Treated domestic sewage irrigation significantly decreased the CH4, N2O and NH3 emissions from paddy fields with straw incorporation

Atmospheric Environment 169 (2017) 1e10

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Treated domestic sewage irrigation significantly decreased the CH4, N2O and NH3 emissions from paddy fields with straw incorporation Shanshan Xu a, b, 1, Pengfu Hou b, 1, Lihong Xue b, *, Shaohua Wang a, Linzhang Yang b a b

Key Laboratory of Crop Physiology and Ecology in Southern China, Ministry of Agriculture, Nanjing Agricultural University, Nanjing 210095, China Institute of Agricultural Resources and Environment, Jiangsu Academy of Agricultural Sciences, Nanjing 210014, China

h i g h l i g h t s
2-yrs paddy experiment with straw returning & domestic sewage irrigation was set.
Domestic sewage irrigation reduced 45% chemical nitrogen input without yield loss.
Domestic sewage irrigation significantly decreased N2O and NH3 emissions.
Straw returning significantly increased GHG and NH3 emission of paddy fields.
Domestic sewage irrigation decreased GWPs of paddy with straw returning by 24%.

a r t i c l e i n f o

a b s t r a c t

Article history: Received 28 February 2017 Received in revised form 11 August 2017 Accepted 3 September 2017 Available online 9 September 2017

Straw incorporation and domestic sewage irrigation have been recommended as an environmentally friendly agricultural practice and are widely used not only in China but also in other countries. The individual effects on yield and environmental impacts have been studied extensively, but the comprehensive effect when straw returning and domestic sewage irrigation are combined together has seldom been reported. This study was conducted to examine the effects of straw returning and domestic sewage irrigation on rice yields, greenhouse gas emissions (GHGs) and ammonia (NH3) volatilization from paddy fields from 2015 to 2016. The results showed that the rice yield was not affected by the irrigation water sources and straw returning under the same total N input, which was similar in both years. Due to the rich N in the domestic sewage, domestic sewage irrigation could reduce approximately 45.2% of chemical nitrogen fertilizer input without yield loss. Compared to straw removal treatments, straw returning significantly increased the CH4 emissions by approximately 7e9-fold under domestic sewage irrigation and 13e14-fold under tap water irrigation. Straw returning also increased the N2O emissions under the two irrigation water types. In addition, the seasonal NH3 volatilization loss was significantly increased by 88.8% and 61.2% under straw returning compared to straw removal in 2015 and 2016, respectively. However, domestic sewage irrigation could decrease CH4 emissions by 24.5e26.6%, N2O emissions by 37.0e39.0% and seasonal NH3 volatilization loss by 27.2e28.3% under straw returning compared to tap water irrigation treatments. Global warming potentials (GWP) and greenhouse gas intensities (GHGI) were significantly increased with straw returning compared with those of straw removal, while they were decreased by domestic sewage irrigation under straw returning compared to tap water irrigation. Significant interactions between straw returning and domestic sewage irrigation on NH3 volatilization loss, CH4 and N2O emissions were observed. The results indicate that domestic sewage irrigation combined with straw returning could be an environmentally friendly and resource-saving agricultural management measure for paddy fields with which to reduce the chemical N input, GHG emissions, and NH3 volatilization loss while maintaining high rice productivity. © 2017 Elsevier Ltd. All rights reserved.

Keywords: Paddy fields Straw returning Domestic sewage irrigation Yield Greenhouse gas Ammonia volatilization

* Corresponding author. Jiangsu Academy of Agricultural Sciences, JAAS, 50#Zhongling Street, Nanjing 210014, China. E-mail address: [email protected] (L. Xue). 1 These authors contributed equally to this study. http://dx.doi.org/10.1016/j.atmosenv.2017.09.009 1352-2310/© 2017 Elsevier Ltd. All rights reserved.

1. Introduction Feeding the continually increasing global population while avoiding dangerous climate change and water pollution are the

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S. Xu et al. / Atmospheric Environment 169 (2017) 1e10

greatest challenges humanity is currently facing (Smith et al., 2013). In order to address global warming, greenhouse gases (GHGs) must be reduced. Methane (CH4) and N2O are important long-lived GHGs, and the global warming potentials (GWP) of CH4 and N2O over a time span of 100 years are approximately 28 and 265 times greater, respectively, than that of carbon dioxide (CO2) (IPCC, 2013). Agriculture as a source of GHG emissions contributed 22% (20-year) and 14% (100-year) of total metric-weighted global GHG emissions in 2010 according to the IPCC (2014). Rice paddies are important anthropogenic sources of GHG emissions (Cai et al., 1997). China, the largest rice-producing country in the world, accounted for approximately 26% of the global rice production. It was estimated that approximately 7.4 Tg methane (CH4) and 32 Gg N2O-N nitrous oxide (N2O) were emitted annually from rice cultivation in China, contributing up to 22% of the total GHG emissions from cropland in the country (Yan et al., 2005; Xing et al., 2009). The emissions of CH4 and N2O from rice paddies are strongly affected by agronomic practices, such as straw management, N fertilization and water regime (Zou et al., 2005; Shang et al., 2011; Yan et al., 2005; Xia et al., 2016). Ammonia (NH3) is another important gas emitted by agriculture, and the global NH3 emission from agricultural activities was 33.7 Tg N year1 in 1990 (Van Aardenne et al., 2001). NH3 is not only a secondary source of atmospheric N2O and NO (Mosier et al., 1991) but can also cause the acidification of terrestrial ecosystems and the eutrophication of water bodies after it is returned to the ground through dry and wet deposition. Nitrogen fertilizer application is one of the main sources of atmospheric NH3, and the global N loss from fertilization through ammonia volatilization reaches 11 million T year1, which accounts for 14% of the annual nitrogen application rate (FAO/IFA, 2001). Approximately 15e40% of N application in rice paddies is lost through ammonia volatilization, contributing approximately 20e70% of the total N loss from the paddy fields (Chien et al., 2009; Xue et al., 2014). Straw incorporation to soil has been widely used to maintain soil fertility and crop productivity not only in China but also in other countries (Bogner et al., 2008; Wang et al., 2015; Timsina, 2005; Bhattacharyya et al., 2012; Xia et al., 2016). Especially in the Tailake region in China, rice and wheat straw are directly incorporated into the soils when the grains are gathered, due to a high degree of mechanization in the region and also because of the straw burning ban. However, the direct incorporation of straw triggers substantial CH4 emissions, by providing methanogens with abundant carbon sources under flooded soils (Xia et al., 2016). The application of straw at 6 t ha1 before rice transplanting can increase CH4 by 2.1 times (Yan et al., 2005). The straw incorporation into paddy fields can also promote the NH3 volatilization due to the increasing NHþ 4 -N concentration and pH in the floodwater (Wang et al., 2012, 2013; Xu et al., 2016). Therefore, it is still a major challenge to mitigate the GHG and ammonia emissions from paddy fields with straw incorporation. Water eutrophication is another world-wide environmental problem mainly induced by the enrichment of nutrients such as nitrogen in aquatic ecosystems. Domestic sewage discharge is one of the main pollution sources of surface water and contributed 35e40% of nitrogen load into Tailake in China (Xie et al., 2007). Domestic sewage effluents are rich in organic matter and also contain appreciable amounts of macronutrients and micronutrients, and thus, sewage irrigation can substitute for partial chemical fertilizer, increase the soil nutrient levels and improve productivity (Yadav et al., 2002; Carr et al., 2004; Minhas et al., 2015; Xu et al., 2016; Ma et al., 2016). Therefore, sewage irrigation was taken as an effective measure in recent years for recycling the nutrients and water and avoiding the potential pollution caused by direct sewage discharge not only in China but also in other countries (Grant et al., 2012; Minhas et al., 2015; Sun et al., 2013;

Ma et al., 2016). However, increased CH4 and N2O emissions accompanying the increased grain yields were observed by domestic sewage irrigation in paddy fields with the same fertilizer N input (Zou et al., 2009). Furthermore, sewage irrigation boosted the NH3 emission flux of paddy fields without straw returning and mitigated the NH3 emission flux when the straw was incorporated into the paddy fields due to the change in ammonium content and pH of the flood surface water (Sun et al., 2013; Xu et al., 2016). Since both the rice yields and the GHGs and ammonia emissions are strongly affected by agronomic practices, such as straw management, N fertilization and water regime (Zou et al., 2005; Shang et al., 2011; Yan et al., 2005; Sun et al., 2013; Xu et al., 2016), it is necessary to evaluate the comprehensive effect of these measures. To our knowledge, however, no studies have examined the effects of sewage irrigation combined with straw incorporation on CH4, N2O and NH3 emissions from rice paddies. It is well documented that CH4, N2O and NH3 emissions from rice paddies are closely associated with soil carbon and nitrogen availabilities and transformation processes, which are greatly dependent on soil properties and soil microbial communities (Cai et al., 1997; Yan et al., 2005). Therefore, we hypothesized that relative to clean water irrigation, sewage irrigation would significantly decrease CH4, N2O and NH3 emissions from rice paddies with straw returning without having to sacrifice yields. To test this hypothesis, we performed a two-factor experiment including straw returning and domestic sewage irrigation on an undisturbed soil column. The objectives of this study are to quantify CH4, N2O and NH3 emissions and yields as influenced by wheat straw returning and sewage irrigation and to thereby testify whether the sewage irrigation can mitigate the adverse effects of straw returning on GHG emissions and NH3 volatilization. 2. Materials and methods 2.1. Experimental sites The soil column experiment was performed at the experimental farm of the Jiangsu Academy of Agricultural Sciences, Nanjing, Jiangsu Province (32120 N, 119 270 E), China, in 2015 and 2016. The region has a subtropical monsoon type climate (mean annual precipitation, 1243 mm), with the majority of rainfall occurring during the rice growing season. The soil of the experimental fields was classified as Gleysols, and the main physicochemical properties were as follows: pH 5.60, organic matter 17.15 g kg1, total nitrogen 1.62 g kg1, total phosphorus 0.40 g kg1, available nitrogen 156.42 mg kg1, available phosphorus 13.6 mg kg1, and available potassium 136 mg kg1. 2.2. Experimental design A two-factor design consisting of water irrigation and straw returning treatments in rice paddies was carried out using soil columns with a height of 100 cm and diameter of 30 cm. Five treatments including SWN (straw incorporation þ sewage irrigation þ urea), STN (straw incorporation þ tap water irrigation þ urea), WN (sewage irrigation þ urea), TN (tap water irrigation þ urea) and CK (tap water irrigation without urea and straw) were set up. Each treatment was replicated three times. Wheat straws were chopped to approximately 3e5 cm in length and incorporated into the soil for the SWN and STN treatments. The amount of wheat straw returning was 5.9 t hm2, which was equal to all of the preceding wheat straw. Domestic sewage effluents were collected from the septic tank in the Jiangsu Academy of Agricultural Sciences and were diluted to meet the national farmland irrigation water quality in China. Total N, pH, and other

S. Xu et al. / Atmospheric Environment 169 (2017) 1e10

indicators of the sewage after dilution were determined prior to each irrigation. The properties of the experimental sewage and tap water, including the heavy metals and Escherichia coli, are shown in Table 1. Except for the CK, the total N input for all of the treatments was the same (240 kg hm2), including the N input from sewage irrigation. Urea was used as the chemical N fertilizer, and the detailed N application for each treatment is shown in Table 2. A basal fertilizer (BF) of 30% of total N, 150 kg P2O5 hm2 (calcium superphosphate) and 100 kg K2O hm2 (potassium chloride) was broadcast and mixed into the topsoil (0e10 cm) before transplanting. The first and second topdressing Urea-N fertilizers (TF, 40% of total N; PF, 30% of total N) were surface applied without incorporation at the tillering and panicle initiation stages, respectively. The local rice cultivar (Wuyunjing 23) was used in 2015 and 2016. The rice seedlings were transplanted on 22 June and 7 July with a density of 100 plants m2 and were harvested on 31 October and 25 October in 2015 and 2016, respectively. All of the soil columns were maintained under continuously flooded conditions at 3e5 cm depths and followed without water logging until a week before rice harvesting, except for a midseason drainage for 1 week between tillering and the turning-green stage. The midseason drainage was started on July 27, 2015 and August 6, 2016, and ended on August 1, 2015 and August 13, 2016, respectively. Fertilization and irrigation were conducted at the same time, and the amount of irrigation water was kept consistent for all treatments. When supplementary N fertilizer was applied, the N amount supplied from urea was calculated based on the N amount from the previous irrigation water to ensure that the N inputs of the four treatments were equivalent. 2.3. CH4 and N2O emission CH4 and N2O gas samples were collected during the rice growing season (June to October) by using the Static-Gas Chamber method (Ma et al., 2009). The chamber was a transparent Plexiglas cylinder with a 100-cm height and 32-cm inner diameter. The chamber was equipped with a circulating fan to ensure complete gas mixing and was wrapped with a layer of sponge and aluminum foil to minimize air temperature changes inside the chamber during the period of sampling. When the gas sampling was conducted, the chamber was placed over the vegetation with the rim of the chamber fitted into the water-filled groove of the collar. Gas samples were collected from the headspace gas from 0800 through 1100 LST since the soil temperature during this period was close to the mean daily soil temperature (Zou et al., 2005; Jiang et al., 2015; Ma et al., 2009). Gas samples were taken at 1, 2, 3, 5, and 7 d after each fertilization, and then were taken once a week at other stages throughout the whole season (Sun et al., 2013). The mixing ratios of CH4 and N2O were simultaneously determined with a modified gas chromatograph (Agilent GC-7890B, Agilent Technologies, Palo Alto, California, USA)

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Table 2 Average nitrogen application of each treatment in 2015 and 2016/kg hm2 (g column1). Treatments

Urea N

SWN STN WN TN CK

131.6 227.8 131.6 227.8 0

(0.93)a (1.61) (0.93) (1.61)

Sewage N

Tap water N

Total N

108.4 (0.77) 0 108.4 (0.77) 0 0

0 12.2 (0.09) 0 12.2 (0.09) 0

240 240 240 240 0

(1.70) (1.70) (1.70) (1.70)

SWN, sewage irrigation with straw returning; STN, tap water irrigation with straw returning; WN, sewage irrigation without straw; TN, tap water irrigation without straw; CK, tap water irrigation without straw and N fertilizer. a The N amount is given in kg hm2, whereas the figure in brackets is the amount (g) per soil column.

equipped with a flame ionization detector (FID) and an electron capture detector (ECD) (Zou et al., 2009). Fluxes were determined from the slope of the mixing ratio change in five samples, taken at 0, 15, 30, and 45 min after chamber closure (Ma et al., 2009). The CH4 flux (mg m2 h1) and N2O flux (mg m2 h1) were calculated from the temporal increase in gas concentration inside the chamber per unit time. F ¼ r  H  (Dc/Dt)  273/(273 þ T) where F is the CH4 flux (mg CH4 m2 h1) or N2O flux (ug N2O m2 h1), r is the CH4 or N2O density at standard conditions (mg cm3), H is the chamber height above the soil-water layer (m), Dc/ Dt is the CH4 or N2O accumulation rate (ppm h1 and ppb h1, respectively), and T is the mean air temperature inside the chamber during sampling. The seasonal total CH4 and N2O emissions were calculated by linearly interpolating the gas emissions between the sampling dates (Zou et al., 2009).

2.4. NH3 volatilization The ammonia volatilization flux was measured with a continuous airflow enclosure method using a chamber in each soil column (Sun et al., 2013). The NH3 volatilization rate was measured on each of the first seven days after each fertilization and then on a weekly interval until the next fertilizer application or rice harvest. The NH3 volatilization rate was measured from 09:00 a.m. to 11:00 a.m. and from 14:00 p.m. to 16:00 p.m. daily until there was no detectable color change of the NH3 absorbent (Sun et al., 2013) (composed of 80 mL of 2% boric acid and a mixed indicator of methyl red, bromocresol green and ethanol). After the air had continuously flowed for 2 h, the chambers were removed to eliminate the differences in conditions between the inside and outside of the chamber. The NH3 absorbent solution was titrated with

Table 1 Properties of the experimental sewage and tap water. Water type

pH

TN /mg L1

NHþ 4 -N /mg L1

TP /mg L1

TK /mg L1

TC /mg L1

TOC /mg L1

C: N

Tap water Sewage

7.7 ± 0.02 7.6 ± 0.05

2.22 ± 0.05 21.47 ± 0.36

0.07 ± 0.01 18.14 ± 2.04

0.13 ± 0.02 1.23 ± 0.20

0.14 ± 0.02 1.61 ± 0.02

18.24 ± 0.57 79.66 ± 5.77

5.61 ± 0.28 55.7 ± 6.21

8.22 3.71

Water type

Cd ug L1

As ug L1

Cr ug L1

Pb ug L1

Cu ug L1

Zn ug L1

Hg ug L1

Escherichia coli MPN L1

Tap water Sewage

0.4 ± 0.1 1.2 ± 0.2

2.8 ± 1.7 5.2 ± 1.4

1.6 ± 0.3 2.4 ± 0.2

1.4 ± 0.3 1.7 ± 1.2

4.0 ± 3.4 10.2 ± 6.7

75.4 ± 15.1 98.5 ± 25.3

/ 0.006

210 ± 51 4950 ± 72

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S. Xu et al. / Atmospheric Environment 169 (2017) 1e10

0.01 M H2SO4. The ammonia volatilization flux was calculated using the following equation (Wang et al., 2012): Fluxvol ¼ 14  V  C  A1  t1 where Fluxvol denotes the mean ammonia volatilization flux (g N ha1 h1); 14 is the atomic weight of N (g mol1); V is the volume of H2SO4 titrated (L); C is the concentration of H2SO4 (mol L1); A is the area of the chamber base (m2); and t is the continuous measurement time. The factor for conversion from square meters to hectares is 104. The daily NH3 volatilization rate was calculated by the average of the rates measured on each day. Total NH3 volatilization of the rice season was calculated by the sum of the daily volatilization rates over the measurement period. 2.5. Crop grain yield measurement Crop grain yields from each soil column were collected at harvest and adjusted to 14% moisture content. 2.6. GWP calculations GWPs were calculated by multiplying the seasonal total CH4 and N2O emissions by their respective radiative forcing potentials. Given a 100-year time horizon, we took the radiative forcing potentials for CH4 and N2O to be 28 and 265, respectively, when the value for CO2 is taken as 1 (IPCC, 2013). Accordingly, the GWPs (kg hm2) of the different treatments were calculated using the following equation: GWPs ¼ 28  CH4 þ265  N2O

3. Results 3.1. Rice grain yield Rice grain yields were increased by N application in both years (Fig. 1). Straw returning slightly lowered the rice yields compared with those without straw returning, irrespective of the irrigation water types, although the difference was not significant. No yield loss was found in domestic sewage irrigation treatments when compared to that with tap water irrigation, although the chemical N fertilizer rate was only 133.4 kg hm2, which was 55.6% of that of tap water irrigation. The yield of WN was slightly higher than TN in both years. ANOVA showed that the interaction of straw incorporation and irrigation water type was not significant to the yield. 3.2. Greenhouse gas emissions 3.2.1. CH4 emissions The CH4 fluxes in 2015 and 2016 are shown in Fig. 2. The seasonal patterns of CH4 emissions were mainly affected by fertilizer application, straw returning, and irrigation type. Several small emissions peaks during the rice-growing season were observed in both years. After the rice had been transplanted, CH4 emissions increased steadily when the soil column was waterlogged. A small peak was observed after basal fertilizer application, the highest peak fluxes were observed during the midseason drainage stage, and another small peak was observed after the panicle initiation fertilization. CH4 emissions then decreased for the grain-filling stage until the rice was harvested and were stable at 0e10 mg m2$h1. Straw returning dramatically increased the CH4 emissions over those without straw returning, especially at the

The greenhouse gas intensity (GHGI, kg CO2-eq$t1 grain yield) was calculated following the method of Jiang et al. (2015) using the following equation: GHGI ¼ GWPs/grain yield Although NH3 itself is not a greenhouse gas, the emission and subsequent re-deposition of NH3 results in damage to air, water and soil quality and indirect emission of N2O (Ferm, 1998). According to the IPCC (2006), about 1% (0.2e5%) of the NH3-N emitted is converted to N2O after deposition to land. This value was used to estimate the GWP (CO2-equivalents, kg$hm2) considering the indirect N2O emission associated with NH3 volatilization in the current study. Then, the total GWP (TGWP) caused by the gas emission including NH3 was compared to evaluate the comprehensive effect of different treatments on global warming. GWP(NH3) ¼ 1%  265  NH3 TGWP ¼ GWPs þ GWP(NH3)

2.7. Statistical analyses Statistical analysis was performed using SPSS version 19.0 (SPSS Inc., Chicago, IL, USA). The effects of irrigation, straw returning, and their interactions on grain yield, GHG emissions, NH3 emission, GWP, GHGI, and TGWP were evaluated using two-way ANOVA. The difference between treatments was tested using Duncan's multiple range test to identify significant differences at a significance level of 0.05 (P < 0.05). The figures were constructed using Origin Pro 8.0.

Fig. 1. Rice grain yield in 2015 and 2016 under different treatments (different letters above the column indicate a significant difference at P < 0.05).

S. Xu et al. / Atmospheric Environment 169 (2017) 1e10

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determined by whether the straw was returned or not. Compared to tap water irrigation with the same N input, the seasonal CH4 emissions with sewage irrigation significantly decreased 24.5% in 2015 and 26.6% in 2016 under straw returning but increased slightly under straw removal (Table 3). 3.2.2. N2O emissions Seasonal patterns of N2O emissions were quite different from those of CH4 fluxes, and substantial N2O emissions occurred after the fertilizer was applied and during the midseason drainage (Fig. 3). Straw returning significantly increased the N2O emissions when compared with those without straw returning under the two irrigation water types in both years. The highest fluxes of TN were only 720.0 mg$m2$h1 in 2015 and 863.1 mg$m2$h1 in 2016, which increased to 1541.1 mg$m2$h1 in 2015 and 1468.6

Fig. 2. CH4 fluxes in 2015 and 2016 under different treatments; the arrow indicates the N fertilizer application. NOTE: B represents the basal fertilization; T represents the tillering fertilization; P represents the panicle initiation fertilization.

early growth stage. Under common irrigation, the highest fluxes of TN were only 3.6 mg m2$h1 in 2015 and 4.9 mg m2$h1 in 2016, which were increased to 54.7 mg m2$h1 in 2015 and 63.6 mg m2$h1 in 2016 when the straw was returned to the field (STN). Correspondingly, the seasonal CH4 emissions in the whole rice season of STN were 14e15 times that of TN. A similar result was also found in the sewage irrigation treatment (Table 3). The highest fluxes of CH4 emission increased dramatically from 4.8 mg m2$h1 to 44.8 mg m2$h1 in 2015 and from 8.5 mg m2$h1 to 48.5 mg m2$h1 in 2016 when the straw was returned. The seasonal CH4 emission in the whole rice season of SWN was 8e10 times that of WN (Table 3). When compared to the zero-fertilizer application treatment (CK), chemical N fertilizer application (TN) significantly increased the CH4 emissions in both years. Sewage irrigation also influenced CH4 emissions and seemed to be

Fig. 3. N2O fluxes in 2015 and 2016 under different treatments; the arrow indicates the N fertilizer application. NOTE: B represents the basal fertilization; T represents the tillering fertilization; P represents the panicle initiation fertilization.

Table 3 Seasonal emissions of CH4, N2O and NH3 under different treatments in 2015 and 2016. Treatments

SWN STN WN TN CK S W SW

2015

2016

CH4 /g m2

N2O /g m2

NH3 /g m-2

CH4 /g m-2

N2O /g m2

NH3 /g m2

21.88b 28.99a 2.38c 1.95c 1.20d 10492.35*** 215.58*** 275.14***

0.37b 0.61a 0.22d 0.31c 0.17e 823.99*** 449.16*** 85.34***

7.85b 10.96a 4.14d 5.83c 2.25e 382.98*** 112.55*** 9.90*

19.95b 25.04a 2.17c 1.69c 1.00d 7985.80*** 100.63*** 146.36***

0.38b 0.60a 0.25c 0.36b 0.21c 38.49*** 31.91*** 3.78***

7.37b 10.13a 4.78d 6.03c 1.53e 135.49*** 48.60*** 6.80*

NOTE: Values followed by different letters within a column are significantly different at P < 0.05; * significant at P < 0.05; ** significant at P < 0.01; *** significant at P < 0.001.

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mg$m2$h1 in 2016 when the straw was returned to the field (STN). The seasonal N2O emissions over the whole rice season of STN were 1.7e1.9 times that of TN. A similar result was also found in the sewage irrigation treatment (Table 3). The highest fluxes of N2O emission were increased dramatically from 320.9 mg$m2$h1 to 929.7 mg$m2$h1 in 2015 and from 1057.4 mg$m2$h1 to 1484.8 mg$m2$h1 in 2016 when the straw was returned. The seasonal N2O emissions over the whole rice season of SWN were 1.5e1.7 times that of WN (Table 3). The chemical N fertilizer application also significantly increased the N2O emissions compared to CK. N2O emissions were decreased under sewage irrigation compared to tap water irrigation, irrespective of straw returning. The seasonal N2O emissions with sewage irrigation significantly decreased, by 29.8e39.0% in 2015 and 30.0e37.0% in 2016. 3.3. Ammonia volatilization The NH3 volatilization flux patterns were similar for different treatments in both years. NH3 volatilization flux increased immediately, and the peaks occurred on the first or third day after N application (Fig. 4). Then, the NH3 volatilization flux dropped to the CK level by the 7th day after fertilization. The NH3 volatilization flux was significantly affected by N application; three peaks appeared after fertilization, with the highest peak at the tillering fertilizer stage. In contrast to CK, the seasonal amounts of NH3 volatilization increased on average by 3.02-, 5.58-, 2.36- and 3.14-fold in SWN, STN, WN and TN, respectively. Straw incorporation increased NH3 volatilization. At the tillering fertilizer stage, the peaks of NH3 volatilization flux increased 1e3-fold in SWN and STN compared to those without straw returning. Finally, the seasonal NH3 emissions

increased by 54e90% under straw returning (Table 3). However, domestic sewage irrigation significantly decreased NH3 volatilization flux compared to those treatments with tap water irrigation. The peaks of NH3 volatilization flux at the tillering fertilizer stage decreased 29.4e31.9% and 32.7e54.0% in SWN and WN compared to WN and TN, respectively. Correspondingly, the seasonal NH3 emissions of sewage irrigation decreased by 28% and 25% compared with tap water irrigation treatments in 2015 and 2016, respectively, irrespective of whether straw was returned or not (Table 3). The interaction of straw between water irrigation treatments on total NH3 losses was significant. 3.4. GWP and GHGI The indirect GWP (CO2-equivalents, kg$hm2) caused by NH3 volatilization was only 3e17% of GWPs of N2O and CH4 (Table 4). Straw returning significantly increased the GWPs over a 100-year horizon by 3e4-fold and 5e6-fold under sewage and tap water irrigation in both years, respectively. Compared to tap water irrigation, sewage irrigation decreased the GWPs whether straw was returned or not, and the difference was significant under straw incorporation in both years. Chemical fertilizer N application also significantly promoted the GWPs. In consideration of the TGWP caused by CH4, N2O and NH3, the difference caused by sewage irrigation and N application was slightly enlarged, but the difference caused by straw was decreased a little. GHGI and TGWP per unit rice yield were significantly increased by straw returning whether under sewage irrigation or tap water irrigation. Sewage irrigation had a mitigating effect on GHGI, especially for the straw returning treatment, and the difference was significant in both years. A significant interaction was observed between straw and sewage irrigation. 4. Discussion 4.1. Domestic sewage irrigation maintained a high yield with a reduced N rate

Fig. 4. Ammonia volatilization flux in 2015 and 2016 under different treatments; the arrow indicates the N fertilizer application. NOTE: B represents the basal fertilization; T represents the tillering fertilization; P represents the panicle initiation fertilization.

The effect of straw incorporation on yield seems to be inconsistent in that it varied with the weather, the amount of residue returned and the water and nitrogen management (Liu et al., 2014; Bi et al., 2009; Yao et al., 2010). In our study, crop residue incorporation had no significant effect on yield, which is similar to the results reported by Bhattacharyya et al. (2012), Timsina (2005). As reported by Zou et al. (2009) and Minhas et al. (2015), domestic sewage irrigation increased the rice yield due to the extra N (57e74 kg hm2) and organic matter brought by the sewage irrigation. In this paper, sewage irrigation had no significant difference in grain yield compared to the tap water irrigation with the same N input (240 kg hm2), including the 108 kg hm2 N in the sewage (Fig. 1). This result means that 44.4% of the chemical N fertilizer rate was reduced in rice. A similar result was also found by Minhas et al. (2015) where rice grain yields equal to those of groundwater irrigation with 100% NP were obtained with sewage irrigation and 50% NP. The rice grain yield increased by 29% and 57% under N-rich wastewater irrigation when 8% and 15%, respectively, of the chemical N fertilizer was substituted by wastewater (Sun et al., 2013). Additionally, domestic sewage irrigation promoted root growth, increased the nutrient contents in crops and the protein content of grain, and improved the physical properties and fertility of soils (Yadav et al., 2002; Mojid et al., 2012; Minhas et al., 2015). It should be noted that the chemical N rate must be reduced when irrigating with domestic sewage to avoid potential lodging caused by the excessive N supplied by sewage (Minhas et al., 2015). Being domestic sewage, especially after it had been treated in wastewater

S. Xu et al. / Atmospheric Environment 169 (2017) 1e10

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Table 4 Global warming potentials and greenhouse gas intensities under different treatments. Treatments

SWN STN WN TN CK S W SW

2015

2016

GWPs /kg hm2

GWP (NH3) /kg hm2

TGWP /kg hm2

GHGI /kg kg1

GWPs /kg hm2

GWP (NH3) /kg hm2

TGWP /kg hm2

GHGI /kg kg1

7110.6b 9727.3a 1249.1c 1374.7c 799.5d 17912.6*** 666.7*** 550.2***

208.1b 290.4a 109.8d 154.5c 59.6e 383.0*** 112.6*** 9.9*

7318.7b 10017.7a 1358.9d 1529.1c 859.2e 18066.8*** 712.5*** 553.4***

0.49b 0.65a 0.08c 0.10c 0.06c 302.7*** 9.9* 6.9*

6587.3b 8601.2a 1278.4c 1431.9c 839.5d 4590.3*** 138.5*** 102.0***

195.4b 268.4a 126.6d 159.8c 40.6e 135.5*** 48.6*** 6.8*

6782.8b 8869.7a 1405c 1591.8c 880.1d 4919.6*** 158.8*** 110.9***

0.49b 0.64a 0.09cd 0.11c 0.07d 1459.3*** 43.6*** 30.4**

NOTE: The GWP factor (mass basis) for CH4 is 28, and for N2O, it is 265 in the time horizon of 100 years. GHGI, GWP per unit of grain yield. S, W, GWP and GHGI represent straw, sewage, Global warming potentials, and greenhouse gas intensities, respectively. Values followed by different letters within a column are significantly different at P < 0.05; ns means not significant, * significant at P < 0.05; ** significant at P < 0.01; *** significant at P < 0.001.

treatment plants, toxic metals such as Cd, Pb, and Cr and pathogens were all very low and can meet the national agricultural irrigation water quality standard in China except for the N concentrations; therefore, the risk for food safety is very low and the contents of toxic metals and pathogens in the crops were only in trace quantities and below permissible critical levels even after three decades of sewage irrigation (Minhas et al., 2015; Yadav et al., 2002). However, the soil contents of heavy metals such as Pb, Cd, Zn, Fe and Mn were observed to be increased with sewage irrigation in some studies (Rothenberg et al., 2007; Fu et al., 2008; Minhas et al., 2015; Yadav et al., 2002). Though many studies have confirmed the benefits of domestic sewage irrigation in terms of crop yields, soil fertility and the recycling of water and nutrients, there remains a need for continuous monitoring of the concentrations of potentially toxic elements in soils, plants and groundwater on a long-term basis. The criteria of proper amount and time of sewage irrigation based on the crop types and soil qualities also need to be further studied to ensure the sustainability of agricultural development. 4.2. Domestic sewage irrigation reduced the GHG emissions from the paddy fields with straw returning 4.2.1. CH4 fluxes Straw returning significantly increased the CH4 emission flux, irrespective of the water irrigation type, which was consistent with previous findings (Ma et al., 2009). Straw returning provided a carbon source material for the generation of CH4, and a large amount of straw-C was transformed to CH4 during the rice growing season (Sui et al., 2015). Also, the soil reducibility was enhanced by straw returning, which was conducive to the growth and reproduction of methanogens and resulted in increased CH4 emissions (Chen et al., 1994). Sewage irrigation increased CH4 emissions under straw removal, which is consistent with the findings of Zou et al. (2009). However, sewage irrigation significantly reduced CH4 emissions under straw returning in our study (Table 1). Due to the massive amount of organic matter in the sewage (Yadav et al., 2002; Carr et al., 2004; Xie et al., 2007), the decomposition of organic matter provided a substrate for the generation of CH4, and thus, increased CH4 emissions were observed in sewage irrigation without straw returning (Zou et al., 2005). For paddy fields with straw returning, sewage irrigation increased the microbial N content and aerobic cellulose decomposing bacteria in the soil (Zhang et al., 2014), which promoted the decomposition of straw (Xu et al., 2016) and lowered the methanoic acid and acetate content in soil. The substrate for methanogen growth was decreased, and the activity of methanogens was inhibited; thus, CH4 emissions were reduced

when straw returning was combined with sewage irrigation. Moreover, it is well known that the emission of CH4 from rice paddy soil to the atmosphere is the result of the balance between its production and oxidation. The existence of NHþ 4 can stimulate CH4 emission from rice paddy fields due to the competition of NHþ 4 for the oxidation with CH4 by methanotrophs (Mosier et al., 1991). In this study, total N input was the same including the N carried in sewage water, and the soil NHþ 4 content would decrease because some N was immobilized by bacteria to decompose the straw, which suggested that more of the CH4 produced would be oxidized and that the final CH4 emission would be reduced. Furthermore, it has been demonstrated that sulfate (SO2 4 ) can depress CH4 emissions (Sophoanrith et al., 2011) and that the lower CH4 emissions under straw returning may also be related to the sulfate (46.9 mg/L in sewage water in the present study) brought by sewage irrigation. For a paddy without straw returning, the depressing effect of sulfate on CH4 emission would be offset by the stimulation effect of rich ammonia and organic matter with sewage irrigation. In addition, the responses of the physicochemical properties and microbial activity of the soil related to the generation of CH4 to sewage irrigation may vary with straw returning or not (Huang et al., 1997; Zou et al., 2009), which may be another reason for the difference in CH4 emission caused by sewage irrigation between straw returning and straw removal. 4.2.2. N2O fluxes The N2O emission is affected by the processes of nitrification and denitrification, which are affected severely by soil conditions such as moisture, temperature, synthetic N fertilizer management, and so on (Shan and Yan, 2013). Crop residue returning may have effects on soil moisture, temperature, dissolved organic carbon concentration, inorganic N content, microbial activity and redox potential, thus leading to regulation of N2O release in soil. Generally, N2O release was inhibited when wheat residue was applied in paddy fields due to the reduced nitrogen substrate availability for N2O production, which resulted from the net immobilization of plant-available nitrogen caused by the straw incorporation with a high C:N ratio (Zou et al., 2005; Ma et al., 2009; Xia et al., 2014). However, straw returning showed an increased N2O emission in our study. This may be partially associated with the high chemical N rate (240 kg hm2) and a relatively high ratio (40%) of N applied in the basal application. The N immobilization may not be obvious under this situation, and the soil organic carbon content with straw returning increased 18e30% in our study and may have promoted the denitrification rate in soil caused by denitrifiers. As shown in Fig. 3, the emission flux of N2O is small when the paddy field is submerged and dramatically increased during the mid-season

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drainage (Cai et al., 1997; Zou et al., 2005, 2009). The highest peak of N2O flux was observed when the field was reflooded in both years, and it was greater in the straw returning treatments (Fig. 3). During this field-drying period, the paddy is more like an upland field, and the soil temperature and water content with straw incorporation may be higher and more favorable for denitrification (Ma et al., 2010; Shan and Yan, 2013); hence, enhanced N2O emission was observed. Sewage irrigation significantly decreased N2O emissions, regardless of the straw returning or not (Table 3). This was mainly associated with the N inputs (Bouwman et al., 2002) and the nitrogen supplying capacity of the soil (Li et al., 2008). Although the total N input was the same in the present study, the chemical N rate was 227.8 kg hm2 under tap water irrigation, which is higher than that (131.6 kg hm2) under sewage irrigation. Also, the N contained in sewage water was mainly ammonia and was continuously added to the paddy fields with an interval of 3e4 days. Therefore, the soil available N content after each fertilization under sewage irrigation was much lower than that under tap water irrigation, which resulted in the reduced N2O emissions. However, when the chemical N rate of the sewage irrigation treatment was the same as the traditional river water irrigation treatment, enhanced N2O emission was observed due to the extra N brought by the sewage improved N availability for soil nitrification and denitrification processes (Zou et al., 2009). Sun et al. (2013) also reported that irrigating with N-rich wastewater did not result in more environmental effects caused by N2O emission compared with the CK treatment when the N input amounts were balanced. On the other hand, the availability of organic C is often considered to be a major factor influencing soil nitrification and denitrification processes where N2O is produced (Huang et al., 2004; Zou et al., 2005). Irrigation with sewage provided a source of readily available C in the soil, which could potentially inhibit the activity of reductase involved in the conversion of nitrite and nitrate to nitrous oxide and may contribute to reducing the N2O emissions (Yao et al., 2010). In addition, the percentage of N2O formation in the denitrification products (i.e., the total amount of N2O and N2 production) has been shown to decrease with increasingly anoxic conditions (Weier et al., 1993). In paddy fields, sewage irrigation stimulated microbial activity and O2 consumption, further facilitating the anaerobic conditions that are conducive to the reduction of N2O to N2 during denitrification and resulting in lower N2O emissions. 4.3. Domestic sewage irrigation significantly reduced the NH3 volatilization of paddy fields The decisive factor affecting the NH3 volatilization loss was the NHþ 4 -N concentration in the floodwater, which was influenced by N application and straw incorporation (Li et al., 2008; Rochette et al., 2009). A significantly positive correlation between NH3 volatilization loss and NHþ 4 -N concentration was observed (Xu et al., 2016). Crop straw increased the microorganism activity and the pH in which accelerated urea hydrolysis would raise the floodwater NHþ 4N concentration (Wang et al., 2012; Hayashi et al., 2010; Xu et al., 2016). Therefore, straw incorporation significantly increased the NH3 volatilization loss compared to straw removal treatments in both years (Table 3), consistent with the previous study (Wang et al., 2012; Hayashi et al., 2010). The NH3 volatilization loss with straw incorporation ranged from 73.7 to 109.58 kg N hm2, accounting for 30.7e45.6% of N applied, which was higher than the previous studies (Wang et al., 2012; Chen et al., 2015). This was mainly because our experiment was carried out in a greenhouse, where the temperature was higher than the outdoor temperature and the ammonia volatilization rate is closely related to temperature. Domestic sewage irrigation significantly decreased NH3

emissions, irrespective of straw returning or not. This was mainly caused by the reduced Urea-N application in domestic sewage irrigation treatments, which decreased the NHþ 4 -N concentration after fertilization. Therefore, the peak of ammonia volatilization flux was obviously reduced (Fig. 3). Furthermore, a decreased pH of the flood water was also observed in sewage irrigation treatments, which also contributed to the mitigation of NH3 emissions (Xu et al., 2016). 4.4. Domestic sewage irrigation could mitigate the GWP of paddy fields under straw returning GWP is usually used to estimate the comprehensive effect of CH4 and N2O on climate change (Frolking et al., 2004). GHGI represents the effect of production of a specific grain yield on the climate in the process of agricultural production. It is a comprehensive evaluation index that coordinates and unifies the environmental benefits and economic benefits (Frolking et al., 2004). In our study, straw returning increased GWP and GHGI compared to straw removal, regardless of the irrigation water type (Table 4). Compared to tap water irrigation, sewage irrigation decreased GWP and GHGI of paddy fields whether straw was returned or not. In addition, NH3 emitted from paddy fields re-deposited to land subsequently, and then a small portion of it could convert to N2O and make a contribution to global warming potential. Taking into account the indirect N2O warming potential of NH3 converted, the total GWP increased significantly by straw returning, regardless of the irrigation water type (Table 4). However, domestic sewage irrigation can significantly mitigate the total GWP by 13e28%. Since straw returning has been widely used not only in developing countries such as China but also in developed countries such as the USA, domestic sewage irrigation seems to have the potential to reduce both the GHG emissions and NH3 volatilization loss of paddy fields with straw returning to simultaneously maintain the high rice yield and save the N-fertilizer input. However, the results were from a two-year soil column experiment, and the long-term effects of straw and domestic sewage irrigation on greenhouse gas mitigation and crop production need to be further studied in paddy fields. 5. Conclusions Under the same total N input, sewage irrigation showed no significant effect on rice yield whether straw was returned or not but reduced the chemical N rate by 45.2% due to the rich N in sewage water. Straw returning significantly increased the CH4 emissions and NH3 volatilization compared to straw removal treatments in both years, while sewage irrigation significantly mitigated the CH4 emission and NH3 volatilization with straw returning. N2O emissions were slightly affected by straw returning and irrigation water type. Considering the total GWP caused by CH4 and N2O emission and the indirect contribution of NH3 volatilization, sewage irrigation could significantly reduce the GWPs from paddy fields by 24e27% when the straw is returned and 14e16% when the wheat straw is removed. Therefore, sewage irrigation combined with straw returning may be a sustainable environmentally friendly and resource-saving agricultural management strategy for rice to mitigate GHG and NH3 emission and reduce the chemical N input. Acknowledgments This research was supported by the Special Fund for Agro-Scientific Research in the Public Interest (201503106), the National Key Research and Development Program (2016YFD0801101) and the Jiangsu Agriculture Science and Technology Innovation Fund

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