.9 113.0 40.4 90.9 408.0 35.1 35.9 49.6 46.0 42.7 57.1 94.9 155.3 149.4 748.4 1098.8 400.8 216.0 758.7 734.7

Das and Adhya (2014)

Ali et al. (2014)

Pandey et al. (2014)

Haque et al. (2013)

Datta et al. (2013b)

Zhang et al. (2012)

Khosa et al. (2010)

Naser et al. (2007)

Bhatia et al. (2005)

Bharati et al. (2000b)

Wang et al. (1999)

Chidthaisong et al. (1996)

methane emission among these studies as the soils in different experiments varied not only in soil organic matter content but also the water management was different. 6.3. Soil redox potential (Eh) Soil redox potential is one of the most critical factors for production of methane. For initiation of methane production, the redox potential of soil must be between -100mv to -200mv (Dubey, 2005; Wang et al., 1993; Yagi and Minami, 1990). The low land flooded rice field provides favorable redox potential for methane production. After flooding, the soil Eh decreases sharply upto − 150 mv in 10–21 days in rice field and fluctuates between − 150 to 450 mv through out the growing


883

Table 7 Methane emissions under different soil texture and organic matter contents of soil. Study location

Texture

Water condition

OC (g kg−1)

CH4 (kg ha−1)

References

China Korea Republic Bangladesh Myanmar China Vietnam Bangladesh Korea Republic Korea Republic Myanmar India India India India Japan Japan Indonesia India India India India China China India India

Clay loam Clay loam Clay loam Clay loam Silty clay Slit loam Slit loam Silt loam Silt loam Alluvial soil Alluvial soil Sandy clay loam Sandy clay loam Sandy clay loam Sandy loam Sandy loam Sandy loam Sandy loam Sandy loam Sandy loam Sandy loam Sandy loam Sandy loam Sandy loam Loam

CF IF IR CF CF CF CF CF CF CF CF CF CF CF IR CF CF SC IF CF IF IF IF IF IF

41.34⁎ 39.6 17.8 5.1 18.29 12.55 39.6⁎ 20.4⁎

153.5 163 158 285 440.9 108 124.0 205.0 390 280 18.61 246.22 113.39 125.34 146 140 1845.34 22.59 30.72 32.33 35.1 294 207.87 21.5 14.1

Liang et al. (2016) Ali et al. (2015) Ali et al. (2015) Oo et al. (2015) Ahmad et al. (2009) Pandey et al. (2014) Ali et al. (2013) Haque et al. (2013) Lee et al. (2010) Oo et al. (2015) Adhya et al. (2000) Datta and Adhya (2014) Das and Adhya (2014) Babu et al. (2006) Ali et al. (2015) Riya et al. (2014) Hadi et al. (2010) Jain et al. (2014) Bhatia et al. (2013) Suryavanshi et al. (2013) Bhatia et al. (2005) Dong et al. (2011) Yao et al. (2012) Khosa et al. (2010) Pathak et al. (2003)

23.4 5.1 8.6 9.0 6.6 6.6 36.8 9.0 23.7 5.0 4.9 5.6 5.9 18.4 18.4 6.9 4.5

OC — organic carbon;⁎ — organic matter of soil; SC — saturated condition; IF — intermittent flooding; CF — continuous flooding.

season (Oo et al., 2015; Ali et al., 2014; Babu et al., 2006; Yagi and Minami, 1990). Development of such a low Eh is due to intensive anoxic condition caused by continuous flooding of soil (Ali et al. 2009a). Labile organic carbon and low availability of active-Fe also helps in attaining lower Eh (− 200 to -300 mV) after submergence of soil (Neue and Roger, 1994). Availability of iron oxide increases soil redox potential (Ali et al., 2014, 2015).The active iron acts as electron acceptor which suppresses the activity of methanogens resulting in reduction of CH4 production in soil (Ali et al., 2012, 2013 and Jackel and Schnell, 2000). After flooding of soil redox potential deceases sharply due to decomposition of the organic matter applied in rice field. (Ali et al., 2014). Soil redox potential deceases sharply after flooding (Takai et al., 1956). In Indian rice growing soil Babu et al. (2006) reported that under continuously flooding conditions Eh drops sharply to -155 mV at 10 days after transplanting (DAT) and it further reduced to − 287 mV after 30 DAT. Eh then almost became stable between 40 and 80 DAT and was observed to be in the range of − 213 to − 256 mV, it subsequently increased sharply after 80 DAT to −140 mV. In Bangladesh under continuously flooding in rice Ali et al. (2014) reported that Eh deceased up to −150 mV after 21 DAT and further reduced to −250 mV between flowering to heading stage (91 to 98 DAT) resulting in maximum CH4 emission. The Eh declined after flooding and fluctuated between −150 and −450 mV in low land rice throughout the growing season in Myanmar (Oo et al., 2015). In Japanese rice soil Yagi and Minami (1990) observed that the soil Eh at 5 cm depth dropped slowly after flooding and reached approximately −150 mV at the heading stage in rice. The low Eh led to higher CH4 production and the soil Eh status was not affected by changing the surface water depth during the crop growth period in continuously flooded rice (Oo et al., 2015; Gaihre et al., 2011). 6.4. Oxygen availability Availability of oxygen in soil profile is major limiting factor, which controls the dynamics of methanogens and methanotrophs dominant population (Bender and Conrad, 1993). With an increase in oxygen availability, oxidation of methane by methanotrops has been reported to increase, resulting in low methane emission. Presence of oxygen increases the thickness of the oxidizing layer and the reduction of carbon

into CH4 gets suspended due to inactivity of methanogens (Bender and Conrad, 1993, 1994, 1995). Further, methanotrophs increases the CH4 oxidation in soil (Kightley et al., 1995). The availability of oxygen in flooded rice field is influenced by several factors like soil texture, availability of light, photosynthetic aquatic plants and rice cultivars. Wassmann and Aulakh (2000) reported that the CH4 oxidation in paddy fields is localized near surface aerobic layer and in the rhizosphere. In rhizosphere, the concentration gradients of O2 and CH4 overlap. Aerenchymal transportation of O2 from atmosphere to rhizosphere enhances the process of CH4 oxidation in rice soil. As the soil porosity increases more O2 diffusion occurs, while increased water content reduces O2 diffusion into the soil (Dubey, 2005). In completely flooded rice soil, oxygen never penetrated N 3–6 mm from floodwater soil boundary layer (Liesack et al., 2000), however, Frenzel et al. (1992) detected dissolved oxygen at 40 mm depth in rice field. The oxygen concentration in soil was higher during day (N 1 mm deeper into soil profile) than night (1 mm deeper into soil profile) (Hanson and Hanson, 1996, Liesack et al., 2000). The rate of CH4 oxidation is also affected directly and indirectly by the concentration of CH4 itself. Bender and Conrad (1995) reported that the enhanced concentration of CH4 increases the rate of CH4 oxidation due to increases in population of methanotrophs. Born et al. (1990) reported that the threshold concentration below which no CH4 oxidation occurs is much greater for sediments (2–3 ppm) than soils (b 0.1–0.4 ppm). The highest rates of CH4 oxidation occurred, when the vertical profiles of CH4 and oxygen overlapped. 6.5. Soil temperature Temperature is one of the most important factors controlling the methane production by influencing the methanogenic and methanotrophic activity (Lu et al., 2015; Luo et al., 2013; Mohanty et al., 2007; Schrope et al., 1999; Winfrey and Zeikus, 1979). The soil temperature influences methane production by affecting methanogenic activities and oxidation of soil organic matter (Peng et al., 2008). CH4 production increases exponentially as soil temperature of paddy soil increases (Conrad, 1996). In anaerobic zones of rice soils, methane formation starts at 15 to 20 °C (Nozhevnikova et al., 2007), however, the reported value of optimum temperature for CH4 production ranges from 25 °C to 40 °C

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depending on climate and soil of different parts of the world (Chen et al., 2015; Yang et al., 2015b; Hattori et al., 2001; Yagi et al., 1997; Neue and Scharpenseel, 1984). Reports suggest that methane emission increases from 4 °C to a maximum at 37 °C (Yang and Chang, 1998), while methanogenesis dramatically decreases below 10 °C to 15 °C and is arrested above 60 °C (Pacey and Gier, 1986). Furthermore, Lu et al. (2015) reported that different mathanogenic archaea is responsible for CH4 production in soil at different temperatures. Schutz et al. (1990) found a significant correlation between the diel changes in CH4 flux and temperature at a particular soil depth. At low temperature (20 °C) acetoclastic methanosaetaceae archea were responsible for CH4 production and at high temperature (45 °C) hydrogenotrophic methanogens play a significant role in CH4 production (Chen et al., 2015). The oxidation of methane is also highly influenced by temperature (Borken and Beese 2006; Le Mer and Roger, 2001). The optimum conditions for aerobic oxidation of methane ranged from 25 to 35 °C in paddy rice soil (Mohanty et al., 2007; Min et al. 2002). Although most of the CH4 oxidizing bacteria are mesophilic, some bacteria (thermoacidiophilic) have also been reported to even oxidize methane at 55 °C (Islam et al., 2008). Populations of methonotrophs type II bacteria decreases as the temperature of soil increases and it directly reduce CH4 oxidation. Under future climate change scenarios, there may be an increase in mean surface air temperature (IPCC, 2013), however, there are no studies on the effect of increasing air temperatures on methane oxidation and on the oxidative capacity of methanotrophic bacteria.

fertilization, etc. (Pathak et al., 2008). Studies suggest, higher methane emission at the beginning of the growing season in rice with decreasing trend as the season progressed, reaching a minimum at the middle of the season; and then it increased again over the reproductive stages (Tokida et al., 2014). No diurnal variation during decreasing methane emission trend has also been reported; however, generally more CH4 emission occurs during the day time than during night. Datta et al. (2013b) also reported variation in cumulative CH4 emission between two seasons (wet and dry) in Cuttack, India with seasonal differences in CH4 flux of about 108.52 kg CH4 ha− 1 in control, 150.37 kg CH4 ha−1 in prilled Urea, 30.11 kg CH4 ha−1 in Dhaincha (Sesbania aculeate), 96.73 kg CH4 ha−1 in Morning glory (Ipomoea lacunose), 91.30 kg CH4 ha−1 in farmyard manure and 217.03 kg CH4 ha−1 in Urea super granules . CH4 oxidation rate showed seasonal variations along with the growth stage of rice plants: high rates until the panicle initiation stage and negligibly or small rate at the ripening stage (Kruger et al., 2001). Seasonal variations were attributed to the limitation of inorganic nitrogen for methanotrophs in the rhizosphere especially in the later stages of rice growth which was in contrast to the variation at the oxic surface soil (Conrad and Rothfuss, 1991). Meijide et al. (2011) reported that CH4 flux sharply increases as water table rise, with highest methane flux when water table was above 10–12 cm. Yagi et al., 1996 observed a large flush of CH4 (about 7% of the total CH4) just after drainage in intermittently drained plots and final drainage in continuously flooded plots followed by rapid decrease during the drained period.

6.6. Plant growth stage 6.8. Effect of elevated CO2 concentration The CH4 production/oxidation is also influenced by the growth stage of the rice plants. At transplanting when plant is just in acclimatization phase and flooding is recently done, the CH4 emission is low, due to the less activity of methanogens (Conrad, 2007). With the growth of the plant, CH4 production increases due to fermentation of easily degradable soil OM and anaerobic conditions for methanogenesis in the flooded rice soil (Li et al., 2011). Generally, highest peak of methane has been reported around the tillering stage in rice by Bhattacharya et al. (2014) and Suryavanshi et al. (2013) in India, Miyata et al. (2000) in Japan; Alberto et al. (2014) in Pillippines. It has been attributed to microbial decomposition of rizodeposition, root exudates and other carbon inputs such as algal biomass, microbial biomass which has been observed to be maximum during the tillering stage (Holzapfel-Pschorn et al., 1986; Mitra et al., 1999; Kimura et al., 2004; Tokida et al., 2010; Suryavanshi et al., 2013). However, Tokida et al. (2010) observed highest methane peak at the heading (70 DAT) to early grain-filling stages and Singh et al. (1998) and Inubushi et al. (2003) observed the peak of CH4 flux at flowering stage (about 80 DAT). The highest CH4 emission during maximum tillering to panicle initiation was also observed by Meijide et al. (2011), due to the higher methanogensis and available soil labile carbon. 6.7. Diurnal and seasonal variation Emission rates of CH4 generally show strong diurnal and seasonal variations. The CH4 emission increases rapidly after sunrise, peaking around noon (11 A.M. to 1 P.M.) (Kumar and Viyol, 2009). The diurnal mean CH4 concentration in tropical rice was observed to be in the range of 1.7–2.6 μmol/mol by Bhattacharya et al. (2014). The highest peak (5.72 mg CH4 m−2 h−1) was observed at maximum tillerging to panicle initiation stage in wet season while in dry season maximum peak (5.23 mg CH4 m−2 h−1) was observed during panicle initiation to the flowering stage (Bhattacharya et al., 2014). The seasonal variations in CH4 emissions depends on factors like water management (Hou et al. 2012; Yagi et al., 1996), soil temperature (Zou et al., 2005), solar radiation, growing stage (Bhattacharya et al., 2014; Alberto et al., 2014; Guo and Zhou, 2007), humidity, day-length

Studied show substantial increase in CH4 emission under elevated CO2 condition (Lou et al. 2008; Cheng et al. 2006 and 2008; Xu et al., 2004; Ziska et al., 1998; Inubushi et al., 2003; Allen et al., 2003). Allen et al. (2003) reported about 50%–100% increase in CH4 emission under ambient + 300 μmol mol− 1 elevated CO2 in open-top chambers. While, Xu et al. (2004) observed up to 200% enhancement in seasonal CH4 emission in free air CO2 enrichment system (FACE) under ambient + 200 μmol mol−1 elevated CO2. Tokida et al. (2010) did not observe any significant increase in CH4 emissions under similar elevated CO2 conditions; however with an increase in soil temperature (2 °C), the increase in CH4 emission was significant. The higher methane emission under elevated CO2 condition may be attributed to (a) suppression of methanotrophs and promotion of methanogenesis in the rice fields (Okubo et al., 2015), (b) increase in the number of tillers (Seneweera, 2011; Inubushi et al., 2003; Yagi et al., 2000), (c) enlargement of aerenchymatous cell/tissue (Kim et al. 2003, 2001), (d) increase in the supply of organic matter or rhizodeposition in soil due to higher photosysnthesis (Prior et al., 2011; Toriyama et al., 2005; Inubushi et al., 2003; Rogers et al., 1996), (e) Stimulation of root growth (Lou et al. (2008), (f) Higher population of methanogens and methanotrophs in the upper soil layer (0-1 cm) under elevated CO2 than ambient CO2 condition (Inubushi et al., 2003), and (g) elevation in temperature (Allen et al., 2003; Ziska et al., 1998). Increases in the number of tiller from 14 (300 ppm CO2) to 21 (700 ppm) and root mass per tiller from 0.15 g (300 ppm) to 0.28 g (700 ppm) has been reported under elevated CO2 condition (Seneweera, 2011). Increase in number of tillers helps in the transportation of CH4 from soil to atmosphere resuting into higher methane emission (Inubushi et al., 2003; Cheng et al., 2003). Tokida et al. (2010) reported about 80% enhancement in total CH4 seasonal emissions by the additive effects of elevated CO2 and temperature. Elevated CO2 concentration increases photosynthesis (Prior et al., 2011) of the crop which eventually supplies carbon from the roots to the soil (Rogers et al., 1996), which in turn is used as a substrate for carbon reduction and CH4 production under anaerobic conditions (Rogers et al., 1996). Under elevated CO2, temperature of the system also increased


stimulating the microbial activity in submerged soils, leading to a higher rate of CH4 production (Fey and Conrad 2000). Soil warming increased the seasonal CH4 emission by about 44% (Tokida et al., 2010). The stimulatory effect of atmospheric CO2 enrichment upon CH4 emissions also depends on factors like nitrogen supply. A positive correlation has been reported between methane emission and nitrogen addition rate under long term atmospheric CO2 enrichment in paddy rice ecosystem. However, the impact has been observed to be negative with addition rates of decomposable organic carbon (Zheng et al., 2006). Low soil nitrogen availability counter acts the stimulatory effect of elevated CO2 upon CH4 emission from nitrogen-poor paddy rice ecosystems (Zheng et al., 2006). The simulatory effect of high soil nitrogen availability on CH4 emission under elevated CO2 has mainly been attributed to (a) enhancement of plant growth and nitrogen uptake, and (b) reduction in C:N ratio of plant residue leading to higher decomposition rates. Schrope et al. (1999) reported a negative impact of high CO2 on CH4 emission, despite a substantial increase in root (up to 83%) and above-ground dry weight (up to 35%). Improved O 2 supply to below-ground parts through extensive root system of the plant under elevated CO 2 , resulted in suppression of CH4 production in the vicinity of the roots. Elevated CO2 has no net effect on CH4 oxidation activity (Toriyama et al., 2005). However, Schrope et al. (1999) stated that the increased root biomass aerates soil effectively and suppress CH4 production under elevated CO2 condition. The cultivars, soil types, water; nitrogen and residue management can also influence the CH4 production/oxidation under elevated CO2 condition. Under elevated CO2 (550 μmol mol−1), the CH4 emissions from the rice fields increased significantly, by 38% and 51% in 1999 and 2000 respectively (Cheng et al., 2006). Allen et al. (2003) observed CH4 emissions in high-CO2, hightemperature treatments with a sustained maximum efflux density of 7 mg −2 h−1 and 0.17 g m−2 d −1 near the end of the growing season. Total seasonal CH4 emission was observed four times higher under elevated CO2-high temperature than ambient CO2 low-temperature treatment (Allen et al., 2003). However, how elevated CO2 can increase CH4 emissions in initial period has not been established clearly? That may be due to a strongly close association between metabolism of plant and microbial activity; thereby newly formed photosynthetic product is readily available for fermentation through root exudation (Huang et al., 1998). The increased CH4 emissions in most herbaceous species were explained by an increase in photosynthesis in many studies (Ziska et al., 1998; Hutchin et al., 1995; Dacey et al., 1994). 6.9. Rice cultivar There are significant variations in quantity of CH4 emissions from soils due to different rice cultivars. Various field studies (Kumar and Viyol, 2009; Aulakh et al., 2000; Mitra et al., 1999; Adhya et al. 1994) have indicated substantial differences in the rate of CH4 emission among different rice cultivars. Wang et al. (1997a) reported that this variation in CH4 emissions from paddy soils is due to differences in amounts of root exudates produced per plant, decaying of root tissues and leaf litters and the population level of methanogenic bacteria in roots. Setyanto et al. (2000) reported that early maturing cultivar emits least CH4 (52 to 112 kg CH4 ha−1) as compared to late maturing cultivar (116 to 142 kg CH4 ha−1). The high yielding cultivars emit more CH4 as compared to low yielding cultivars. On the basis of field experiment conducted in 2005 at Punjab Agricultural University, Ludhiana, India, Khosa et al. (2010) reported that rice cultivar Pusa 44 with high vegetative growth emitted more mean CH4 (5.45 mg m−2 h−1) than rice cultivar PR 118 (4.09 mg m− 2 h−1) having less vegetative growth .The ideal rice cultivar for mitigating CH4 emission from rice fields should have high root oxidizing potential, less ineffective tillers and high harvest index (Wang et al., 1999).

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6.10. Fertilizer There are several scientific studies which revealed the impact of fertilizer on CH4 emissions from rice soil (Yang et al., 2015a; Yang et al., 2014; Datta et al. 2013a; Banger et al., 2012; Bruce et al., 2012; Jain et al., 2004; Lindau, 1994). CH4 fluxes are strongly affected by the rate, mode and methods of application of fertilizers. Nitrogen application in the form of urea enhances CH4 emissions due to drop in redox potential and increasing soil pH, which favors methonogenesis processes (Wang et al., 1993). However, application of fertilizers like ammonium sulfate (Serrano-Silva et al., 2014), ammonium thiosuphate (Rath et al., 2002), super single phosphate (SSP) (Adhya et al., 1998) in paddy field have reported to lower CH4 emission as compared to urea. Serrano-Silva et al. (2014) reported CH4 emissions were lower in flooded rice soils when ammonium sulfate was used as a chemical fertilizer as compared to urea. Rath et al. (2002) reported about 38% and 60% reduction in CH4 emission due to application of ammonium thiosulphate at the rate of 45.6 and 60 kg N ha−1 in rice soil over control due to stimulation of the population of sulphate-reducing bacteria (SRB). The impact of fertilizers on CH4 emission has mainly reported due to stimulatory and inhibitory effect on methanogens and methanotrophs. Application of ammonium-containing nitrogen fertilizers at a high rate can decrease methane emissions (Xie et al., 2010) due to suppression of methanogens through changes in the soil C:N ratio and by encouraging the predomination of denitrifying bacteria (Wu et al., 2009; Singh et al., 2003). Ammonium fertilizer has reported to reduce CH4 emission due to competation of CH4 oxidizer with similar size NH+ 4 (Fig. 1a,b) ion for O2 as electron accepter (Bedard and Knowles, 1989). Cai et al. (1997) reported 30–50% lower CH4 emission in ammonium sulfate application than urea. However, several studies have shown that inorganic fertilizers inhibit methanotrophs while stimulate methanogens in rice paddies (Bodelier 2011; Hanson and Hanson, 1996; Hutsch et al. 1994; Conrad and Rothfuss, 1991). Kiese et al. (2003) reported no effect of NH+ 4 on CH4 oxidation while negative effect and positive effect were reported by Hutsch et al., 1994 and Jacinthe and Lal (2006), respectively. In higher concentration, NH4 may stimulate nitrification and reduce availability of O2 for CH4 oxidation (Conrad and Rothfuss, 1991). Balanced fertilization as compared to sole N- application has reported to enhances activities of methanotrophs, leading to less methane emission. Application of nitrogen and potassium together (e.g. potassium chloride) or the combination of nitrogen, phosphate, potassium, and crop residue stimulate the growth of methanotrophic communities (Zheng et al. 2008). Datta et al. (2013a) reported 48% reduction in CH4 emission due to combined application of nitrogen, phosphorous, and potassium as compared to N fertilizer application alone in wet rice soil. Nitrite has also been reported to inhibit CH4 oxidation in two pure culture of Methylosinus trichosporium OB3b and Methylomonas albus BG8 (King and Schnell, 1994) whereas Hutsch et al. (1994) reported no effect of nitrite on CH4 oxidation. However, long-term application of NH+ 4 -N fertilizer has been reported to decrease soil CH4 sink strength, whereas NO− 3 -N did not (Willison et al. 1995). Conversely, organic fertilizers (compost but not manure) had no effect on methanotrophy in comparison to inorganic fertilizers (Seghers et al., 2005). Thus, the form of fertilizer (organic versus inorganic) as well as the form of N + (NO− 3 –N versus NH4 –N) are important in determining CH4 sink potential. Methane consumption by rice field soils has also been reported due to application of both ammonium and nitrate at an elevated methane concentration after addition of N fertilizer (Mohanty et al. 2006). 6.11. Pesticide application There are few reports about the inhibitory effect of pesticide on CH4 production. Commonly used herbicide (Butachlor), commercial formulation of insecticide carbo-furan and fungicide tridemorph have reported to inhibits CH4 production. Mohanty et al., 2004 reported 98% while

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Jiang et al., 2015 reported 58% reduction due to application of butachlor in rice soil. Herbicide (butachlor) reduces CH4 production by increasing the soil redox potential as well as by reducing population of CH4 producing bacteria (methanognes) (Jiang et al., 2015; Mohanty et al., 2001). Bharati et al. (1999) reported that fungicide tridemorph inhibited production of CH4 at the rate 50–100 μg kg−1 soil but it stimulated CH4 production 5–20 μg kg−1 of soil. The effectiveness of application of insecticide carbofuran in methane production depends on the dose of insecticide. Sethunathan et al. (2000) reported that the application of carbofuran and carbamate in rice fields enhances the rate of CH4 oxidation. While Kumaraswany et al. (1998) suggested that carbofuran application increased the oxidation of CH4 when applied at low rates (5 and 10 μg g−1 soil) and inhibited CH4 oxidation when applied at higher rate of 100 μg g−1 soil. Butachlor application especially at high concentration reduces the population of methanotrophs that produce the MMO. 7. Method for methane flux measurements There are several techniques for measuring CH4 fluxes from rice fields and depending upon the goal of the study and resources available a suitable technique can be chosen. Table 8 presents the major commonly used techniques with their scale, relative advantages and limitations. Two techniques: closed-chamber technique and micrometeorological techniques are generally used to measure CH4 emissions from rice soils commonly. The close chamber measurement techniques can be further divided into manual and automated. 7.1. Manual close-chamber method Closed-chambers can be used manually for measuring methane gas flux from soil. Gas samples are collected periodically from soil for measuring the change in concentration of the methane gas in the chamber. To check the linearity of CH4 concentration in the chamber minimum three sampling should be taken at regular intervals of time. In the closed chamber, the concentration of gas starts to increase just after closing the chamber. Therefore, first gas sample should be taken immediately after closing the chamber followed by two more sampling at equal interval of time. Time interval between sampling should not exceed more than two hours. Chamber can be made from materials like acrylic sheet, perspex or rigid plastics. For collecting gas samples from rice fields, dimensions 50 cm × 30 cm × 100 cm, length, breath and height respectively made of 6-mm acrylic sheets are generally used (Pathak et al., 2012b). The gas samples should be analyzed immediately after sampling to prevent

the diffusion loses of gas. Concentration of CH4 gas in the collected gas samples are then measured by using gas chromatography (GC) equipped with flame ionization detector (FID). After analyzing by GC the flux of CH4 is calculated by using the following equation: F ¼ ρ x ðV=AÞ x ðΔc ¼ Δt Þ x ð273=T Þ where F is the CH4 flux (mg CH4 m− 2 h− 1), ρ is the gas density (0.714 mg cm−3), V is the volume of chamber (m3), ‘A’ is the surface area of chamber (m2), Δc/Δt is the rate of increase of CH4 gas concentration in the chamber (mg m−3 h−1) and T (absolute temperature) can be calculated as 273 + mean temperature in (°C) of the chamber. 7.2. Automated close-chamber method An automated system is the same as the manual close chamber but the opening and closing of close chamber is controlled electronically by a computer programme and sampling and analyzing of CH4 emission is done simultaneously. The measured CH4 emission by automated close chamber has less uncertainty than manual. An automated shutter driving by an air valve is installed in to open and to close the chamber. Two fans are installed, one below the ceiling of the chamber for mixing the air inside the chamber and another fan is attached for introducing ambient air into the chamber through a flexible duct. A water-tight channel is also attached at the bottom over which each chamber is fitted vertically. The channel when filled with water provides a seal between paddy soil and the chamber even if the field is drained. The pump, computer, and gas chromatograph for analyzing CH4 concentrations should be installed in a close proximity of the experimental field. The samples can be collected diurnally from the chambers at desired intervals. Methane concentration of the air sample is determined by using a gas chromatograph equipped with a flame ionization detector (FID) as in the manual methods. 7.3. Micrometeorological method (Eddy Covariance technique) The eddy covariance is a non-destructive, statistical, micrometeorology technique for quantification and determination of CH4 exchange rates over the rice fields. The eddy covariance analyzes high-frequency (5–40 Hz) vector and scalar data series within the atmospheric boundary layer and produces fluxes of CH4. The 3D wind and CH4 concentration and temperature are converted into average and their fluctuating components. Mathematically, “eddy flux” is calculated as a covariance

Table 8 Comparison of different measuring techniques to determine methane emission from rice soil. Source: Topp and Pattey, 1997. Measuring technique

Measuring Scale

Area (m2)

Analyzer

Advantage

Disadvantage

Can measure small fluxes No or limited energy required Easy to hand Good for short duration collection sampling periods Low manufacturing cost Easy to handle Environmental conditions similar to ambient fields It is effective for continuous long-term monitoring

Build up gases concentrations in chamber, alter the atmospheric pressure , temperature etc. which may inhibit the normal emission rate of soil Labour costly Soil distribution during instillation Pressure deficit inside chamber can cause artificially methane flux Automated sampling is required Expensive as compared to close chamber It disturbs the soil environment

Closed chamber (manual)

Small

b1

GC-FID⁎

Close chamber (automated)

Small

b1

GC-FID

Soil incubation

Small

b1

GC-FID

Soil vertical probes Eddy covariance

Small Large

b1 N100

GC-FID IRGA⁎⁎

⁎ GC-FID — gas chromatography–flame ionizing detector. ⁎⁎ IRGA — infra-red gas analyzer.

Inexpensive Controlled conditions studies Methane exchange with depth No or minimum distribution Can measure fluxes of ecosystem basis Useful for mentioning diurnal and seasonal variations

Causes intimal distribution of soil High cost, Data analyzing in difficult Required continuous energy supply, Assumption and correction level high Dependence on atmospheric conditions


between instantaneous deviation in vertical wind speed (w′) from the average (w-overbar) and instantaneous deviation in CH4 concentration, mixing ratio (s′), from its average (s-overbar), multiplied by average air density (ρa). The measured flux is proportional to the covariance.

Basic strategies of methane mitigation in paddy cultivation

Management practices

F≈ρa w0 s0 Water Management

There are few assumption also required for this techniques such as the flux measurements should be at a point can represent an upwind area and it will be measured in the adequate fetch with fully turbulent wind condition in a horizontal and uniformed terrain. The instrumental limitations such as effect of sensor separation, sonic path averaging, cospectral correction are especially required for CH4 measurements at low heights below 1–1.5 m. The close chamber and eddy covariance are the only techniques at present available for the measurement of the CH4 from the rice fields. But both the techniques are having different level of uncertainty and limitation. The close chamber technique is having discrete and limited actual measurement data during the crop duration, so, comparatively has higher uncertainty. The eddy covariance data is more representative due to its continuous measurement; therefore, the uncertainty level is lower.

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Other interventions

Alternate wetting & drying Midseason drainage Intermitted drainage Controlled irrigation

Management of Soil organic carbon

Transplanting Management

Fly ash Phosphogypsum Steel slag Microbial fuel cell

Biochar application Vermi-composting

Zero tillage System of rice intensification (SRI) Direct seeded rice (DSR)

Time of Sowing

Late sowing reduce cumulative CH4 emission by reducing crop duration

Fertilizer management

Nitrification inhibitors Slow releasing fertilizer Biofertilizers Adjusting time, rate and placement

Fig. 5. Basic strategies of methane mitigation in paddy cultivatio.

8. Mitigation of methane emission The understanding of different factors responsible for methane production, emission and consumption help in formulating mitigation strategies. The management of factors like water level, soil organic carbon, fertilizer and rice cultivar has been well studied and doccumanted for mitigation of methane emission from rice fields. However, adaptability of technology generated from managing these factors depends on economy of the technologies (Gupta et al., 2015). Farmers generally give highest priority to economic production of crop rather than mitigation. According to finding of different studies, the possible ways of CH4 mitigation in rice cultivated paddy wetlands may be broadly oriented in two major groups namely: (a) Management practices, and (b) Other interventions (Fig. 5). The controlling factors for CH4 mitigation range from smallest scale to global scale. Some widely reported management practices which can be used for mitigation of CH4 are reported in the section below: 8.1. Water management Water management is considered to be one of the important practices in rice production and is also observed to be the most promising tool for CH4 efflux mitigation. However water management has low potential in deep water rice cultivation, where the needed management is yet to be developed. Proper water management such as intermittent irrigation/flooding (irrigating alternately throughout the growing season), midseason drainage (short-term drainage (5–20 days) before maximum tillering stage during crop growth phase in rice), alternate wetting and drying (periodic drying and re-flooding of the rice field), controlled irrigation (control either the irrigation duration or volume of water applied for control purposes) and multiple drainages (multiple short periods of drainage (2–3 days) approximately every three weeks during the growing season) are effective strategies for reducing CH4 emission (Table 9). Water management practices improve soil permeability and increase soil redox potential (Tyagi et al., 2010) which suppresses methanogensis, resulting in less CH4 emissions. 8.1.1. Midseason drainage Mid-season drainage may be an effective tool to reduce CH4 emission.Mid-season drainage is short-term drainage (5–20 days) before maximum tillering stage during crop growth phase in rice. A short mid-season drainage may reduce cumulative seasonal CH4 flux. Mid-season drainage reduces 43% CH4 emission due to influx of oxygen

into soil which was favorable for menthnotrophic bacteria (Corton et al., 2000). Shiratori et al. (2007) reported that mid-seasonal drainage has potential to reduce CH4 emission by 71% compared with no drainage practice in rice. Itoh et al., 2011 tested different watermanagement strategies such as prolonged midseason drainage at nine paddy sites across Japan. On an average due to extended midseason drainage (7–28 days), seasonal CH4 emission were suppressed up to 69.5% relative to conventionally managed plots while maintaining grain yield (96%).

8.1.2. Intermittent drainage CH4 emission can be mitigated by intermitent drainage (stopping irrigation and allowing the standing water to drain from field). It increases the thickness of oxidizing layer due to diffusion of oxygen into the soils and reduces the CH4 production. Kudo et al. (2014) stated that intermittent drainage can mitigate CH4 emissions by 47% as compared to continuous flooding. Kim et al. (2014a) also reported 43–53% reduction in CH4 seasonal flux to that of continuous flooding in rice soil. Pathak et al. (2003) reported that intermittent drying and wetting reduced CH4 emissions by 51% due to the formation of aerobic condition. In a four-year (July to October; 1994 to 1997) study in northern India, it has observed that intermittent flooding have potential of reducing CH4 emission by 22% as compared to continuously flooding (Jain et al., 2000). Thus, intermittent drainage practice in paddy cultivation play crucial role in reducing CH4 emissions without having any significant effect on grain and biological yield.

8.1.3. Alternate drying and wetting It is a practice of periodic drying and re-flooding of the paddy field. Drainage of flooded water results in aerobic conditions which avoid CH4 production as well as enhances CH4 oxidation (Adhya et al., 2014). Alternate drying and wetting cycles of 20 or 40 days reduce CH4 emission than the continuous flooding practice (Mishra et al., 1997). Khan et al. (2015) reported that alternate wetting and drying (irrigated at 5 cm depth, 3 days and 4 days drying in week) effectively mitigated CH4 emissions by 28% over continuous flooding while maintaining grain yield (6.71 t/ha). Therefore alternate drying and wetting could be one of the practices for achieving the goal for sustainable rice production while minimizing CH4 emissions from irrigated paddy cultivation.

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Table 9 Relative methane mitigation potential of various water management practices as compared to traditional flooding in rice. Suggested practice

Mitigation (%)

Water saving irrigation

60

Alternate wetting and drying

26.37

Alternate wetting and drying

72.94

Intermittent drainage

47.1

Midseason drainage

12–27

Midseason drainage

37–51

Midseason drainage

65

Midseason drying

88

Midseason drainage

43

Midseason drainage (prolonged) (7–28 days) Controlled irrigation Controlled irrigation Multiple drainage

66.1–72.9

Intermittent irrigation

24.22

Intermittent irrigation Intermitted irrigation

15 25.4

No flooding (wet)

88.33

81.8 79.1 41

Remarks

References

Location — Tokyo, Japan Duration — 143 days Location — Mymensingh, Bangladesh Duration — 118 days Location — IRRI, Philippines Duration — 136 days Location — Kanagawa, Japan Duration — 140 days Location — Jurong City, China Duration — 140 days; Location — Jiangxi Province, China, Duration — April to July in 2009 and from July to November in 2010 Location — Nanjing, China; Duration — three years field study from 2000 to 2002 Location — Lucknow, India; Duration — 84 days Location — Munoz, Nueva Ecija, Duration — for nine consecutive seasons (five dry + four wet) from 1994 to 1998 Location — 9 sites of Japan

Win et al. (2015)

Location — Jiangsu Province, China Duration — 130 days Location — Jiangsu Province, China Location —Lucknow, India Pot experiment; Duration —112 days Location — Shenyang, China Duration — 149 days Location — Central Rice Research Institute, Cuttack, India Location — Beijing, China Duration — 122 days Greenhouse pot experiment, Duration — 120 days

8.2. Plantation methods Two plantations methods: direct seeded rice (DSR) and system of rice intensification (SRI) have been reported to be very effective in reducing GHG emission. In, DSR puddling and transplanting is avoided and direct sowing of rice seed is done on tilled or no tilled soil. Pathak et al. (2011) reported that direct seeded rice method (DSR) could reduce CH4 emissions significantly over conventional transplanting method. DSR was a common practice before green revolution in India (Singh and Shahi, 2015) and it has again become popular under changing climate scenario as it reduces CH4 emission as compared to conventional puddled transplanted rice (TPR) of rice. Cumulative CH4 emission reduction by DSR over TPR has been reported between 82 and 98% (Gupta et al., 2016; Pathak et al. 2012). SRI is a method of transplanting 15–20 days old single rice seedling per hills into puddled soil where flooding is avoided and soil is kept at field capacity. Jain et al., 2014 reported 61% reduction in CH4 emission from SRI as compared to TPR.

Khan et al. (2015) Katayanagi et al. (2012) Kudo et al. (2014) Li et al. (2014) Ma et al. (2013) Zou et al. (2005) Singh et al. (2003) Corton et al. (2000) Itoh (2011) Hou et al. (2012) Yang et al. (2012) Tyagi et al. (2010) Jiao et al. (2006) Adhya et al. (2000) Wang et al. (1999) Mishra et al. (1997)

rice plants helps in increasing soil redox potential, and resulting in oxidation of CH4. Therefore; selection of suitable cultivars may play a major role in the regulation of CH4 emissions from rice fields. Various studies suggest that rice cultivars with few unproductive tillers, small root system, high root oxidative activity, high harvest index, low root exudation and which are early maturing are ideal for mitigating CH4 emission in rice fields (Aulakh et al., 2001; Wang and Adachi, 2000; Shin and Yun 2000). Therefore, qualitative and quantitative difference in root exudates composition among different cultivar could affect CH4 production rate significantly (Jia et al., 2002). Wang et al. (1997b) demonstrated that the root air space and root oxidation power adjusted the CH4 source strength in the root medium. Thus, these variations in cultivar could build differences in CH4 emission rate directly and/or indirectly. Some reported varieties with low emission of methane are: Dasanbyeo (36.9 g m−2) b Ilpumbyeo (42.9) b Gyehwabyeo (47.8) b Daeanbyeo (50.9) b Dongjinbyeo (58.8) b Hwaseongbyeo (59.7) b Odaebyeo (62.9) b Mangeumbyeo (76.0) in Korea (Shin and Yun, 2000) and PR 118 (4.09 mg m−2 h−1) b Pusa 44 (5.45 mg m−2 h−1) in India (Khosa et al. (2010).

8.3. Rice varietal selection 8.4. Fertilization and nitrification inhibitors The difference in amount of CH4 emission under different varieties of rice is well documented in United States of America (Simmonds et al., 2015; Lyman and Nalley, 2013), India (Das and Baruah, 2008; Mitra et al., 1999), Japan (Riya et al., 2012; Koga and Tajima, 2011; Jia et al., 2006), Philippines (Wassmann et al., 2002; Wang et al. 1997a) and South Korea (Gutierrez et al., 2013; Shin and Yun, 2000). The difference of CH4 emission in different cultivar is due to the difference in plant structure, size, number of tillers, metabolism, CH4 gas transport potential and root exudates etc. (Setyanto et al., 2004; Jia et al., 2002; Wang et al. 1997a). CH4 production is mainly control by soil redox potential and threshold level for production is − 150 mV (Nishimura et al., 2004) and is stimulated further at lower Eh values. Oxygen transport from the atmosphere to the rhizosphere via aerenchyma cells of the

CH4 emission is effected by type, rate and method of fertilizer application in rice crop. Recently it has been reported that N management in rice reduces CH4 emission by 30–50% as compared to the control (Dong et al., 2011) (Table 10). Application of ammonium-based N fertilizer has potential for reducing overall CH4 emission as compared to urea (Linquist et al., 2012; Ali et al., 2012; Xie et al., 2010) by increasing CH4 oxidation rate in the rice root zone (Bodelier et al., 2000). Sulfatebased fertilizer is known to enhance the substrate competition between methanogens and sulfate-reducing bacteria, thus reducing CH4 production in anaerobic conditions (Hussain et al., 2015). Singla and Inubushi (2014) reported that if N was applied as ammonium sulfate, it reduced the total seasonal CH4 emission from 22.2 g m− 2 to 16.9 g m−2.


889

Table 10 Influences of different fertilizers and chemical interventions on methane emission from soils. Treatment

CH4emission (kg CH4 ha−1)

Mitigation (%)

Reference and location

Urea (220 kg ha−1) Urea + calcium carbide (30 pmm) Urea + calcium silicate (500 kg ha−1) Urea + phosphogypsum (500 kg ha−1) Urea + biochar (1 t ha−1) Urea (250 kg ha−1) Urea (250) + phosphogypsum (90 kg ha−1)

124 118 93 91 130 117.3 92.6 89.5 102.9 102.5 95.5

Control (C) 4.84 25.00 26.61 4.84a C 21.57

Ali et al., 2013 (Bangladesh)

Urea (250) + silicate fertlizer (150 kg ha−1) Urea (190) + (azolla + BGA(1 t ha−1)) Urea (250) + coal ash (1 t ha−1) Sulphate of ammonia (400 kg ha−1) ABFb (0 kg N ha−1) ABF (150 kg N ha−1) ABF (250 kg N ha−1) No fertilization Urea ( 240 kg N ha−1) Controlled release fertilizerc (240 kg N ha−1) Compound fertilizerd (0 kg ha−1) Compound fertilizer (150 kg ha−1) N fertilization (250 kg ha−1) No fertilization Urea (50 kg N ha−1 ) + compound fertilizerd (70 kg N ha−1) Urea (180 kg N ha−1 ) + compound fertilizer (70 kg N ha−1) Urea (120 kg N ha−1) + phosphorus (60 kg P2O5 ha−1) + K (0 kg ha−1) Urea + phosphorus + K (30 kg ha−1) Urea + phosphorus + K (60 kg ha−1) Urea + phosphorus + K(120 kg ha−1) Urea (120 kg N ha−1) Urea + hydroquinone (10%) Urea + Neem cake (10%) Urea + Thiosulphate (10%) Calcium carbide coated urea (120 kg N ha−1) Neem oil coated urea (120 kg N ha−1) Urea + dicyandiamide (10%) No fertilization Urea (60 kg N ha−1) AS (45.6 kg N ha−1; 20 kg S ha−1) AS(60 kg N ha−1; 28 kg S ha−1) No N fertilization Ammonium sulphate (100 kg N ha−1) Urea (100 kg N ha−1) Ammonium sulphate (300 kg N ha−1) Urea (300 kg N ha−1) Steel slag (0 Mg ha−1) Steel slag (2 Mg ha−1) Steel slag (4 Mg ha−1) Steel slag (8 Mg ha−1) a b c d e

524 256 225 76.9 65.8 64.9 155.9 113.8 73.9 220.5 136.2 111.9 125.34 63.81 82.03 64.43 27.0 30.2 23.9 28.4 23.4 24.9 23.8

23.70 12.28 12.62 18.58 C 51.15 57.00 C 14.4 15.6 C 27.00 52.60 C 38.23 49.25 C 49.09 34.55 48.60 C 11.85 11.48 5.19a 13.33 7.78 11.85

34.7 40.6 20.7 14.3 95.3 55.0 88.4 38.6 82.1 2.34e 1.49e 1.12e 1.03e

C 17.00a 40.35 58.79 C 42.29 7.240 59.50 13.85 C 36.33 52.14 55.98

Ali et al., 2012 (Bangladesh)

Xie et al., 2010 (China)

Yang et al., 2014 (China)

Yao et al., 2012 (China)

Dong et al., 2011 (China)

Babu et al., 2006 (India)

Malla et al., 2005 (India)

Rath et al., 2002 (India)

Cai et al., 1997 (Japan)

Wang et al., 2015 (China)

Emission more than control. ABF — ammonium based-fertilizers (70% urea plus 30% compound fertilizer-N: P2O5: K2O = 15%: 12%: 12%). Controlled released fertilizer — thermoplastic resin-coated urea. Compound fertilizer is a mixture of NH4H2PO4 and KCl, with N:P2O5:K2O = 15%:15%:15; AS—ammonium thiosulphate. mg m−2 h−1.

Application of ammonium sulfate as a source of N in rice field reduced CH4 emission by 23% (Ali et al., 2012). Corton et al. (2000) observed that ammonium sulfate reduced CH4 emissions by 25–36% over urea. Ali et al. (2008) suggested that silicate fertilizer application at the rate of 10 Mg ha−1 could mitigate CH4 emission by 28% along with a 17% increase in yield over the control. As Application of potassium led to a drop in soil redox potential, reducing the CH4 production and stimulating the CH4 oxidation, thereby resulting in a reduction of CH4 emissions (Hussain et al., 2015; Babu et al., 2006). Potassium application at the rate of 30 kg K ha−1 reduced cumulative CH4 emissions by 49% as compared no application of K (Babu et al., 2006). Bio-fertilizers are capable of sustainable soil improvement, increasing yields (Pabby et al., 2003) along with CH4 mitigation in rice (Kollah et al. 2015b; Singh and Strong, 2016) viz. Azolla (Ali et al., 2015; Nadeem et al., 2014), mycorrhizae (Nadeem et al., 2014),

cyanobacteria/blue green algae (BGA) (Singh, 2014; Ali et al., 2014; Shukia et al., 2008), diazotrophs (Kennedy et al., 2004). BGA/Azolla oxygenates the rice soil (Prasanna et al., 2002; Lakshmanan et al., 1994; Mandal, 1961) through their photosynthetic capacity. Azolla, (aquatic pteridophyte) are capable of N2-fixation and symbiotically associated along with Anabaena azolla, and are the most widely used biofertilizer in China (Shao et al., 2011), India (Raja et al., 2012), Bangladesh (Ali et al., 2012, 2014), and Vietnam (Phong et al., 2011) in rice field (Yadav et al. 2014). Azolla had a moderating effect on CH4 emission from flooded rice soil through an increase in the dissolved oxygen concentration at the soil-floodwater interface. Bharati et al. (2000b) observed the lowest CH4 flux (89.29 kg CH4 ha− 1) in dual cropping of Azolla along with urea (30 + 30 kg N ha−1). Ali et al. (2015) reported the highest mitigation on the application of Azolla-Cyanobacteria (AC) along with phosphogypsum and NPK (Fig. 6a). Ali et al. (2012) also

890


a 180 160

NPK NPK + SS + AC

Urea 140

158 146.5

143

135

140

116

100

112

100 80 60

91.3

80 60 40

40

20

20 0

0 Japan

c

Bangladesh

BAU Site (Upland)

Bhalukan Site (Lowland)

135 132

180 160

158.3

d

130.7

130

149.4

126.7

140

126

105.6

100

89.3

80 60 40

kg CH4 ha-1

125

120

kg CH4 ha-1

114.5 105.5

113.7 109

120

Urea + AC 129

120

kg CH4 ha-1

kg CH4 ha-1

b

NPK + BC + AC NPK + PG + AC

120 116 115 110

20 105

0 Urea

Urea + Az

Urea + ADC

Az + ADC

Urea (U) + U + RS + U + SS + U + SS + U + SB + RS SS SB SB +BGA CMC

Fig. 6. Potential of different bio-fertilizer for methane mitigation in rice (Source: Fig. 6a- Ali et al., 2015: Fig. 6b- Ali et al., 2012; Fig. 6c-Bharati et al., 2000b; Fig. 6d-Ali et al., 2014). NPK — nitrogen, phosphorus, potassium; BC — bio-char; AC — azolla, cyanobacteria; SS — steel slag; PG — phosphogysum; U — urea; RS — rice straw compost; SB — sesbania; CMC — cattle manure compost; ADC — azolla dual cropping.

reported the lower CH4 emission from the urea + cynobacteria + Azolla treatment (114.5 and 91.3 kg CH4 ha−1) over urea alone (129 & 105 kg CH4 ha−1) in lowland and upland rice field in Bangladesh respectively (Fig. 6b). Bharati et al. (2000b) observed a decreasing trend of CH4 emission from the Azolla (incorporated) + urea N Azolla (incorporated + dual crop) N no N control N urea + Azolla (dual crop) treatments in rice field (Fig. 6c). Synechocystis sps. Among the cyanobacteria are most promising for CH4 mitigation from the rice fields (Prasanna et al., 2002). Ali et al. (2014) also observed the lowest CH4 emission on the application of cyanobacteria along with the Sesbaina biomass, silicate fertilizer and urea (Fig. 6d). Use of nitrification inhibitors (NI) or slow-release N based fertilizer are capable of reducing greenhouse gas emissions from rice fields (Majumdar, 2003). NI slows down the process of conversion − of NH+ 4 nitrogen into NO3 N nitrogen. The application of hydroquinone (urease inhibitor), dicyandiamide (nitrification inhibitor) and hydroquinone plus dicyandiamide decreases CH 4 emissions by 30, 53 and 58% respectively (Boeckx et al., 2005). Li et al. (2009) reported that combined use of hydroquinone (HQ) and dicyandiamide (DCD) with basal fertilizer, and fertilizer application at the time of tillering and panicle initiation reduced CH4 emissions by 35, 19 and 12% respectively. Similar results were also reported by Mohanty et al. (2009), who observed that the application of DCD at the time of soil incubation resulted in a 31% reduction in CH4 production as compared to untreated soil as investigated in a laboratory study. Application of DCD along with urea (10%) has been reported to significantly decrease CH4 emissions by 30% as compared to urea alone (Pathak et al., 2003). Malla et al. (2005) reported that the application of natural NI like neem cake and neem oil coated urea reduced CH4 emission by 8 and 11% respectively as compared to urea alone. Encapsulated calcium carbide (ECC) has also been observed to reduce CH 4 emission (13%) from rice fields (Malla et al., 2005).

8.5. Other interventions for mitigation of methane in rice Phospho-gypsum, silicate slag and fly ash, which are waste or byproduct of phosphate fertilizer industry, steel industry and coal burning industry respectively have potential in mitigating CH4 emissions from rice (Table 10) (Ali et al. 2008 and 2013). It may be a win-win technology in future as it helps in mitigating global warming and also helps in effective waste utilization. Phosphogypsum contains high amount of calcium and sulfate. The high content of sulfate in rice might prevent CH4 production as well as CH4 emissions due to stronger competitor for the substrate (acetate or hydrogen) between sulfate-reducing bacteria and methanogens (Hussain et al., 2015; Ali et al., 2012). Ali et al. (2009a) reported that application of fly ash, silicate slag and phosphogypsum at the rate of 10 Mg ha−1 level, reduced CH4 emissions by 20% to 27% while increasing the rice grain yield by 15 to 23% as compared to application of urea alone in lowland rice field of Bangladesh. Microbial fuel cells (MFCs) are a green technology device that converts chemical energy bound in organic compound into electrical energy by using microorganisms (Rismani-Yazdi et al., 2013). As MFCs are able to generate electricity from wetlands soils, including rice fields therefore, MFCs can be a novel strategy for mitigation of CH4 from paddy fields (Rizzo et al., 2013). Typical MFCs are constructed with cathode placed at the air-water interface and an anode buried in anaerobic (reduced) flooded soil. Electricity is generated due to release of electrons by the oxidation of soil organic matter or plants roots (Chen et al., 2012). Rizzo et al. (2013) according to a simulation study reported that MFCs could reduce CH4 emissions up to 22.0% of the total CH4 emissions. 9. Concluding remarks Many techniques have been suggested for reducing CH4 emission however, the farmers will accept only those that ensure that grain


yield is not affected. Changing irrigation practices, modifying use of fertilizer and low emitting rice varieties have the potential to reduce the global CH4 emission to the order of 10–30%. Multiple-aeration reduces CH4 emission to a significant extent however; this mitigation option has limited scope due to rice being grown under different water regimes. Some upland rice growing regions require frequent irrigation whereas it may be difficult to drain excessive water from the paddy fields due to heavy rain in many lowland areas. The emission of CH4 from rice can be reduced by site-specific nutrient management, drainage of excessive water, practicing intermittent irrigation and direct seeding of rice. Application of fermented cow dung and leaf manures, change in N fertilizer (urea to ammonium chloride and ammonium sulphate instead of prilled urea) application of nitrification inhibitors and slow release fertilizers have a potential to mitigate methane emissions. Biochar, straw compost and straw ash incorporation are more promising than the direct straw incorporation. Some other important mitigation options are breeding improved rice varieties with low CH4 emission potential and diversification of crops in a rice-based cropping system. The above stated mitigation options are just scientific studies but to get the full applicability of these options either alone or in combination in the farmer fields will need the policy and governmental support. The policy for the CH4 abatement varies with the region/country specific and is greatly influenced by the financial aid provided by the government. We did not find any direct policies in major rice producing countries to reduce the CH4 emission from the rice field such as Vietnam, Philippines, Malaysia, India, Pakistan, and China. 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