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The first three authors contributed equally to this paper.
One hundred million tons of farm stalk waste and livestock and poultry excrement are used every year in China for the production of clean energy (biogas) by anaerobic digestion. Consequently, a large amount of fermented liquid is produced, and if disposed of improperly, it will result in secondary pollution. Agricultural application of this anaerobic slurry as a liquid fertilizer would reduce possible eutrophication of water sources from random slurry discharge and supply a superior organic fertilizer for farming. This study investigated the effect of applying anaerobic digestion slurry as a liquid fertilizer on the methane emitted from a paddy field. A two-year (2008–2009) field experiment replacing chemical fertilizer with liquid fertilizer from anaerobically digested pig manure slurry was conducted in a paddy field in Yixing, Jiangsu, China. A static closed chamber method was used to measure methane fluxes over the period from June 2008 to October 2009. All fertilizer treatments increased methane emissions relative to untreated controls, with increases in methane ranging from 40–70% in 2008 to 48–84% in 2009. Paddy fields treated with anaerobically digested pig manure slurry had greater methane emissions (8–84% in 2008 and 3–26% in 2009) than those treated with chemical fertilizer. This suggests that the anaerobic digestion slurry would increase methane emission and so is unsuitable as a liquid fertilizer in paddy fields without development of cultivation practices to limit these emissions.
Methane (CH4) is an important greenhouse gas, ranking only after carbon dioxide (CO2) in forcing, which contributes 15% to the greenhouse effect. Atmospheric methane increases at a rate of 1% every year. The majority of this increase originates from paddy fields (Jiang et al., 2004; Smith et al., 2007; Alexander et al., 2010). Rice cultivation has been identified as a major source of atmospheric CH4. The global CH4 emission rate from paddy fields was estimated to be 40 Tg yr−1 (Neue & Sass, 1998; Sass et al., 1999); 10–20% of the atmospheric methane is attributed to methane derived from paddy field soil. This demonstrates the importance of evaluating global methane sources by investigation of methane emission from paddy fields (Follett, 2001; Mosier et al., 2006; Smith et al., 2007). China is the most important rice producing country in the world, and its planting area accounts for about 20% of global cultivation and rice cultivation represents 23% of all cultivated land in China (Frolking et al., 2002; Jiang et al., 2004). Consequently, methane emission from Chinese rice paddy fields is of great concern.
Relative to irrigation with unpolluted river water, irrigation with sewage significantly increases CH4 and N2O emissions from rice paddy fields (Zou et al., 2009). Adding organic materials influences methane formation. Amendments with fresh organic matter, like rice straw and green manures, greatly increase methane production and emission. Application of composted material, which has a higher degree of humification, only slightly increases methane formation and fluxes (Yagi & Minami, 1990; Hou et al., 2000). All growth variables for different species of rice, except mean shoot and root biomass, show strong positive relationships with seasonal CH4 emission. CH4 source strength is dependent on the rice variety under cultivation, its phenology, growth variables, and soil N-fertilization (Singh et al., 1999). Previous studies concentrated on controlling and limiting methane emission by focusing on water management, control of soil organic matter, and selection of chemical fertilizers. However, a little attention has been given to effects on methane emission from paddy fields from application of biogas slurry liquid fertilizer produced from the large number of methane-generating tanks working in China.
China is the world's largest cereal producer and has the most herds of livestock and poultry and produces large quantities of farming stalk and livestock and poultry excrement. To prevent environmental pollution from these agricultural pollutants, some of these farm wastes have been used to fertilize field soil while larger quantities of the waste are recycled and used to produce renewable clean energy by fermentation in methane-generating pits. Over 30 million methane-generating tanks have been built in rural villages and towns in China that annually generate over 12.2 billion cubic meters of methane and approximately 385 million tons of liquid fertilizer. The methane produced equals 18.5 million tons of standard coal and consequently eliminates 45 million tons of carbon dioxide emissions (Ni, 2007). However, continuous production and discharging of liquid wastes from methane-generating pits have led to river pollution and spurred efforts to identify ways that this waste can be suitably disposed including fertilizing crops.
To investigate the effects of application of liquid anaerobic digestion slurry from methane-generating pits on methane emission from paddy field soils, 0–100% of chemical nitrogen fertilizer applied to rice fields was replaced by anaerobic digestion slurry. The effects of variation in fertilizers on methane emission are critical for evaluating the potential for slurry application to be a sustainable agricultural management strategy.
Materials and methods
The two-year field experiment started in summer of 2008 in a long-term fertilizer experimental grid at Gaochen Town (31°26′N, 119°47′E), Yixing, Jiangsu, China, where a rice-wheat rotation system was used. The region is characterized by a subtropical oceanic monsoon climate which is warm and humid throughout the year. The annual average air temperature is 15.7 °C and the average monthly air temperature is 28.3 °C during the summer. Average annual precipitation is 1177 mm with 136.6 average days of precipitation. The paddy soil tested in this study was classified as yellowish earth with 1.23 g kg−1 of total N, 0.45 g kg−1 of total P, pH of 6.23, and organic matter content of 16.2 g kg−1. The rice variety tested was Zhendao 10.
A randomized block experiment with three replicate plots of 25 m2 was established with eight different fertilizer treatments. Application rates of total P and K were 26.2 kg P hm−2 and 150 kg K2O hm−2 and controls (CK) had no fertilizer. Phosphorus and potassium deficiencies in the anaerobic digestion slurry (ADS) were corrected by addition of chemical phosphorus and potassium fertilizer. In all treatments, pure chemical fertilizers were applied as base fertilizer. Total nitrogen application rates of 240 kg hm−1 were used but the source of N varied among treatments. Some N in chemical fertilizer was substituted by N from liquid fertilizers. In addition, treatments varied in the timing of fertilizer application during the growing season (Table 1).
Table 1. Descriptions of fertilizer treatments including fertilizer types, application rates, and application timing. ADS (anaerobic digestion slurry) indicates liquid fertilizer from methane-generating pits
Application rates and timing
Only chemical fertilizers (N 240 kg hm−2)
Applied 3 times, 40% base 25%, tillering, 35% heading
Urea N applied 3 times as above, ADS applied in base fertilizer
75% N as ADS, 25% N as Urea
Urea N applied 3 times as above, ADS applied in base fertilizer
Important chemical components of the tested anaerobic digestion slurry (ADS) were: total N of 880 mg l−1 with NH4+-N: 718 mg l−1, total P of 37.6 mg l−1, total K of 590 mg l−1, pH 7.83, and chemical oxygen demand (CODCr) of 3737 mg l−1.
Chemical fertilizer treatments included a phosphate fertilizer, a potassium chloride fertilizer, and urea. Anaerobic digestion slurry (ADS) was applied by calculating the amounts necessary to provide the nitrogen in each treatment at each application time, weighing the required amount of ADS in a plastic barrel and spreading it evenly throughout the paddy field. The experiment was conducted over two consecutive summer seasons.
In 2008–2009, base fertilizer, tillering fertilizer (fertilizer applied when plants are growing and splitting to form many stems) and heading (earring) fertilizer (fertilizer applied when plants are flowering) were applied on June 28, July 9, August 23 of 2008 and June 16, July 13, August 28 of 2009, respectively.
Plots were managed according to local farming practices. During the experiment in 2008, rice was transplanted on June 28 and harvested on October 25 after 120 days of rice growth. Mid-season drainage began on July 29 and ended on August 8. During the 2009 experiment, rice was transplanted on June 19 and harvested on October 25 with 133 days of rice growth, and mid-season drainage began on July 21 and ended on August 21 due to persistent rain.
Sampling and measurement of methane
CH4 flux was determined by using a static closed chamber method (Zou et al., 2009; Shang et al., 2011). The chamber was enclosed around the perimeter and the top had two small holes, one for determination of air temperature inside the chamber and one for sampling. It was equipped with two circulating fans inside to ensure sufficient gas mixing and wrapped with a layer of sponge and aluminum foil to minimize air temperature changes inside the chamber during sampling. Measurement of CH4 emissions were initiated during summer 2008 and continued over the two annual cycles. One chamber during each rice growing season was fixed to a random site in each plot. The chamber bodies were premounted into iron sockets under 15 cm of field soil. The bottom edge of the frame had a groove for holding water to seal the rim of the chamber. Gas samples were taken from 08:00 hours through 12:00 hours every 20 min as the soil temperature during this period was close to the mean daily soil temperature (Zou et al., 2009). Gas samples were collected and measured in triplicate plots each week during rice plant growth. Air samples from the chamber headspace were collected by using 100 ml plastic syringes with two-way stopcocks via a Teflon tube (with an outer diameter of 1/8 in) connected to the chamber.
Eighteen milliliter gas samples were immediately transferred to pre-evacuated vials with rubber stoppers. The air temperature inside the chamber and soil temperature at 5 cm of soil were monitored during gas collection and the depth of the sealing water layer was measured using a ruler. CH4 concentration in the air samples collected from crop canopy was analyzed by gas chromatograph (GC-12A, Shimadzu Scientific Instruments Inc., Kyoto, Japan) equipped with a flame ionization detector (FID). The oven was operated at 80 °C, and the FID at 200 °C, respectively. The carrier gas (N2) flow rate was 40 ml min−1. Hydrogen gas (H2) was used as a flammable gas with a flow rate of 35 ml min−1 with air used as an assistant flammable agent with a flow rate of 350 ml min−1. A standard CH4 gas sample was supplied by the National Japanese Agriculture and Environment Technology Institute.
Methane emission was measured as CH4 emission flux, defined as the quantity of methane released from one unit area of paddy field soil in one unit of time (LI et al., 2007). Average flux and standard deviation of CH4 were calculated from triplicate observations for each time point. Seasonal CH4 emission was averaged from the average daily flux based on weighted duration intervals. The formula for calculation of CH4 emission flux is shown below: F = ρ × V/A × dc/dt × 273/T where: F = CH4 emission flux in mg m−2 h−1; ρ = CH4 density under standard conditions = 0.714 kg m−3; V = effective volume inside the chamber (the space from the top of the chamber to soil surface or water layer surface while waterlogged) in m3; A = area of soil surface covered by chamber in m2; dc/dt = change of methane concentration inside the chamber at one unit time in ppm h−1;T = temperature inside the sampling chamber in K. Seasonal gross CH4 emission was calculated as:
where, T = seasonal gross CH4 emission in g m2; Fi and Fi+1 indicate the average CH4 emission fluxes sampled at times i and (i + 1) in mg/(m2 h); Di and Di+1 indicate sampling time at time points i and (i + 1).
Data were processed in Microsoft Excel. All data were expressed as mean with standard deviation (mean ± SD) for each treatment and the experiment was repeated three times. One-way anova was used to assess data based on the average of triplicate observations. Analysis of significant differences among treatments was conducted by using SPSS version 11.5 software (SPSS, IL, Chicago, USA) to compare the means of three replicates using Tukey's test at P < 0.05.
Effect of different dosages of ADS on methane emission from paddy field soil
Results indicate that CH4 emission fluctuated in a duration and fertilizer dependent manner during the entire rice growth period. CH4 emission fluxes were initially small for all treatments and rapidly increased 15 days after seedling transplant. Peak flux was reached (over 85 mg m−2h−1) in 20 days, followed by a gradual decrease to normal levels after 45 days. The minimum levels were reached after 106–120 days. This pattern was found in all treatments (Figs 1 and 2). CH4 emission testing was focused on the growth stages from tillering to mid-season drainage (a farming practice of sun-drying field to remove water from soil in the end of rice plant growth in China) for all treatments. After seedling transplantation, a small amount of CH4 emission was observed due to persistent waterlog while emission was significantly elevated after tillering and fertilizer use. CH4 emission persisted for a shorter duration (about 20 days) after heading (earring) fertilizer application at the end of the growth season. Little CH4 emission was observed in the late stage of rice cultivation.
Effect of different ADS dosage on gross CH4 emission during rice plant growth
Differing effects of varied dosages of ADS on cumulative CH4 emission were found during all growth stages of rice plants (Fig. 3). The lowest emissions were observed in control treatments with 14 g m−2 in 2008 and 30 g m−2 in 2009. Cumulative CH4 emission gradually increased with the increasing use of ADS. Low seasonal gross CH4 emission was observed in the treatment of 25% chemical N replaced by ADS, followed by the treatment of 50% chemical N replaced by ADS and 75%, and 100% chemical N replaced by ADS. In 2008, the largest cumulative CH4 emission (33 g m−2) was observed in the treatment where 100% chemical N was replaced by ADS (Fig. 3a). However, the cumulative CH4 emission in the same treatment in 2009 was not the highest (Fig. 3b). Cumulative CH4 emissions in the treatments of ADS were higher than those in the pure chemical fertilizer treatment. Cumulative CH4 emission for the same treatment differed between 2008 and 2009. Overall, emissions in 2008 were twice as large as those in 2009.
Effect of drying field on CH4 emission fluxes from paddy field soil in different treatments
China has its own traditional rice growing techniques which include drying the field in the middle of the growth season to stimulate grain filling and fruiting to increase yields. This mid-season drainage is a farming practice which drains the paddy field to keep the topsoil dry for about 1 week. Average CH4 emission fluxes before, during, and after mid-season drainage varied among treatments (Fig. 2). Results demonstrated that CH4 emission fluxes before mid-season drainage in all treatments were greater than those during mid-season drainage, while the emission during mid-season drainage was greater than that after mid-season drainage. Compared to the period before mid-season drainage, average CH4 emission fluxes were decreased, while the fluxes were much lower after mid-season drainage. Fluxes were generally different among treatments. Typically, the fluxes in control treatment were the smallest (Table 2). All estimates of fluxes in 2008 were higher than those in 2009 (Table 2), which might reflect the occurrence of more rain leading to lower air temperature and decreased activities of microorganisms in soil related to methane formation in 2009. The farming practice of mid-season drainage markedly reduced CH4 emissions after mid-season drainage; although it somewhat affected emissions during mid-season drainage.
Table 2. Effects of different fertilizer types, application rates, and application timing on CH4 emission flux from paddy field soil during different growth stages of rice plants in 2008–2009 (mg m−2 h−1). Means ± standard deviation. Treatments with the same letter were not significantly different in post hoc tests (P <0.05). See Table 1 for treatment details
Before mid-season drainage
After mid-season drainage
Whole growth season
7.99 ± 1.57a
4.55 ± 0.83a
1.28 ± 0.29a
4.76 ± 0.95a
12.3 ± 2.15c
6.14 ± 1.11bc
1.78 ± 0.23b
6.15 ± 1.13b
10.00 ± 1.82b
5.86 ± 1.37b
1.37 ± 0.27ab
5.78 ± 1.25ab
13.56 ± 2.17 cd
7.51 ± 1.17c
2.43 ± 0.42 cd
7.25 ± 2.31b
15.22 ± 2.91d
9.33 ± 2.85de
3.20 ± 0.35e
7.66 ± 1.63bc
22.13 ± 6.12e
14.09 ± 1.57e
3.47 ± 0.48ef
11.34 ± 2.34c
12.94 ± 2.57c
6.36 ± 0.83bc
2.15 ± 0.37c
7.03 ± 1.73b
13.65 ± 1.73 cd
8.73 ± 2.17d
2.42 ± 0.27 cd
7.30 ± 1.49b
0.47 ± 0.05a
0.74 ± 0.08a
1.14 ± 0.12de
2.31 ± 0.27f
0.77 ± 0.09b
0.89 ± 1.01b
0.84 ± 0.09c
1.81 ± 0.25de
1.18 ± 0.26 cd
1.07 ± 0.23bc
0.53 ± 0.11ab
0.89 ± 0.29b
0.81 ± 0.17bc
2.11 ± 0.33e
0.86 ± 0.15c
1.16 ± 0.35c
1.40 ± 0.19d
0.99 ± 0.17bc
0.57 ± 0.15ab
0.90 ± 0.17b
1.06 ± 0.27c
1.33 ± 0.31c
0.99 ± 0.24d
2.20 ± 0.41f
0.96 ± 0.15c
1.55 ± 0.34d
0.43 ± 0.08a
0.72 ± 0.14a
1.54 ± 0.31de
1.64 ± 0.32de
0.70 ± 0.12b
1.70 ± 0.23d
Though significant differences were observed among most treatments in mid-season drainage, the ratios of cumulative CH4 emission to seasonal cumulative CH4 emission during the whole rice growth period were almost the same. Different CH4 emission fluxes were observed at different years resulting in varying contributions to seasonal cumulative CH4 emission in paddy field soil: 8.75–11.39% in 2008 and 2.26–3.60% in 2009 (Table 3).
Table 3. Effects of different fertilizer types, application rates, and application timing on average cumulative CH4 emission over the entire growing season, CH4 emission during mid-season drainage, and the percent of total emissions from mid-season drainage. See Table 1 for treatment details
Cumulative CH4 emission: whole growth season (g m−2)
Successive two-year (2008–2009) results demonstrated that seasonal cumulative CH4 emissions in paddy field plots treated with fertilizer, both chemical fertilizer and liquid fertilizer from methane-generating pits (ADS), were significantly greater than unfertilized controls (Figs 1 and 2). This result was likely due to biogas sewage use, which has previously been shown to increase CH4 emission from paddy fields (Zou et al., 2009), whereas the result was inconsistent with the finding of lower methane emissions from rice fields amended with biogas slurry from farm yard manure (Dehnath et al., 1996). Methane is exclusively produced by methanogenic bacteria that can metabolize only in the strict absence of free oxygen and at redox potentials of less than −150 mV. In wetland rice soils, methane is largely produced by transmethylation of acetic acid and, to some extent, by the reduction of carbon dioxide (Neue, 1993).
CH4 emission was very low in the control treatment likely from inhibition of microbes due to lack of nutrients and suitable reducing substrates; however, CH4 emissions were significantly greater in the plots treated with chemical fertilizer and ADS, presumably because sufficient nutrients and reducing substrates for methane-producing microorganism were present. The greater seasonal cumulative CH4 emissions from paddy fields in which chemical fertilizer nitrogen was partially or wholly replaced by ADS could be ascribed to more organic components (soluble and easily transformed organic molecules), which supply more reducing substrates for methane-producing microbes in soil.
CH4 produced in soil is often oxidized by some methanotrophic bacteria. An important factor controlling soil CH4 oxidation is nitrogen (N) fertilization. Ammonium-based (NH4) fertilizers frequently reduce soil CH4 uptake (Dunfield & Knowles, 1995; Willison et al., 1995). Paddy fields amended with organic matter increased methane emission (Agnihotri et al., 1999). These observations have been related to the finding that ammonia can competitively inhibit CH4 oxidation by methanotrophs (Whittenbury et al., 1970; Gulledge & Schimel, 1998). However, this decreased CH4 emission by N only took place under drought conditions (Petra et al., 2011). In this study, the case was just the reverse. Furthermore, the increased CH4 emissions may also reflect methane-producing microbes contained in ADS (from CH4 formation in methane-generating tanks) that led to greater abundances of methane-producing microbes in paddy field soil where it was applied.
Variations in annual average CH4 emission fluxes for all treatments in paddy fields were observed likely due to fluctuating air temperatures during paddy rice growth. This agrees with many studies (Zou et al., 2009; Shang et al., 2011), but contradicts the application of ammonium-based fertilizers at widely applied rates, which usually inhibit CH4 emission from rice fields as compared to no N addition (Xie et al., 2010). Meanwhile, CH4 emission flux was associated with plant growing condition, farming management, and climate (Yu et al., 1994), as the population level of methanogenic bacteria differed significantly in root exudates of rice in soil (Wang & Adachi, 2000).
In this investigation, the contribution to overall CH4 emission flux from the earlier stage of rice growth was nearly the same across treatments, which was ascribed to lower air temperature and soil temperature that lead to lower biomass of paddy rice and small amounts of root exudates when seedlings are transplanted. Furthermore, aerobic cropping of wheat before the rice growing season likely caused there to be relatively few active methane-producing microorganisms in soil, consequently resulting in little CH4 emission in the earlier stages of rice cultivation (Figs 1 and 2). With increasing air and soil temperatures, rice seedlings grow quicker resulting in elevated metabolism to biosynthesize more organic compounds, which increases root vigor and root exudates. Subsequently, with prolonged soil flooding and aerobic decomposition of soil organic matter, decreasing oxidation potentials in soils gradually lead to an anaerobic state. This increases the diversity and density of methane-producing microbes that increase CH4 emission, which peaked 20–30 days after seedlings were transplanted (Figs 1 and 2). At this time, rice tillering began and tillering fertilizer was applied. This led to peak growth of rice accompanying the most anaerobic state in soil. This creates optimal conditions for microbe growth and methane production: anaerobic soils, high nutrient levels, and abundant reducing substrates.
Field drying is a novel technique and farming practice initiated in China over a hundred years ago. The drying field technique is a practical tactic which aims to suppress excessive growth and tillering that leads to ineffective rice heading by draining paddy field soil for about 1 week. Though short in duration, this mid-season drainage strongly inhibits strictly anaerobic methane-producing microorganism growth. By aerating and drying the soil for several days, this results in much fewer methane-producing microbes that make less CH4, independent of nutrients and reducing substrates accumulated, which in this short duration account for 2.2–11.6% of emissions (Figs 1 and 2; Tables 2 and 3). This agrees with studies by Zou et al. (2009), Hou et al. (2000) and Shang et al. (2011). A significant difference was found in CH4 emission in paddy field soil treated or untreated with fertilizers in normal growth conditions, however, during mid-season drainage, CH4 emissions did not vary among treatments. It has been suggested that the majority of CH4 emissions are in the period between tillering fertilizer and mid-season drainage which could be thought as the key stage to control CH4 emission. Intermittent shorter durations of drainage and drying farming fields in such crucial moments might further cut CH4 emissions in paddy field (Yagi & Minami, 1990). It was also proposed that intermittent drainage can be an appropriate technology option to reduce the greenhouse gas emission from paddy soil (Agnihotri et al., 1999; Wang et al., 1999; Corton et al., 2000; Hadi et al., 2010). Application of anaerobic digestion slurry, as a fertilizer source in paddy fields, should be avoided until research is conducted to provide ways to reduce the methane emissions when the slurry is used.
In this study, types and quantities of fertilizer significantly affected CH4 emissions in fields. Partial chemical fertilizer nitrogen substitution by ADS significantly elevated the rate and amount of CH4 emissions from paddy fields over the entire rice growth period. Furthermore, cumulative CH4 emissions increased with increasing proportions of chemical fertilizer N replaced by ADS and the highest CH4 emission was associated with the 100% ADS treatment (Fig. 2). This agrees with the finding that application of rice straw to paddy fields increased CH4 emission rates. Application of compost slightly increased emissions (Yagi & Minami, 1990; Qin et al., 2010). Compared with controls, CH4 emissions in plots treated by ADS increased by 40–70% (2008) and 48–84% (2009). When compared to pure chemical fertilizer, CH4 emissions in those plots treated by ADS increased by 8–84% (2008) and 3–26% (2009). It indicated that biogas slurry liquid fertilizer can significantly increase cumulative CH4 emissions from paddy fields which make it difficult to combine development of renewable methane supplies, reduction of pollution from agricultural solid wastes, and production of large amounts of superior organic fertilizer which would be helpful for sustainable agricultural development. In fact, scientists, agricultural decision-makers, and growers should be concerned about increased CH4 emissions resulting from application of biogas slurry liquid in paddy field and they should consider measures, such as intermittent shorter duration of drying fields to mitigate CH4 emission and minimize the risk of global climate change.
In conclusion, fertilizer, especially nitrogen fertilizer increases CH4 emission in paddy field soils. In addition, much larger and significant increases in CH4 emissions were caused by using biogas slurry liquid fertilizer (anaerobic digestion slurry) from a methane-generating tank as the source of nitrogen fertilizer.
This work was financially supported by Ministry of Science and Technology of China, Project in the National Science & Technology Pillar Program during the Eleventh Five-Year Plan Period (2006BAD17B06) and Ministry of Agriculture, Special Fund for Agro-scientific Research in the Public Interest (200903011-01) and Jiangsu Provincial Government Independent Innovation Fund for Agricultural Science and Technology (cx(10)205). Thanks also to Drs. Tiffany Weir (Colorado State University) and Evan Siemann (Rice University) for their help in editing and correction of manuscript.