Effects of different organic fertilizers on nitrous oxide and methane emissions from double-cropping rice fields

Mingcheng HU ,Andrew J.WADE ,Weishou SHEN,* ,Zhenfang ZHONG ,Chongwen QIU and Xiangui LIN

1Jiangsu Key Laboratory of Atmospheric Environment Monitoring and Pollution Control,Collaborative Innovation Center of Atmospheric Environment and Equipment Technology,School of Environmental Science and Engineering,Nanjing Universityof Information Science&Technology,Nanjing 210044(China)

2Department of Geography and Environmental Science,University of Reading,Reading RG6 6DW(UK)

3Haina Research Institute of Guangdong Haina Agricultural Co.,Ltd.,Huizhou 516000(China)

4State Key Laboratory of Soil and Sustainable Agriculture,Institute of Soil Science,Chinese Academy of Sciences,Nanjing 210008(China)

ABSTRACT Rice fields are a major source of greenhouse gases,such as nitrous oxide(N2O)and methane(CH4).Organic fertilizers may potentially replace inorganic fertilizers to meet the nitrogen requirement for rice growth;however,the simultaneous effects of organic fertilizers on N2O and CH4 emissions and crop yield in paddy fields remain poorly understood and quantified.In this study,experimental plots were established in conventional double-cropping paddy fields in the Pearl River Delta,China,including an unfertilized control and five fertilizer treatments with fresh organic fertilizer(FOF),successively composted organic fertilizer(SOF),chemically composted organic fertilizer(COF),COFsupplemented with inorganic fertilizer(COIF),and chemical fertilizers(CFs)(TFOF,TSOF,TCOF,TCOIF,and TCF,respectively).Paddy field soils behaved simultaneously as an N2O sink(cumulative N2O emission:-196to-381 g N ha-1)and as a CH4 source(cumulative CH4 emission:719 to 2 178 kg ha-1).Compared to CFs,the effects of organic fertilizers on N2O emission were not significant.In contrast,total annual CH4 emission increased by 157%,132%,125%,and 37%in TFOF,TCOF,TSOF,and TCOIF,respectively,compared to TCF.In TCOIF,rice yield was maintained,while CH4 emission was not significantly increased from the paddy fields characterized by a prolonged flood period.An important next step is to extend these field-based measurements to larger rice cultivation areas to quantify the regional and national-scale impacts on greenhouse gas emissions and to help determine the optimum practice for fertilizer use.

Key Words:crop production,global warming potential,greenhouse gases,manure,paddy,sustainable agriculture

INTRODUCTION

Rice fields are a significant source of nitrous oxide(N2O)and methane(CH4)(Bhattacharyyaet al.,2013;Das and Adhya,2014;Songet al.,2021).Soil microorganisms degrade soil organic matter(OM)in paddy fields through a series of complex aerobic,anaerobic,and facultative anaerobic biochemical reactions.These processes can produce N2O and CH4,and soil OM determines the resulting N2O and CH4emissions to a certain extent in paddy fields(Das and Adhya,2014;Valenzuela and Cervantes,2021).Nitrous oxide is an important greenhouse gas in the atmosphere,and its global warming potential (GWP) is 273 times that of CO2over a 100-year time horizon(Shenet al.,2022).Atmospheric N2O produces secondary pollutants such as nitric acid and nitrate particles through a series of oxidation reactions.The generated secondary pollutants can enter wetlands,forests,lakes,grasslands,and other surface ecosystems through dry and wet deposition,resulting in soil and water acidification,as well as water eutrophication(Guoet al.,2010;Qiaoet al.,2012).Additionally,CH4is another important greenhouse gas,with an estimated contribution rate of 14%to the global greenhouse effect and GWP being 27 times that of CO2on a 100-year scale(Shenet al.,2022).

China is the largest producer and consumer of mineral nitrogen(N)fertilizer globally,and the application rate of nitrogenous fertilizers in China accounts for approximately one-third of the total amount of nitrogenous fertilizers used worldwide(Zhaoet al.,2014;Chenet al.,2015).Nitrogen use efficiency in China is relatively low,with approximately two-thirds of the N applied as inorganic fertilizers being lost through gaseous N loss,such as N2O emission and NH3volatilization(Zhanet al.,2021;Zhaoet al.,2021).

Application of chemical fertilizers(CFs)could increase crop yield and promote economic development;however,long-term excessive application of CFs could lead to a series of negative environmental effects,such as the reduction of soil fertility and OM content.Due to the high environmentand human health-related risks caused by excessive mineral fertilizer application,the alternative use of organic fertilizer is now receiving increasing attention,partly because it is regarded as a convenient means of using a waste product to replace mineral fertilizer application(Baruah and Baruah,2015;Songet al.,2021).Organic fertilizers,primarily made of plant waste and animal manure,may also include food waste and solid residues from biogas production(Suet al.,2014;Baruah and Baruah,2015;Zhonget al.,2021).Compared with CFs,organic fertilizers have many positive effects on paddy fields,including increasing soil carbon(C)and N contents,improving soil physical structure,and enhancing crop yield and quality(Dillonet al.,2012;Zhaoet al.,2014,2020).

On a field-plot scale,N2O and CH4emissions are highly variable and depend on multiple factors,including the raw materials used in the production of organic fertilizers,application rate,and fertilization period (Baruah and Baruah,2015;Zhanget al.,2016;Mohantyet al.,2020;Nanet al.,2020;Songet al.,2021).However,there are few reports on the effects of organic fertilizers produced using different production techniques on N2O and CH4emissions in paddy fields.Of those that are reported,they have primarily focused on single-cropping rice fields in the eastern and central regions in China,while studies on double-cropping rice fields in southern China are relatively scarce (Zhanget al.,2020;Islam Bhuiyanet al.,2021).A more complete exploration of regional differences is important because N2O and CH4emissions from paddy fields depend on organic fertilizer type and application amount,as well as soil type(Islam Bhuiyanet al.,2021).Therefore,the aim of this study was to evaluate the effects of organic fertilizers on N2O and CH4emissions in double-cropping paddy fields in southern China.These organic fertilizers were produced by different processes,including fresh organic fertilizer(FOF)and successively composted organic fertilizer(SOF)produced by traditional techniques and chemically composted organic fertilizer(COF)produced by the latest-model composting technology.To achieve the aim,two objectives were defined.The first was to quantify the effects of CFs and various organic fertilizers,all with an identical equivalent N application amount,on N2O and CH4emissions in a double-cropping rice field in the Pearl River Delta,southern China.The second objective was to assess our findings in terms of soil fertility improvement,N management strategy,and development of environmently friendly organic fertilizers.

MATERIALS AND METHODS

Experimental location

A field experiment was conducted in Huizhou City,Guangdong Province,China(23°1′N,114°5′E)(Fig.S1,see Supplementary Material for Fig.S1).Huizhou has a subtropical monsoon climate,with an average annual temperature of 22°C and an average annual precipitation of approximately 2 200 mm.Huizhou is the main rice-planting area in the Pearl River Delta of China.The primary rice planting mode in this region is double cropping,including the early-and late-season rice.The soil is classified as an Anthrosol with a pH(H2O)of 5.8,an organic C content of 18.6g kg-1,and total N,phosphorus,and potassium contents of 1.1,0.9,and 18.9 g kg-1,respectively,determined in samples collected from the 0-20 cm soil layer.

Fertilizer manufacture

We selected two widely used traditional production processes and a latest-model process for the preparation of organic fertilizers.Chicken manure from livestocks and poultry farms was selected as the raw material for organic fertilizer production.The organic fertilizers produced by the two traditional organic fertilizer-manufacturing processes included FOFand SOF.The FOFwas made of fresh chicken manure collected from livestocks and poultry farms without any additional physical or chemical treatment.The SOF was produced by composting fresh chicken manure into organic fertilizer(Das and Adhya,2014;Valenzuela and Cervantes,2021).The latest-model composting technology may promote physical and chemical decomposition of chicken manure by adding chemical decomposing agents,along with high-temperature treatment,to produce chemically composted organic fertilizer(COF).This new composting technology can potentially shorten the production cycle of organic fertilizers and kill pathogenic microorganisms in organic materials.In addition,COFsupplemented with inorganic fertilizer(COIF)was also prepared.

Experimental design and field management

Six treatments were set up in this study,including an unfertilized control(CK)and five fertilized treatments with CFs(TCF),FOF(TFOF),SOF(TSOF),COF(TCOF),and COIF(TCOIF).The amount of N applied was the same for all fertilized treatments,i.e.,105 kg N ha-1(Table I).Four replicates were set in four plots(7.5 m×5.7 m each)for each treatment.

The rice variety used was Meixiangzhan 2,which has a growing period of approximately four months.The row spacing was approximately 20 cm.Seedling transplanting,field management,and grain harvest were the same for both the early-and late-season rice,and field management followed the conventional practices of local farmers.Before the beginning of the experiment,the experimental plots were flooded for 1-2 weeks,and then cultivated and harrowed.Basal fertilizer was applied and rice seedlings were transplanted on March 29,2019.Approximately one month aftertransplanting,the field plots were flooded again by artificial irrigation,and then there was 2-4 weeks of mid-season drainage,followed by one more waterflooding.Finally,water was drained,and the plots dried over the last 10 d of the maturity stage.Drying allowed harvesting the early-season rice on July 15,2019.Late-season rice was applied with a basal fertilizer on August 8,transplanted on August 10,and harvested on November 15,2019(Fig.1).

Fig.1 Field management of paddy fields during the early-season(a)and late-season(b)rice growing periods in a field experiment conducted in 2019 in Huizhou City,Guangdong Province,China.

TABLE IFertilization strategies of each treatmenta) in a field experiment conducted in Huizhou City,Guangdong Province,China

Static chamber-gas chromatographic techniques

Emissions of N2O and CH4were measured using static chambergas chromatography (Liet al.,2020).Before the experiment,24 square base frames(0.5×0.5 m)were inserted 20 cm into the soil in the center of each plot.Small gas chambers(0.5-m long×0.5-m wide×0.6-m high)or large gas chambers(0.5-m long×0.5-m wide×1-m high)were used to collect gas samples depending on the height of the rice plants.During gas sampling,the chamber was placed onto the frame,which had a 2-cm wide×3-cm deep groove.Water was added to the groove during sampling to ensure air-tightness of the entire gas collection device.Sampling was performed at 3-d intervals during the first 2 months after transplanting,and then at 5-d intervals.The specific sampling dates were determined based on the real-time weather and actual experimental conditions,and the sampling time was between 8:00 a.m.and 12:00 a.m.In each plot,three 40-mL gas samples were collected using a 100-mL plastic syringe with a 3-way stopcock at 0,15,and 30 min after the chamber was placed onto the frame.The air temperature inside the chamber was measured when each gas sample was taken using a portable digital electron probe thermometer(TP677,MITIR Co.,Ltd.,China)installed in the reserved hole on the top of the chamber.The collected gas samples were injected into vacuum glass bottles and immediately sent to the laboratory for further analysis.The N2O and CH4concentrations in the gas samples were analyzed by gas chromatography(Agilent GC-7890B,Agilent Technologies,USA)using an electron-capture detector for N2O concentration measurement and a flame ionization detector for CH4concentration measurement.Emission fluxes of N2O and CH4were calculated using Eq.1(Liet al.,2020):

whereFis the emission flux of N2O (μg m-2h-1) or CH4(mg m-2h-1),ρis the gas density of N2O(1 340 μg cm-3)or CH4(0.717 mg cm-3)under standard conditions(0°C,101 kPa),His the height of the chamber above the water layer (m),Δtis the sampling interval time (h),Δcis the concentration change of N2O(μg m-3)or CH4(mg m-3)within Δt,Δc/Δtis the cumulative emission rate of N2O(μg m-3h-1)or CH4(mg m-3h-1)in the chamber,andTis the mean temperature inside the chamber at each sampling(°C).

Cumulative emissions,GWP,greenhouse gas intensity(GHGI)and emission intensity of N2O and CH4

Cumulative emissions(S)of N2O(g N ha-1)and CH4(kg ha-1)were calculated using Eq.2(Liet al.,2020):

whereiis theith sampling,nis the total number of sampling times,Fiis the N2O(μg m-2h-1)or CH4(mg m-2h-1)emission flux for theith sampling,and (ti+1-ti) is the interval of days between theith and(i+1)th sampling.Global warming potential refers to the radiative forcing potential of the two greenhouse gases converted to the carbon dioxide equivalent(CO2-eq)based on a 100-year scale(Mosieret al.,2005).The GWP of N2O and CH4(kg CO2-eq ha-1)were calculated using Eq.3(Qiet al.,2020):

wherefis the GWP coefficient of N2O(273 kg CO2-eq)or CH4(27 kg CO2-eq).Greenhouse gas intensity(kg CO2-eq kg-1),which relates GWP to rice yield(Y,kg ha-1),was calculated using Eq.4(Qiet al.,2020):

The emission intensity (T) of N2O (mg N kg-1) and CH4(g kg-1) were calculated using Eq.5 (Chenget al.,2010):

Statistical analysis

One-way analysis of variance(ANOVA)was performed followed by a least significant difference(LSD)test using IBM SPSS Statistics(version 21.0)to assess the differences in emission fluxes,cumulative emissions,GWP,GHGI,and emission intensity of N2O and CH4among the six different treatments.

RESULTS

N2O emission flux

The N2O emission flux from the double-cropping rice field in 2019 occurred mainly within the mid-season drying period for both the early-and late-season rice(Fig.2)and was mostly negative.During the early-season rice growing period,N2O emission flux for different treatments ranged between-22.68 and 27.16μg N m-2h-1and the mean N2O emission flux of each treatment ranged from-9.51 to-5.75 μg N m-2h-1(Fig.2a,Table II).Only two N2O emission peaks were particularly noticeable:one on April 7,2019 in TCOIFand another on May 17,2019 in TCFduring the early-season rice growing period.Mean N2O emission flux in fertilized treatments was not significantly different from that in CK during the early-season rice growing period(Table II).During the late-season rice growing period,N2O emission flux in different treatments ranged between-138.55 and 64.3 μg N m-2h-1and the mean N2O emission flux of each treatment ranged from-10.01 to 1.24 μg N m-2h-1(Fig.2b,Table II).Furthermore,there was an absorption trough of N2O on September 13,2019 and an N2O emission peak on September 16,2019 both in TFOF.Compared with TCFduring the late-season rice growing period,mean N2O emission flux in TCOFsignificantly increased by 112%(P ＜0.05),whereas those in TFOF,TSOF,and TCOIFdidn’t significantly increase(Table II).

Fig.2 Emission flux of N2O from paddy fields after applying chemical and organic fertilizers during the early-season(a)and late-season(b)rice growing periods in a field experiment conducted in 2019 in Huizhou City,Guangdong Province,China.Values are means and standard deviations(n=4).CK=control with no fertilizer;TCF,TFOF,TSOF,TCOF,and TCOIF=treatments applied with chemical fertilizers,fresh organic fertilizer,successively composted organic fertilizer,chemically composted organic fertilizer(COF),and COFsupplemented with inorganic fertilizer,respectively.

Cumulative N2O emission and N2O emission intensity

During the growing period of the early-season rice,the cumulative N2O emission was negative for all treatments,indicating an overall N2O uptake in paddy fields(Table II).The cumulative N2O uptake was the highest in TCOF,followed by TSOF,TCOIF,TFOF,TCF,and CK.Compared to TCF,the cumulative N2O uptake increased by 6%,22%,46%,and 52%in TFOF,TCOIF,TSOF,and TCOF(P ＞0.05),respectively.Similarly,during the growing period of late-season rice,the cumulative N2O emission for the different treatments were negative,except for TCOF.Compared to TCF,the cumulative N2O emission in TCOFwas significantly higher (P ＜0.05),and the N2O uptake in TSOF,TCOIF,and TFOFwas not significantly different from that in TCF.Total N2O emission during the whole year from different treatments followed this order:CK＞TCOF＞TSOF＞TFOF＞TCOIF＞TCF.In addition,total N2O emission in the different chemical and organic fertilizer treatments showed no significant differences in comparison to the unfertilized control.

TABLE IIMean emission flux,cumulative emission,and emission intensity of N2O from paddy fields after applying chemical and organic fertilizers in the early-season(ESR)and late-season(LSR)rice growing periods in a field experiment conducted in 2019 in Huizhou City,Guangdong Province,China

Except for TCOFduring the late-season rice growing period,N2O emission intensity was negative for all the treatments during the early-and late-season rice growing periods (Table II).Total N2O emission intensity for the whole year was the highest in TCOF,followed by TCOIF,CK,TFOF,and TSOF,while the lowest was observed in TCF.Total N2O emission intensity for the whole year increased by 10%,11%,22%,and 36%in TSOF,TFOF,TCOIF,and TCOF,respectively,compared to TCF(P ＞0.05).

CH4 emission flux

During the early-season rice growing period,CH4emission occurred mainly within 75 d after rice transplanting,and then after that the CH4emission flux for each treatment was steady and close to zero(Fig.3a),fluctuating with an overall decrease during the growing period.Further,mean CH4emission flux for each treatment followed the order:TFOF＞TCOF＞TSOF＞TCOIF＞TCF＞CK.Therefore,compared to CK,the mean CH4emission flux in the chemical fertilizer and the four organic fertilizer treatments showed a significant increase.Compared to TCF,the mean CH4emission flux in TCOFand TFOFmarkedly increased by 62%and 69%,respectively(Table III).In contrast,during the late-season rice growing period,CH4emission mainly occurred within 45 d after transplanting,approximately 30 d in advance compared with that in the early-season rice growing period.Mean CH4emission flux was the highest in TFOF,followed by TSOF,TCOF,TCOIF,and CK,and was the lowest in TCF.Compared with TCF,the four organic fertilizer treatments enhanced CH4emission flux.

Fig.3 Dynamic variation of CH4 flux from paddy fields after applying chemical and organic fertilizers in the early-season(a)and late-season(b)rice growing periods in a field experiment conducted in 2019 in Huizhou City,Guangdong Province,China.Values are means and standard deviations(n=4).CK=control with no fertilizer;TCF,TFOF,TSOF,TCOF,and TCOIF=treatments applied with chemical fertilizers,fresh organic fertilizer,successively composted organic fertilizer,chemically composted organic fertilizer(COF),and COFsupplemented with inorganic fertilizer,respectively.

Cumulative CH4 emission and CH4 emission intensity

During the early-season rice growing period,cumulative CH4emission was the greatest in TFOF and ordered as follows:TFOF＞TCOF＞TSOF＞TCOIF＞TCF＞CK(Table III).Compared with CK,CFand the four organic fertilizer treatments significantly enhanced CH4emission(P ＜0.01).Compared with TCF,cumulative CH4emission increased by 4%(P ＞0.05),26%(P ＞0.05),58%(P ＜0.05),and 67%(P ＜0.05)in TCOIF,TSOF,TCOF,and TFOF,respectively(Table III).During the late-season rice growing period,cumulative CH4emission ranked in the following order:TFOF＞TSOF＞TCOF＞TCOIF＞CK＞TCF.Compared with TCF,CH4emission in TCOIF,TCOF,TSOF,and TFOFincreased by 145%(P ＜0.05),381%(P ＜0.01),457%(P ＜0.01),and 458%(P ＜0.01),respectively.Furthermore,TFOF showed the maximum cumulative CH4emission throughout the whole year among the treatments(2 177 kg ha-1),followed by TCOF(1 969 kg ha-1),TSOF(1907 kg ha-1),TCOIF(1158 kg ha-1),TCF(848 kg ha-1),and CK(719 kg ha-1).Compared with TCF,cumulative CH4emission increased significantly by 125%,132%,and 157%in TSOF,TCOF,and TFOF,respectively,and increased by 37%in TCOIF,although not significantly.

Among all treatments,CH4emission intensity followed this order:TFOF＞TCOF＞TSOF＞TCOIF＞TCF＞CK during the early-season rice growing period,TSOF＞TCOF＞TFOF＞CK＞TCOIF＞TCFduring the late-season rice growing period,and TFOF＞TCOF＞TSOF＞CK＞TCOIF＞TCFin the whole year(Table III).It increased by 149%(P ＜0.05),148%(P ＜0.05),144%(P ＜0.05),and 33%(P ＞0.05)in TFOF,TCOF,TSOF,and TCOIF,respectively,compared to TCFin the whole year.

N2O and CH4 GWP and GHGI

To evaluate the combined greenhouse effects of N2O and CH4emissions from the double-cropping rice fields,GWP of N2O and CH4were calculated for the different fertilizer treatments(Table IV).The N2O-GWP in the different treatments were all negative during both the early-and late-season rice growing periods,except in TCOFduring the late-season rice growing period(5 kg CO2-eq ha-1).Total N2O-GWP for the whole year showed no significant variation between CF and the four organic-fertilizer treatments.For each treatment,CH4-GWP was much higher than N2O-GWP.The CH4-GWP ranked as follows:TFOF＞TCOF＞TSOF＞TCOIF＞TCF＞CK during the early-season rice growing period,with CH4-GWP in TCOFand TFOFbeing 58%and 67%higher than that in TCF,respectively(P ＜0.05).During the late-season rice growing period,CH4-GWP followed this order:TFOF＞TSOF＞TCOF＞TCOIF＞CK＞TCF,and CH4-GWP in TCOIF,TCOF,TSOF,and TFOFwas 145%,381%,457%,and 458% higher than that in TCF,respectively(P ＜0.01).Additionally,total GWP for N2O and CH4for the whole year followed this order:TFOF＞TCOF＞TSOF＞TCOIF＞TCF＞CK,being 37%(P ＞0.05),125%(P ＜0.05),133%(P ＜0.05),and 158%(P ＜0.05)higher in TCOIF,TSOF,TCOF,and TFOFthan TCF,respectively.

TABLE IIIMean emission flux,cumulative emission,and emission intensity of CH4 from paddy fields after applying chemical and organic fertilizers in the early-season(ESR)and late-season(LSR)rice growing periods in a field experiment conducted in 2019 in Huizhou City,Guangdong Province,China

Total N2O-GHGI for the whole year ranged from-9 to-5 g CO2-eq kg-1,with no significant difference among the different treatments(Table V).Meanwhile,CH4-GHGI was much higher than N2O-GHGI in each treatment.Total CH4-GHGI for the whole year followed the order:TFOF＞TCOF＞TSOF＞CK＞TCOIF＞TCF.Similarly,total GHGI of N2O and CH4for the whole year followed this order:TFOF＞TCOF＞TSOF＞CK＞TCOIF＞TCF,being 33% (P ＞0.05),145% (P ＜0.05),149% (P ＜0.05),and 150%(P ＜0.05)higher in TCOIF,TSOF,TCOF,and TFOFthan TCF,respectively.

DISCUSSION

Effects of organic fertilizers on N2O emission

During both the early-and late-season growing periods in 2019,N2O emission in each fertilization treatment occurred mainly during the mid-season drying period(Figs.1 and 2),confirming the results of previous studies (Ahnet al.,2014;Ribaset al.,2019).Further,consistent with the findings of Diet al.(2014) and Dowhoweret al.(2020),this study showed that soil moisture directly influenced soil nitrification and denitrification,causing variations in N2O emission flux(Figs.2 and S2,see Supplementary Material for Fig.S2).Both conventional organic fertilizers(FOFand SOF)and the latest-model organic fertilizer(COF)showed promising effects in mitigating N2O emission from paddy fields (Table II).This result indicated that organic fertilizer substitution strategies could be used to maintain crop production while reducing N2O emission from paddy fields.In this study,total N2O emission for the whole year from double-cropping paddy fields was negative in all treatments.There was N2O uptake in double-cropping rice fields in the Pearl River Delta,therefore,the double-cropping rice fields in this area can be considered an N2O sink during rice-growing seasons.

Previous studies have shown that N2O from soil can be produced by multiple microbial processes such as nitrification,denitrification,nitrifier denitrification,and dissimilatory nitrate reduction to ammonium (DNRA),in which nitrification and denitrification account for approximately 70%of soil N2O emission(Diet al.,2014;Panet al.,2016;Wanget al.,2020).Three reasons have been suggested to explain the low N2O emission and N2O uptake.The first reason is that,during the rice-growing seasons,excessive precipitation led to the flooding of rice fields with a high water level after the application of basal fertilizer (Figs.S2 and S3,see Supplementary Material for Fig.S3).High soil water content inhibited the transport and diffusion of N2O to the atmosphere and kept the soil in an anaerobic state,enhancing soil denitrification to further reduce N2O to N2.Extended denitrification not only consumes N2O produced by soil,but also reduces N2O diffused into soil from atmosphere,showing absorption of atmospheric N2O(Phillipset al.,2009;Diet al.,2014;Yaoet al.,2019).The second reason is that the four organic fertilizer treatments were only applied with basal fertilization before rice transplanting and the basal and tillering fertilization were applied to TCFwithin 25 d after rice transplanting(Table I,Fig.1).Therefore,all fertilization events occurred during the period when the plots were flooded after rice transplanting.During the flooding period,most of the available N was likely consumed by denitrification,rice growth,and soil methanogens(Table III),which accounts for the reduction in available N used to produce N2O in the mid-season drying period (Panet al.,2016;Mohantyet al.,2020;Timilsinaet al.,2020).The last reason is that the background soil N content was low and mineral N produced by urea and organic fertilizer hydrolysis,nitrification,and denitrification may have been lost through NH3volatilization,leaching,leakage,and surface runoff,resulting in lower N availability for N2O production(Howarth,2008;Stein,2020;Timilsinaet al.,2020).

Overall,the double-cropping rice field in the Pearl River Delta showed a distinctive characteristic of being an N2O sink.The corresponding key microbial processes and mechanisms of N transformation for N2O emission warrant further study,such as the community and abundance of soil nitrifying bacteria and denitrifying bacteria at different growth stages of rice plants.Further research is also needed to determine the emission characteristics and microbial mechanisms of N2O in the non-rice growing season(winter fallow or winter vegetable growing season) of double-cropping rice fields and to determine whether the double-cropping rice fields in the Pearl River Delta are an N2O sink on the year-round scale(Lianget al.,2007).

The distinctive N2O behavior of double-cropping rice fields in the Pearl River Delta in South China contrasts with other major rice cropping regions in East China (Zhonget al.,2016),North China(Kreyeet al.,2007),Southwest China (Qiet al.,2020),and Central China (Zhanget al.,2016)which show N2O emission rather than uptake.This result implies that the current N2O emission from paddy fields across China,which was mainly estimated using N2O emission data from rice fields in eastern and Central China,is likely to be overestimated.Furthermore,this study highlights the regional variability and complexity of rice field N2O emission,and therefore,the need for more extensive N2O measurement for a range of climate and field management settings throughout the year.

Effects of organic fertilizers on CH4 emission

Addition of exogenous nutrients can enhance the growth and metabolic activities of soil microorganisms and promote the production of CH4by soil methanogens(Dowhoweret al.,2020).All organic fertilizer applications increased CH4emission from paddy fields compared with CFapplications,which is consistent with Mohantyet al.(2020).Compared with TCF,the total CH4emission of the whole year in TFOF significantly increased by 157%.This increase attributed to the diversity and abundance of the microbial population and the content of the dissolved organic C(primarily monosaccharide and fatty acid),which might be easily used by the microorganisms(Das and Adhya,2014).In TFOF,soil microorganisms could quickly use dissolved organic C to produce a high concentration of CH4.Chemically composted organic fertilizer was produced by physicochemical techniques that promoted rotting,and the available organic C and organic N contents in the fertilizer were higher than those in traditional CF,which might promote the growth and metabolism of soil methanogens.Successively composted organic fertilizer was produced by a conventional composting process,and the fertilizer produced has a relatively high availability of organic C,resulting in higher CH4emission(Das and Adhya,2014).However,total CH4emission from TCOIFwas not significantly higher than that from TCF.The COIFconsisted of two components:inorganic N fertilizer with urea and organic N fertilizer with COF.The addition of urea likely decreased the dissolved organic C content in COIF(Das and Adhya,2014;Baruah and Baruah,2015).This result showed that COFcombined with CFsignificantly reduced CH4emission in comparison to FOF,SOF,or COF applied alone,and kept the cumulative CH4emission similar to that from TCF.

The main reason for this observation is that CH4is mainly produced under anaerobic conditions,whereas N2O is mainly produced under aerobic conditions (Serrano-Silvaet al.,2014;Chenget al.,2021;Maieret al.,2021).In the Pearl River Delta region,more precipitation,a longer flooding period,and higher soil moisture led to a predominantly anaerobic environment for most of the rice-growing season,which seemingly promoted the production of CH4while inhibiting the production of N2O (Figs.S2 and S3).The reduction of CH4emission from double-cropping rice fields in the Pearl River Delta should focus on the field flooding stage after transplanting,because it seems to be the most active phase for CH4emission in such rice fields(Fig.3),for example,reducing the height of the field water and decreasing the frequency of fertilization in the flooding stage(Hadiet al.,2010;Lagomarsinoet al.,2016).

Effects of organic fertilizers on GWP and GHGI

Overall,CH4was dominant in the relative contribution of N2O and CH4emissions from paddy fields to the greenhouse effect,resulting in a net increase in greenhouse gas emissions under all organic fertilizer treatments.In contrast,COIF could ensure rice yield and did not significantly enhance the greenhouse effect of paddy fields.Previous studies have shown that the application of conventional organic fertilizers or conventional organic fertilizers combined with CFs in paddy fields might increase soil organic C content and improve soil quality,which plays a role in improving soil fertility and C fixation (Yin and Cai,2006;Shenet al.,2021).Therefore,CH4emission from paddy fields with the application of COIFis at the same level as that from paddy fields with the application of CFs,but it has the advantage of increasing C sink in paddy fields.

Previous studies have shown that the application of conventional organic fertilizers alone or combined with CFin paddy fields would increase the greenhouse effect of paddy fields compared to the application of CFalone (Das and Adhya,2014;Baruah and Baruah,2015;Bharaliet al.,2018;Mohantyet al.,2020).However,compared with conventional organic fertilizers,COIFwould not significantly enhance the greenhouse effect of paddy fields,meanwhile,COIFhas distinctive advantages,including a shorter fertilizer production cycle (approximately one month shorter than SOF),as well as harmless production standards(killing pathogens during fertilizer production).Therefore,the application of COIFon a larger scale of rice production seems worthy of investigation in double-cropping rice cultivation areas.

CONCLUSIONS

The double-cropping rice fields in the Pearl River Delta appear to be a N2O sink during the rice-growing seasons,most likely due to the extended flood periods during rice cultivation.Compared with CFs,the effects of organic fertilizers on N2O emission were not significant;simultaneously,the total CH4emission over the whole year depended on the organic fertilizer type,with increases of 157% (P ＜0.05),132%(P ＜0.05),125%(P ＜0.05),and 37%(P ＞0.05)in TFOF,TCOF,TSOF,and TCOIFrespectively,compared with TCF.The total GWP and GHGI of CH4from paddy fields far outweighed the same indicators for N2O,and thus the reduction of greenhouse gas emissions from paddy fields in the Pearl River Delta region should focus on reducing CH4emission.Chemically composted organic fertilizer supplemented with inorganic fertilizer was found to maintain rice yield,and COIFdid not significantly increase greenhouse gas emissions from paddy fields in the study area characterized by prolonged flooding of rice.An important next step is to extend these field-based measurements to similar rice cultivation areas across the Pearl River Delta to quantify their regional and national-scale impacts on greenhouse gas emissions and fertilizer practices and evaluate if CH4emission is non-significant on a larger scale.

ACKNOWLEDGEMENT

This study was funded by the National Natural Science Foundation of China (No.41771291),the Jiangsu Agricultural Science and Technology Innovation Fund,China(No.CX(21)3183),the Jiangsu Specially Appointed Professor Program,China,and the Jiangsu Six Talent Peaks Program,China(No.NY-083).

SUPPLEMENTARY MATERIAL

Supplementary material for this article can be found in the online version.