Effects of Irrigation Regime and Nitrogen Fertilizer ... · Abstract: Irrigation regime and...

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Effects of Irrigation Regime and Nitrogen FertilizerManagement on CH4, N2O and CO2 Emissions fromSaline–Alkaline Paddy Fields in Northeast China

Jie Tang 1,2, Jingjing Wang 1,2, Zhaoyang Li 2,*, Sining Wang 2 and Yunke Qu 21 Key Laboratory of Groundwater Resources and Environment, Ministry of Education, Jilin University,

Changchun 130012, China; [email protected] (J.T.); [email protected] (J.W.)2 College of Environment and Resources, Jilin University, Changchun 130012, China;

[email protected] (S.W.); [email protected] (Y.Q.)* Correspondence: [email protected]

Received: 30 November 2017; Accepted: 6 February 2018; Published: 11 February 2018

Abstract: Irrigation regime and fertilizer nitrogen (N) are considered as the most effective agriculturalmanagement systems to mitigate greenhouse gas (GHG) emissions from crop fields, but few studieshave involved saline–alkaline paddy soil. Gas emitted from saline–alkaline paddy fields (1-year-oldand 57-year-old) was collected during rice growing seasons by the closed chamber method. Comparedto continuous flooding irrigation, lower average CH4 flux (by 22.81% and 23.62%), but higher CO2 flux(by 24.84% and 32.39%) was observed from intermittent irrigation fields. No significant differences ofN2O flux were detected. Application rates of N fertilizer were as follows: (1) No N (N0); (2) 60 kg ha−1

(N60); (3) 150 kg ha−1 (N150); and (4) 250 kg ha−1 (N250). The cumulative emissions of GHG andN fertilizer additions have positive correlation, and the largest emission was detected at the rate of250 kg N ha−1 (N250). Global warming potential (GWP, CH4 + N2O + CO2) of the 57-year-old fieldunder the N250 treatment was up to 4549 ± 296 g CO2-eq m−2, approximately 1.5-fold that of N0 (noN application). In summary, the results suggest that intermittent irrigation would be a better regimeto weaken the combined GWP of CH4 and N2O, but N fertilizer contributed positively to the GWP.

Keywords: methane; nitrous oxide; carbon dioxide; irrigation regime; N fertilizer; rice paddy;saline–alkali soil

1. Introduction

The burgeoning population and increasing future rice demands have created tremendous concernsabout agricultural greenhouse gas (GHG) emissions, which account for about one-tenth of total globalanthropogenic GHG emissions [1]. The greenhouse warming potential (GWP) of rice crop fields isapproximately 4.6 times and 1.6 times that of wheat and maize, respectively [2]. It is reported thatpaddies cover nearly 153 million ha., approximately 11% of the world’s farmland and 50% of thepeople on the earth are supported by rice [3]. China is the most important producer of rice, of whichcultivated areas and rice yields both account for about 1/5 of the world’s planting area [4].

CO2, which serves as the major greenhouse gas contributor, supplies 60% of the greenhouse effectfrom humans, CH4 and N2O contribute 15% and 5%, respectively [5]. In the global warming potentialfor the one hundred year horizon in terrestrial ecosystems, the contribution of CH4 and N2O is 25 and298 times larger than CO2 respectively [6]. CH4 and N2O fluxes from paddies contribute approximately30% and 11% of rural emissions, and paddies also can be either a source or sink of CO2 [7–9]. Soilmicrobial activities have an effect on the production and uptake of GHG [10] and are impacted bysoil characters (e.g., soil temperature, water content and content of NH4+ and NO3−) [11–15]. Waterregimes and N fertilizer application affect soil moisture, nutrient content and the soil’s physicochemicalproperties and could be effective crop management tools to mitigate GHG emissions.

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Single spring paddy rice is widely cultivated in northeast China, and phenological developmentsaffected by climate change include green, tillering, booting, heading and maturity [16]. CO2 isassimilated and stored in the soil by plants and roots via rice growth. In addition, the labile carbon(C) pool with easily decomposable soil organic matter is decomposed and utilized for crop growthor emission as CH4 or CO2 into the air. Watanabe et al., covered that the translocation of carbonassimilated by rice into the soil organic matter (SOM) with crop growth and that the content of carbonabsorbed by rice and emitted as CH4 tended to increase by 0.003%, 0.26%, and 0.30% at the tillering,booting, and maturity stage, respectively [17]. The fluxes of GHGs, including CO2, CH4 and N2O, arehighly variable during the five phenophases and are strongly affected by agricultural management.

Continuous flooding irrigation (CF) and intermittent flooding irrigation (IF) are common wateringmanagement systems during rice cultivation in northeast China. Methanogenic bacteria whichdecompose the dissolved organic carbon and produce CH4, are active in the CF pattern due tothe anaerobic conditions made by a flooded water layer [18]. Intermittent flooding irrigation, withdrying-wetting alternation during the rice-growing period, has been recognized as a valid way ofmitigating CH4 emission in rice-production [19,20]. Less CH4 fluxes were monitored in IF pattern thanCF paddies [21]. However, other reports have found that the role of intermittent irrigation could benot obvious, compared to flooding irrigation [19]. The effects of different irrigation regimes on cropproduction and gas fluxes may diverge from various practices or exhaust gas emissions for the samepractice in different regions [22].

Nitrogen (N) fertilizer is an effective measure to enhance rice production which will feedmore than a billion people worldwide over the next 30 years [23]. Crop-growth is escalated bynitrogenous fertilizer; sufficient substrates are accommodated for methanogens and the transport ofGHG emissions to the air is easier due to the larger aerenchyma [24]. As reported, CH4 emissions couldbe significantly induced by N fertilization. The size and structure of NH4+ and CH4 are similar, thusCH4 monooxygenase adheres and works on NH4+ in place of CH4, inhibiting CH4 consumption andincreasing gas emissions [25]. Zheng et al., evaluated that approximately 3/4 of the annual freeings ofN2O from the plow land of China was caused by anthropogenic N-input [26]. As more fertilizer isused, higher amounts of N2O and CH4 are emitted [27,28]. Nevertheless, other studies have showna substantial decrease in CH4 emissions due to N fertilization. CH4 emissions from microcosmsdisplayed a strong inverse relationship with NH4+ availability. The application of urea fertilizerenhanced rice biomass, leading to greater soil O2 input from roots, combined with higher NH4+

availability which stimulated methane oxidation, leading to a reduction in emissions [29]. In addition,Banger et al., discovered that CH4 emissions were stimulated at a rate lower than 140 kg N ha−1,above which the fluxes were inhibited in rice-based cropping systems [30]. These discrepancies maybe related to the climate conditions and the physical and chemical properties of soil from differentregion [31–33].

Salinization is an enormous threat to environmental resources, and the area would account formore than 50% of the arable land by mid-century [34]. Fields in western Jilin were barely coveredwith vegetation due to the land salinization before 1960s, when large-scale reclamation and ricecultivation were carried out. Nowadays, the region is a major rice-producing area and has madegreat contributions to grain production and food security in the Jilin province. Fields are still beingreclaimed to paddies, especially after the project of irrigation from the Nen River was accomplished.Thus, newly and long-term tillage saline–alkaline paddies are chosen to estimate the impact of tillageon GHG emissions and global climate change during different reclamation years.

In the current study, we monitored the GHG fluxes from 1-year-old and 57-year-old saline–alkalinepaddies in 2012 and 2013 in Qianguo. The objectives of this study were to (i) identify the differenceof GHG fluxes between intermittent irrigation and continuous flooding irrigation in two tillage yearpaddies during rice-growing stages; (ii) ascertain the cumulative GHG emissions under different Nfertilization rates during five rice-growing periods in two tillage year paddies; (iii) estimate the GWPof 1-year-old and 57-year-old paddies under different tillage treatment, comprehensively. We expected


that a reasonable tillage management would be predicted for rice paddies and their reclamation whichwould benefit the minimization of GHG emissions.

2. Materials and Methods

2.1. Site Description

Field experiments were carried out during the rice-growing period of 2012 and 2013 in Qianguotown (123◦35′~125◦18′E, 44◦17′~45◦28′N) (Figure 1), in the west of Jilin province south of theSongnen Plain. The climate is a typical semi-arid. Monthly precipitation and air temperature duringexperimental period is shown in Figure 2 [35]. The freezing period is between late October andmid-April (approximately 165 days) each year. Single-season rice is planted in the study area on 26May and harvested on 2 October. The fertilizer N rate is between 60 and 250 kg N ha−1, the mean rateis 150 kg N ha−1, and the rice variety is Jijing88 (Super-rice I).

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tillage year paddies during rice-growing stages; (ii) ascertain the cumulative GHG emissions under different N fertilization rates during five rice-growing periods in two tillage year paddies; (iii) estimate the GWP of 1-year-old and 57-year-old paddies under different tillage treatment, comprehensively. We expected that a reasonable tillage management would be predicted for rice paddies and their reclamation which would benefit the minimization of GHG emissions.



Field experiments were carried out during the rice-growing period of 2012 and 2013 in Qianguo town (123°35′~125°18′E, 44°17′~45°28′N)（Figure 1）, in the west of Jilin province south of the Songnen Plain. The climate is a typical semi-arid. Monthly precipitation and air temperature during experimental period is shown in Figure 2 [35]. The freezing period is between late October and mid-April (approximately 165 days) each year. Single-season rice is planted in the study area on May 26 and harvested on October 2. The fertilizer N rate is between 60 and 250 kg N ha−1, the mean rate is 150 kg N ha−1, and the rice variety is Jijing88 (Super-rice I).

Figure 1. Location of Jilin province in China and Qianguo in Jilin province.

Figure 2. Monthly mean precipitation and air temperature during the rice-growing period from 2012 to 2013.

2.2. Experimental Design

The land (124°43′03″E, 45°00′19″N, 42.7 m × 20.4 m), barely covered with vegetation due to the soil salinization, has been reclaimed as a rice paddy since 1955, irrigated and fertilized every year.



tillage year paddies during rice-growing stages; (ii) ascertain the cumulative GHG emissions under different N fertilization rates during five rice-growing periods in two tillage year paddies; (iii) estimate the GWP of 1-year-old and 57-year-old paddies under different tillage treatment, comprehensively. We expected that a reasonable tillage management would be predicted for rice paddies and their reclamation which would benefit the minimization of GHG emissions.



Field experiments were carried out during the rice-growing period of 2012 and 2013 in Qianguo town (123°35′~125°18′E, 44°17′~45°28′N)（Figure 1）, in the west of Jilin province south of the Songnen Plain. The climate is a typical semi-arid. Monthly precipitation and air temperature during experimental period is shown in Figure 2 [35]. The freezing period is between late October and mid-April (approximately 165 days) each year. Single-season rice is planted in the study area on May 26 and harvested on October 2. The fertilizer N rate is between 60 and 250 kg N ha−1, the mean rate is 150 kg N ha−1, and the rice variety is Jijing88 (Super-rice I).


Figure 2. Monthly mean precipitation and air temperature during the rice-growing period from 2012 to 2013.


The land (124°43′03″E, 45°00′19″N, 42.7 m × 20.4 m), barely covered with vegetation due to the soil salinization, has been reclaimed as a rice paddy since 1955, irrigated and fertilized every year.

Figure 2. Monthly mean precipitation and air temperature during the rice-growing period from 2012to 2013.


The land (124◦43′03”E, 45◦00′19”N, 42.7 m × 20.4 m), barely covered with vegetation due to thesoil salinization, has been reclaimed as a rice paddy since 1955, irrigated and fertilized every year.


The bare land (124◦42′27”E, 45◦00′05”N, 43.6 m × 21.8 m) without artificial disturbance before riceplantation was reclaimed in 2012. Land plots were plowed in late April before irrigation and then riceseedlings were transplanted in mid-May by machinery.

Experiment I was operated in 2012 to test the impact of water management systems continuousflooding irrigation (CF) and intermittent flooding irrigation (IF) on GHG emission. An earthen row wasbuilt into a ridge in each paddy to divide the patty into two parts (20 m × 20 m) before plowing, whereCF and IF irrigations would be used. The water layer was always kept at 3 to 5 cm in CF treatmentbefore the mature stage and drained for harvest. Under the IF irrigation mode, the water depth was3–4 cm during the green stage, drained and rewetted, and maintained at 1 to 2 cm until the mature stage.To ensure that the nutrients were not limited, N fertilizers (150 kg N ha−1) were applied four times,accounting for 10%, 50%, 25% and 15% of the total amount, respectively. The fertilizer was appliedbefore transplant seedlings (basal fertilizer), added in the third day after transplanting (green-tillerfertilizer), and broadcasted in the beginning and the end of July (booting fertilizer), respectively. Therice variety is Jijing88 (Super-rice I). Crops were planted and managed according to local farmers.

Experiment II was carried out in 2013 to find the influence of N fertilizer management on GHG.Each field was separated into four parts (10 m × 20 m) by artificial ridges before plowing. Localfertilizer application rates were ranged from 60 to 250 kg N ha−1. Thus, four gradients were set:Control group (N0, no N fertilizer added), low N fertilizer (N60, 60 kg N ha−1), medium N fertilizer(N150, 150 kg N ha−1) and high N fertilizer (N250, 250 kg N ha−1). Plots were plowed and cropped(under IF) according to the methods mentioned above.

2.3. Emissions Measurements

Closed chamber technique was used to collect gas samples [36]. The base (50 cm × 50 cm ×30 cm) made of acrylic sheets (6 mm) were put in the fields ahead of rice transplanting and enclosedsix plants. Chambers of 50 cm (Length) × 50 cm (Width) × 50 cm (Height) were placed on the base.Grooves were designed on the top of base and middle chambers and replete with water to make thesystem gas-tight. Fans were fixed to homogenize the air inside [37]. Holes on the chamber were usedfor temperature testing and gas sampling. The middle chamber was put on the pedestal and underthe top box from the booting stage to maturity, when rice was growing faster and taller than 50 cm(Figure 3). Gas samples were collected every half-hour at 9:00~11:00 a.m. two times a week throughoutthe cropping season. Samples were drawn with an air-tight syringe and injected to pro-evacuate50 mL vacuum bags immediately. Gas was sent to the lab of Northeast Institution of Geography andAgro-ecology, Chinese Academy of Sciences. The contents of gases were subsequently tested with agas chromatograph (GC, Agilent 7820A, Santa Clara, CA, USA) [22].


The bare land (124°42′27″E, 45°00′05″N, 43.6 m × 21.8 m) without artificial disturbance before rice plantation was reclaimed in 2012. Land plots were plowed in late April before irrigation and then rice seedlings were transplanted in mid-May by machinery.

Experiment I was operated in 2012 to test the impact of water management systems continuous flooding irrigation (CF) and intermittent flooding irrigation (IF) on GHG emission. An earthen row was built into a ridge in each paddy to divide the patty into two parts (20 m × 20 m) before plowing, where CF and IF irrigations would be used. The water layer was always kept at 3 to 5 cm in CF treatment before the mature stage and drained for harvest. Under the IF irrigation mode, the water depth was 3-4 cm during the green stage, drained and rewetted, and maintained at 1 to 2 cm until the mature stage. To ensure that the nutrients were not limited, N fertilizers (150 kg N ha−1) were applied four times, accounting for 10%, 50%, 25% and 15% of the total amount, respectively. The fertilizer was applied before transplant seedlings (basal fertilizer), added in the third day after transplanting (green-tiller fertilizer), and broadcasted in the beginning and the end of July (booting fertilizer), respectively. The rice variety is Jijing88 (Super-rice I). Crops were planted and managed according to local farmers.

Experiment II was carried out in 2013 to find the influence of N fertilizer management on GHG. Each field was separated into four parts (10 m × 20 m) by artificial ridges before plowing. Local fertilizer application rates were ranged from 60 to 250 kg N ha−1. Thus, four gradients were set: Control group (N0, no N fertilizer added), low N fertilizer (N60, 60 kg N ha−1), medium N fertilizer (N150, 150 kg N ha−1) and high N fertilizer (N250, 250 kg N ha−1). Plots were plowed and cropped (under IF) according to the methods mentioned above.

2.3. Emissions Measurements

Closed chamber technique was used to collect gas samples [36]. The base (50 cm × 50 cm × 30 cm) made of acrylic sheets (6 mm) were put in the fields ahead of rice transplanting and enclosed six plants. Chambers of 50 cm (Length) × 50 cm (Width) × 50 cm (Height) were placed on the base. Grooves were designed on the top of base and middle chambers and replete with water to make the system gas-tight. Fans were fixed to homogenize the air inside [37]. Holes on the chamber were used for temperature testing and gas sampling. The middle chamber was put on the pedestal and under the top box from the booting stage to maturity, when rice was growing faster and taller than 50 cm (Figure 3). Gas samples were collected every half-hour at 9:00~11:00 a.m. two times a week throughout the cropping season. Samples were drawn with an air-tight syringe and injected to pro-evacuate 50 mL vacuum bags immediately. Gas was sent to the lab of Northeast Institution of Geography and Agro-ecology, Chinese Academy of Sciences. The contents of gases were subsequently tested with a gas chromatograph (GC, Agilent 7820A, Santa Clara, CA, USA) [22].

Figure 3. Structure of static chamber monitored greenhouse gas (GHG) fluxes in paddy fields. Figure 3. Structure of static chamber monitored greenhouse gas (GHG) fluxes in paddy fields.


2.4. Soil Properties Analysis

Fifteen samples from each paddy were collected in metal cylinders (100 cm3) before the fieldexperiment, and dried at 105 ◦C for 48 h to calculate water content and report soil bulk density ona dry basis. Twenty-five samples taken with soil auger (7 cm) from each field were mixed and airdried at room temperature, then passed sequentially through a sieve (2 or 1 mm) and stored forphysical—chemical analysis (Table 1). Soil organic carbon (SOC) was tested using a total organiccarbon (TOC) analyzer (Shimadzu TOC-V, Japan). Total nitrogen was determined using Kjeldahlmethod. Total phosphorus was measured according the method of Andetsen (1975) [38]. PH and ECwere measured using PHS-3C (08) pH meter and DDS-307 conductivity meter (Rex China) at a ratioof 5:1 (water to soil). CEC (cation exchange capacity) was tested using an EDTA-ammonium acetateexchange method, and a flame emission photometric method was used for exchangeable sodium. ESPis the percentage of exchangeable sodium to CEC. Experiments were performed in triplicate.

Table 1. Physical-chemical characteristics of study soil (0–20 cm).

TillageYear

BD(g cm−3) 1 pH

EC(ms cm−1)

SOC(g kg−1)

TN(g kg−1)

TP(g kg−1)

ESP(%)

1 1.32 ± 0.25 2 9.72 ± 0.43 1.27 ± 0.38 4.29 ± 1.03 0.78 ± 0.21 0.57 ± 0.14 17.11 ± 0.2257 1.26 ± 0.27 8.31 ± 0.29 0.31 ± 0.11 23.06 ± 2.15 2.24 ± 0.65 1.14 ± 0.22 6.35 ± 0.75

1 BD: Bulk density; EC: Electric conductivity; SOC: Soil organic carbon; TN: Total nitrogen; TP: Total phosphorus;ESP: Exchangeable sodium percentage; 2 Mean Value ± Standard Error.

2.5. Calculation of CH4, N2O and CO2 Emission

Fluxes were computed from the following formula [39,40].

F = ρ × (V/A) × (∆c/∆t) × (273/T) (1)

Fcal = c× F (2)

where F is the flux of CH4, N2O or CO2 (mg m−2 h−1), ρ is the density of gas (mg cm−3), V andA are the volume (m3) and surface area (m2), ∆c/∆t is the rate of gas increase inside of chamber(mg m−2 h−1), and T is the absolute temperature in-house. (Fcal) is the calibration of the averageemission of CH4, N2O or CO2, F is the mean flux of a certain gas (mg m−2 h−1), and C is the calibrationcoefficient (1.24) [41].

Seasonal GHG emission was computed as follows:

FC = Fcal × 24× Di/1000 (3)

where FC is the accumulative fluxes in every rice-growing season (g m−2) and Di is the days of theith period.

Global warming potential of main GHG was calculated using the following equation [6]:

Fc = 25FCH4 + 298FN2O + FCO2 (4)

where Fc is the accumulative flux (g CO2-eqv m−2), FCH4 is the cumulative flux of CH4 (g m−2), FN2O

is the cumulative flux of N2O (g m−2), FCO2 is the cumulative flux of CO2 (g m−2).

2.6. Statistical Analysis

SPSS 19.0 software (SPSS Inc., Chicago, IL, USA) was used for statistical analyses. One-way andtwo-way analyses of variance (ANOVA) were performed to analyze the differences of average andcumulative CH4, N2O and CO2 flows in different irrigation regimes and N fertilization managements


(LSD; p < 0.05). Microsoft Excel 2003 software was used to cypher the standard deviation of means.SigmaPlot 12.5 (Systat Software, Inc., San Jose, CA, USA) was applied for plots.

3. Results

3.1. GHG Emissions under IF and CF Regime

CH4 showed single-peak emission during the rice growing period. The peak values underintermittent irrigation were lower but earlier (4 days) than in the continuous flooding condition,with crest values of 1.98 mg m−2 h−1 and 24.02 mg m−2 h−1 from 1-year-old and 57-year-oldpaddies, respectively (Figure 4A,B). The largest average flux appeared in the booting stage, i.e.,1.70 ± 0.16 mg m−2 h−1 (1-year-old, CF) and 1.25 ± 0.25 mg m−2 h−1 (1-year-old, IF), but the lowestmean value was observed in the green period. Comparatively, CH4 from long-term tillage paddy hadhigher emission flux, with cumulative emissions of approximately 9.21- (CF) and 8.36- (IF) fold higherthan that of new fields. CH4 was sensitive to irrigation regimes during booting, heading and maturestages, which was susceptible to tillage year (Table 2).

In the time of the rice-growing season, N2O flux from CF was low, with a mean rate of0.08 mg m−2 h−1 (1-year-old) and 0.07 mg m−2 h−1 (57-year-old). Three peaks appeared in the green,booting and heading stages and then dropped speedily to low levels (0.02~0.09 mg m−2 h−1). N2Oflux from IF showed similar emission trends, although the peak appeared in the tillering stage, earlierthan booting, and the maximum rate in heading was much higher (0.22 mg m−2h−1, 1-year-old; and0.19 mg m−2 h−1, 57-year-old) (Figure 4C,D). No significant differences of N2O fluxes between the twotreatments (IF and CF) were observed except for the mature stage, and the total cumulative emissionswere 0.23 mg m−2 (1-year-old, CF), 0.29 mg m−2 (1-year-old, IF) and 0.20 mg m−2 (57-year-old, CF),0.24 mg m−2 (57-year-old, IF) (Table 2).

CO2 emissions in CF condition were lower than that from IF fields. During the green stage, theemission flux was lowest, with an average value of 169.03 to 435.65 mg m−2 h−1. The maximum wasobserved in tillering stage for the 57-year-old field, 818.75 mg m−2 h−1 (CF) and 1053.95 mg m−2 h−1

(IF), and maturity for the 1-year-old paddy, 852.78 mg m−2 h−1 (CF) and 893.70 mg m−2 h−1 (IF)(Figure 4E,F). There were significant differences in soil carbon dioxide during growing periods betweenwater regimes, except for green and mature period, while cumulative emissions from the 57-year-oldpaddies were significantly higher than from the 1-year-old paddy (Table 2).

Table 2. Cumulative emission of GHG from continuous flooding irrigation (CF) and intermittentflooding irrigation (IF) of two tillage paddies during rice-growing seasons (n = 3).

GrowingPeriod

1-Year 57-Year Analysis of Variance

CF IF CF IF TillageYear (Y)IrrigationRegime (I) Y × I

CH4(gm−2)

Green 0.13 ± 0.01 2 0.13 ± 0.01 0.22 ± 0.03 0.22 ± 0.06 ** 1 NS NSTillering 0.61 ± 0.12 0.71 ± 0.13 4.37 ± 0.86 4.92 ± 1.43 ** NS NSBooting 1.79 ± 0.01 1.49 ± 0.07 16.11 ± 0.52 14.21 ± 0.64 ** * *Heading 0.65 ± 0.13 0.45 ± 0.03 9.39 ± 0.34 5.36 ± 0.53 ** ** **Mature 0.33 ± 0.04 0.23 ± 0.02 1.83 ± 0.88 0.51 ± 0.04 ** ** **

Total 3.51 ± 0.05 3.01 ± 0.11 32.34 ± 0.59 25.18 ± 2.46 ** ** **

N2O(gm−2)

Green 0.03 ± 0.01 0.03 ± 0.01 0.03 ± 0.01 0.03 ± 0.01 NS NS NSTillering 0.06 ± 0.01 0.07 ± 0.02 0.05 ± 0.01 0.07 ± 0.01 NS NS NSBooting 0.07 ± 0.02 0.05 ± 0.01 0.07 ± 0.01 0.05 ± 0.01 NS NS NSHeading 0.05 ± 0.02 0.07 ± 0.02 0.04 ± 0.01 0.07 ± 0.01 NS NS NSMature 0.02 ± 0.01 0.04 ± 0.01 0.02 ± 0.01 0.03 ± 0.01 NS ** NS

Total 0.23 ± 0.02 0.29 ± 0.06 0.20 ± 0.01 0.24 ± 0.01 NS NS NS

CO2(gm−2)

Green 40.57 ± 5.33 46.52 ± 12.29 87.21 ± 13.15 104.56 ± 19.13 ** NS NSTillering 462.95 ± 28.44 620.59 ± 26.18 589.50 ± 16.64 758.85 ± 50.11 ** ** NSBooting 401.56 ± 9.69 542.02 ± 21.13 451.77 ± 31.36 677.22 ± 41.13 ** ** NSHeading 352.58 ± 2.52 472.28 ± 49.10 389.41 ± 36.65 532.34 ± 41.04 NS ** NSMature 489.12 ± 51.77 552.68 ± 72.04 465.76 ± 13.41 576.59 ± 81.05 NS NS NS

Total 1746.77 ± 111.23 2224.09 ± 215.90 2120.15 ± 285.09 2649.55 ± 112.36 ** ** NS1 * indicates p < 0.05; ** indicates p < 0.01, NS indicates not significant; 2 Mean Value ± Standard Error.

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Figure 4. Seasonal variations in GHG (CH4, N2O and CO2) fluxes from two paddies, i.e., 1st tillage (1-year-old) and 57th tillage (57-year-old), with different irrigation treatments: Continuous flooding irrigation and intermittent irrigation. Error bars denote standard deviation. The vertical arrows indicate N fertilizer application except for the base fertilization before transplant of seedlings.

3.2. GHG Emissions under Fertilizer N Addition

Total cumulative CH4 fluxes ranged from 19.32–36.88 g m−2 and were positive correlated with N addition rates; the maximum was observed in the N250 treatment of 57-year-old paddy. Emissions in the booting stage were the highest, accounting for 41.25–52.67%, and in the green stage, the lowest, the emissions accounted for 0.48–1.27%. The cumulative fluxes were also positively correlated to N fertilization at different stages, but exceptions appeared in booting when the cumulative emissions in the N60 and N150 treatments were lower than the control (N0). More emissions were detected from long-term tillage paddy, approximately 1.56- to 1.75-fold higher than newly developed field in booting period (Figure 5A,B).

N2O fluxes were promoted by the application of nitrogen fertilizers, increasing with seasonal cumulative emissions of 90.34 mg m−2–174.42 mg m−2. Cumulative N2O fluxes reached a peak in the booting stage in all fields and were significantly higher in N250 treatment than N0 from long-term tillage fields during growing periods (Figure 5C,D). N2O emissions were lower in 1-year-old paddy soil than in the long-term tillage fields.

Figure 4. Seasonal variations in GHG (CH4, N2O and CO2) fluxes from two paddies, i.e., 1st tillage(1-year-old) and 57th tillage (57-year-old), with different irrigation treatments: Continuous floodingirrigation and intermittent irrigation. Error bars denote standard deviation. The vertical arrows indicateN fertilizer application except for the base fertilization before transplant of seedlings.

3.2. GHG Emissions under Fertilizer N Addition

Total cumulative CH4 fluxes ranged from 19.32–36.88 g m−2 and were positive correlated with Naddition rates; the maximum was observed in the N250 treatment of 57-year-old paddy. Emissions inthe booting stage were the highest, accounting for 41.25–52.67%, and in the green stage, the lowest,the emissions accounted for 0.48–1.27%. The cumulative fluxes were also positively correlated to Nfertilization at different stages, but exceptions appeared in booting when the cumulative emissions inthe N60 and N150 treatments were lower than the control (N0). More emissions were detected fromlong-term tillage paddy, approximately 1.56- to 1.75-fold higher than newly developed field in bootingperiod (Figure 5A,B).



N fertilizer stimulated CO2 emissions, and the responses of seasonal cumulative CO2 emissions ranged from 1584.72 to 3575.02 g m−2 (Figure 5E,F). The contributions of CO2 emissions in the green stage and in the heading stage were less than others, accounting for 2.05–5.55% and 9.80–14.83% of total, respectively. The cumulative emissions from 57-year-old soils were always more than of 1-year-old fields, at a maximum of 1.5-fold higher in the booting period.

Figure 5. Cumulative GHG (CH4, N2O and CO2) emissions from two paddies affected by different N fertilizer treatments over five growing stages. Capital letters over the bars showed significant differences among different N fertilizer rates (kg N ha−1), whereas lowercase letters indicate differences between 1-year-old and 57-year-old paddies.

3.3. Area-Scaled Global Warming Potential

GWPs of CH4 and N2O from CF were much taller than that from IF: 1112 ± 18 g CO2-eq m−2 for 57-year paddy throughout rice growth (Table 3). In contrast, the total GWPs of IF were higher than that of CF when CO2 was considered, at 2813 ± 23 g CO2-eq m−2 (1-year-old) and 4271 ± 241 g CO2-eq m−2 (57-year-old). GWPs were larger in the long-term paddy than the new paddy.

The GWPs of paddy soils increased with N application rate in all treatments (N0, N60, N150, N250). Moreover, the greatest values were reported among 57-year-old paddies. Annual GWP of CH4 and N2O was highest in N250 treatments from long-term tillage fields (974 ± 132 g CO2-eq m−2), but the value was more than four-fold higher than the former if CO2 was taken into account.

Figure 5. Cumulative GHG (CH4, N2O and CO2) emissions from two paddies affected by differentN fertilizer treatments over five growing stages. Capital letters over the bars showed significantdifferences among different N fertilizer rates (kg N ha−1), whereas lowercase letters indicate differencesbetween 1-year-old and 57-year-old paddies.

N2O fluxes were promoted by the application of nitrogen fertilizers, increasing with seasonalcumulative emissions of 90.34 mg m−2–174.42 mg m−2. Cumulative N2O fluxes reached a peak in thebooting stage in all fields and were significantly higher in N250 treatment than N0 from long-termtillage fields during growing periods (Figure 5C,D). N2O emissions were lower in 1-year-old paddysoil than in the long-term tillage fields.

N fertilizer stimulated CO2 emissions, and the responses of seasonal cumulative CO2 emissionsranged from 1584.72 to 3575.02 g m−2 (Figure 5E,F). The contributions of CO2 emissions in the greenstage and in the heading stage were less than others, accounting for 2.05–5.55% and 9.80–14.83%of total, respectively. The cumulative emissions from 57-year-old soils were always more than of1-year-old fields, at a maximum of 1.5-fold higher in the booting period.

3.3. Area-Scaled Global Warming Potential

GWPs of CH4 and N2O from CF were much taller than that from IF: 1112 ± 18 g CO2-eq m−2 for57-year paddy throughout rice growth (Table 3). In contrast, the total GWPs of IF were higher than thatof CF when CO2 was considered, at 2813± 23 g CO2-eq m−2 (1-year-old) and 4271± 241 g CO2-eq m−2(57-year-old). GWPs were larger in the long-term paddy than the new paddy.

The GWPs of paddy soils increased with N application rate in all treatments (N0, N60, N150,N250). Moreover, the greatest values were reported among 57-year-old paddies. Annual GWP of CH4and N2O was highest in N250 treatments from long-term tillage fields (974 ± 132 g CO2-eq m−2), butthe value was more than four-fold higher than the former if CO2 was taken into account.


Table 3. Area-scaled GWP (global warming potential, g CO2-eqm−2) under different water regimes,continuous flooding (CF) and intermittent irrigation (IF), and N fertilization application rates overentire rice-growing season.

TreatmentArea-Scaled GWP

(CH4 + N2O, g CO2-eq m−2)Area-Scaled GWP

(CH4 + N2O + CO2, g CO2-eq m−2)

1-year-old 57-year-old 1-year-old 57-year-old

WaterRegime

CF 678 ± 26 1 1112 ± 18 2516 ± 26 3630 ± 138IF 546 ± 23.56 916 ± 80 2813 ± 23 4271 ± 241

Nitrogenapplication

N0 515 ± 74a 737 ± 41a 2130 ± 62b 3003 ± 125cN60 515 ± 88a 907 ± 76a 2420 ± 192b 3789 ± 256bN150 551 ± 58a 923 ± 99a 2669 ± 271ab 4332 ± 220abN250 637 ± 43a 974 ± 132a 3252 ± 353a 4549 ± 296a

1 Mean Value ± Standard Error. Different lowercase letters indicate significantly different at significance level ofp < 0.05 among four N fertilization application rates.

4. Discussion

4.1. Seasonal Emissions of CH4, N2O and CO2

CH4 emissions fluctuated with rice-growth. The flux was high from middle tillering to the end ofthe heading stage, observing a peak value in the booting stage in which the cumulative CH4 emissionsaccounted for approximate half of the flux. The lowest cumulative gas flux was in the green and maturestages, with just 6% of the total proportion. CH4 production can be influenced by many factors, likerainfall, temperature and crop growth [33,42]. In July and August, the temperature is high, rice plantsgrow fast and roots develop rapidly, producing more H2 with the help of fermentative bacteria andproducing acetic acid bacteria. More root exudates accelerate the decomposition of SOC and provideadequate substrate for microbes. The relatively high soil temperature increases the methanogenicactivity, and the flooding layer creates a strict anaerobic condition for soil, promoting the productionof CH4 [5]. However, during the mature stage the field drained and soil permeability was better,increasing methanotroph activities and inhibiting methanogens, and thus less CH4 emission fluxwas observed.

Throughout the entire rice-growing season, N2O emission flux showed minor fluctuations exceptfor three drastic changes. In the green stage, the cumulative N2O emissions were lowest, but they werehighest in the booting period. N2O gas produced from nitrification and denitrification, susceptibleto temperature, soil moisture and fertilizer [43]. Rapid growth was primarily stimulated by theapplication of urea, increasing the concentration of the reaction substrate and promoting the formationand emission of gas.

The emission curves of CO2 changed with rice growing, increasing gradually from transplantingand reaching a maximum in tillering, decreasing slightly in booting, and recovering to a high level inthe late heading period. The highest emissions were detected in tillering and late-heading stages, andthe highest cumulative emissions of CO2 were detected in tillering, booting and maturity periods. CO2in paddy fields mainly comes from plant and soil respiration [8]. In the green period, plant respirationis weak due to the limitation of biological factors, such as plant height and leaf area. In the tilleringstage, the air temperature gradually increased, plants grew quickly, soil microbial activities wereenhanced and root exudates production increased, providing suitable conditions for soil respiration.The rate of respiration could be the reason for decrease in booting, when the photosynthetic rate is low.During the mature period, litter provides favorable conditions for the transformation of soil organicmatter, promoting soil respiration and gas emissions [44].


4.2. Effects of Irrigation Regimes on GHG Emissions

Soil moisture is one of the great significance indicators of soil properties during rice-growingseasons and has impacts on greenhouse gas emissions by changing soil permeability, microbial activityand Eh (soil redox potential) [45]. Water content did not change significantly in continuous floodingconditions; the water layer had a constant height of 3–5 cm. This level changed drastically in certainperiods during the entire season in IF treatments.

CH4 emissions, showing a single peak pattern in all fields, were sensitive to irrigation regimes,and the annual cumulative CH4 fluxes in IF were approximately 23% lower than that of CF (Table 2).These results are consistent with records showing that intermittent irrigation management can reduceCH4 emissions [46,47]. Diffusion rates of O2 and CH4 and activities of methane-oxidizing bacteria areimpressed by soil water content [47]. Intermittent irrigation provides better habitat for the growthof methanotroph (obligate aerobic bacteria), beneficial to bacterial reproduction [48], increasing CH4oxidation capability relative to CF (Figure 4). The impact of water regime on CH4 emissions differswith rice-growing stages, and gas fluxes were more sensitive in booting, heading and mature stages,when soil water content changed considerably in the intermittent irrigation mode (Table 2).

N2O emissions under two water regimes were the same as in previous studies, except for therapidly increased peaks [36,46]. The lowest peak value was noted in the heading stages under CFconditions, with no significance differences between CF and IF treatments (Table 2). Over rice-growingperiods, three peaks came out instantly following nitrogen application, compliance with the fact thatpulses of N2O emission are commonly induced by N fertilization addition [24]. With the application ofbooting fertilizer, the peaks in intermittent irrigation appeared much earlier than in CF conditions,mainly due to the gradual drainage of paddy fields at the late tillering period, promoting the synergisticeffects of nitrification and denitrification. N fertilizer addition increased the concentration of substrate,thereby promoting the formation and discharge of gas. During heading stages denitrification (N2 toN2O) was impeded because of the relatively high floodwater depth (3–5 cm) under CF conditions,with high water content and strictly anaerobic conditions, lowering the release of N2O [49]. However,no significant differences between two water regimes were noticed over the entire rice-growing period(Table 2).

CO2 emissions were more likely influenced by water management, especially in the tillering,booting and heading stages (Table 2). CO2 emissions from flooding treatment are always lower than inintermittent irrigation treatment. During rice-growth stages, the paddy field is drained on occasion,supplying rice roots with sufficient oxygen and strengthening root respiration which can possiblypromote the activity of aerobic microorganisms in the soil, decomposing soil organic matter [49]. CO2from soil and plant root respiration can be more easily released into the atmosphere due to good soilpermeability under IF treatments. In contrast, soil water content in long-term submerged paddy soilis higher, and the relatively anaerobic environment suppresses the aerobic activity of aerobic soil,decreasing soil respiration intensity and the production of CO2 gas. The flooded layer promotes thedissolution of CO2 hinders its diffusion into the atmosphere.

4.3. Impacts of N Fertilization Rate on Regulating GHG Emissions

Application of N fertilizer can promote crop growth and increase food production while affectingCH4 emissions. Three processes are involved in CH4 emissions from paddy soil, which can beinfluenced by nitrogen fertilizer addition, increase or decrease production, and consumption, andrelease gas at various ecosystems [42]. Application of N fertilizer could increase crop size and providerich organic matter for methanogens, utilizing roots and root exudates as a carbon source [50]. Inaddition, researchers reported that the use of N fertilizer in paddy fields promoted the growth andactivity of methanogens, promoting CH4 emissions [25,51,52]. In the present study, the total cumulativeCH4 fluxes were encouraged by fertilizer additions; in contrast CH4 emissions were inhibited in N60and N150 treatments during the booting stage, in contrast to some reports showing that lower N rates


tend to increase CH4 emissions but higher N rates could potentially inhibit CH4 emissions [25]. Thereason for the difference may be severe soil salinization, lower SOM content and high pH value [53].

Due to nitrification and denitrification processes, the emission of N2O from cropland was causedpredominantly by nitrogenous fertilizers put on fields [54]. In the current research, the reactionsubstrate concentration was increased through urea application, promoting the emission of N2O [55,56].As more N fertilizer was used, more cumulative N2O emissions were detected at each rice-growingstage. The positive effect is consistent with other reports [4,57,58].

It is reported by Burton et al., that CO2 was inhibited by N fertilizer application as the decreasedactivities of extracellular enzyme and depletion in fungal populations [59–61]. In contrast, the increasedemissions of CO2 attributed to N fertilizer were caught by Iqbal et al. [62]. However, in the currentstudy, the cumulative CO2 emissions had a positive correlation with N fertilizer rate; as more urea wasadded, more CO2 gas emitted. Nitrogen fertilizer increased the activity of roots, improved soil nutrientcontent, enhanced the biological activity in paddy soil, and promoted the mineralization of organicmatter which increased soil respiration [63]. In addition, the carbon source and available nitrogenincreased. The appropriate C/N ratio not only ensures soil microbial activities but also promotesthe vigorous growth of rice plants, thereby enhancing the respiration of soil and plant populations,promoting CO2 emissions from paddy fields.

4.4. Relationships between GHG Emissions and Tillage Year

GHG emissions from two paddy fields showed similar trends, and the gas emissions from57-year-old paddies were much higher; GWPs are always higher (1.4–1.8 times) than for the 1-year-oldpaddy field (Figure 4A,B, Tables 2 and 3). In the current study, CH4 and CO2 emissions weresignificantly influenced by tillage year, and N2O by N fertilizer (Table 2, Figure 4).

Previous studies have reported that GHG can be easily affected by soil chemical-physicalproperties such as pH value, soil organic matter and salinity [14,38]. Microbial growth and activities arestrongly influenced by pH. The optimum pH-value for methanogens is more than four and less thanseven [64]. The pH was as high as 9.72 in the 1-year-old paddy, reducing methanogenic archaea andmethanotroph bacteria, thus lowering CH4 and CO2 production. However, no significant differences intotal N2O emissions from the paddy fields were caught, mainly being ascribable to the weak influencesof pH on the nitrification and dentrification process [65].

It has reported that CH4 and CO2 were influenced by soil organic matters [66]. SOC also couldbe the reason why there were more greenhouse gas emissions in longtime tillage paddies [8]. The57-year-old paddy had a long tillage history, planted rice for many years and accumulated moreorganic matter [18]. The soil was fertile and SOC content was five-fold higher than in the new tillagefield, providing a superior growth environment for rice plants, root and soil microorganisms and moreavailable organic carbon substrate for microorganism by root exudation and microbial decomposition(Table 1). Rice plants were tall and sturdy, and photosynthesis and respiration processes were stronger,transforming more oxide into soil for N2O and CO2 production [67]. Moreover, more gases escaped viarice tissue from paddies to atmosphere with the help of well-developed aerenchyma in roots, rhizomesand stems [62]. In addition, plant respiration may increase GHG emissions from 57-year-old paddies,where above-ground biomass was much higher.

5. Conclusions

We measured CH4, N2O and CO2 fluxes in saline—alkaline paddy fields with typical Chineseirrigation regimes, continuous flooding irrigation and intermittent flooding irrigation, and nitrogenfertilizer managements (N0, N60, N150 and N250). Relative to continuous flooding, intermittentirrigation reduced CH4 but promoted CO2, and had little effect on N2O emissions from rice paddysoils. The N fertilizer showed a positive effect on greenhouse gases compared to no N addition. Thecumulative emissions of CH4, N2O and CO2 all increased with the supply of urea, with a maximum atthe rate of 250 kg N ha−1. The fluxes in the 57-year-old paddy were higher than in the 1-year-old soil,


with higher pH and lower SOC. Intermittent irrigation versus continuous flooding irrigation wouldmitigate the GWP of CH4 and N2O, and N fertilizer contributes to the GWP of net CH4, N2O andCO2 fluxes.

Acknowledgments: This study was supported by the National Natural Science Foundation of China (No.51179073, 41471152) and Specialized Research Fund for Doctoral Program of Higher Education (20130061110065).

Author Contributions: J.T., J.W. and Z.L. drafted the manuscript and designed the experiments; J.W., S.W. andY.Q. collected and tested the samples.

Conflicts of Interest: The authors declare no conflict of interest.

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Introduction Materials and Methods Site Description Experimental Design Emissions Measurements Soil Properties Analysis Calculation of CH4, N2O and CO2 Emission Statistical Analysis

Results GHG Emissions under IF and CF Regime GHG Emissions under Fertilizer N Addition Area-Scaled Global Warming Potential

Discussion Seasonal Emissions of CH4, N2O and CO2 Effects of Irrigation Regimes on GHG Emissions Impacts of N Fertilization Rate on Regulating GHG Emissions Relationships between GHG Emissions and Tillage Year

Conclusions References

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