Co-application of biochar and compost with decreased N fertilizer reduced annual ammonia emissions in wetland rice

1. Introduction

More than 90% of rice (Oryza sativa) in the world is grown in Asia, feeding more than 60% of the global population and it supports the livelihood of millions of small and marginal farm families in south Asia (Brolley, 2015). Bangladesh is the third largest rice producing country in the world where rice contributes about 4.5% to the country's gross domestic product. In this country, rice is grown in three seasons i.e., irrigated winter rice called Boro, pre-monsoon rice called Aus and monsoon rice called Aman. In 2020–21, gross annual production of 3-seasons' rice was 36.61 Mt (BBS, 2021). Despite large quantities of nitrogenous fertilizer being applied to maintain rice yields, there is low use efficiency (30–35%) of this fertilizer, and significant gaseous nitrogen (N) loss (Xia and Yan, 2012). In Bangladesh, N is applied at around 150 kg N ha⁻¹ season⁻¹, which is almost double the rate of Japan (80 kg N ha⁻¹ season⁻¹) and a little higher than in the United States (140 kg N ha⁻¹ season⁻¹) (Linquist et al., 2015; Xia et al., 2016). Ammonia (NH₃) is one of the most important by-products of applied N in rice field and volatilization of NH₃ is the primary source of soil nitrogen loss (Pan et al., 2016; Xu et al., 2019; Kuttippurath et al., 2020; Wang et al., 2021).

In 2021, Bangladesh ranked first globally in air pollution due to elevated concentrations of CH₄ and NH₃ in the air (IQAir, 2021). Even though NH₃ is not a potential greenhouse gas (GHS), its emissions and re-deposition can have negative impacts on the environment (Zhang et al., 2020). Volatilized NH₃ is a secondary source of N₂O and NO (Mosier et al., 1998), and NH₃ volatilization is responsible for around 30% of N deposition (Wolfe and Patz, 2002). Ammonia has a negative impact on regional air quality and human health generating aerosols in the atmosphere, influencing the radiation balance by scattering light and changing the earth's reflectivity (Xu and Penner, 2012; Stokstad, 2014). In Asia, agricultural gaseous N losses including NH₃ volatilization may reach 18.8 Tg N yr⁻¹ in 2030 (Zheng et al., 2002; Liu et al., 2021). The global estimate of NH₃ emissions from urea-fertilized soils ranges from 10 to 20%, although in warmer zones, it is substantially higher (Cantarella et al., 2018). Because of extensive rice cultivation, the Indo Gangetic Plain has been identified as a hotspot for NH₃ fluxes but estimates of the rates of loss are limited (Kuttippurath et al., 2020; Uddin et al., 2021; Jahangir et al., 2022).

Mitigating NH₃ emissions from agriculture will not only cut the cost of fertilizer N, but it will also improve air and water quality (Zhao et al., 2017). To limit N losses, various practices are proposed such as use of nitrification inhibitors, urease inhibitors (UI), elemental S, and polymers (He et al., 2018), crop residue removal management (Battaglia et al., 2018, 2021), and organic amendments (Saarnio et al., 2013; Malińska et al., 2014). The role of organic amendments like poultry manure, biochar, compost, etc. in mitigating NH₃ fluxes from wetland rice fields is unresolved since some researchers have reported positive effects (Saarnio et al., 2013; Malińska et al., 2014; Ali et al., 2019), while others reported negative effects (Feng et al., 2017; Chu et al., 2019; Rahaman et al., 2020). Ammonia emissions increase with the N fertilizer rate (Uddin et al., 2021; Jahangir et al., 2022) which suggests that with organic amendments the rate of N fertilizer application could be decreased to reduce both economic and environmental costs while maintaining soil quality. Biochar is a carbon-rich substance made from the pyrolysis of organic matter (Lehmann and Joseph, 2009). It has been reported to prevent NH₃ loss and improve soil health, crop output, and soil carbon sequestration, while also recycling organic waste (Diatta et al., 2020). Biochar and compost mixture can be utilized as fertilizer sources to increase soil nutrients and reduce nutrient losses (Banik et al., 2021).

Ammonia emissions are estimated by the IPCC Tier 1 method but only a single emission factor is scheduled (Bouwman, 1996). While a large amount of N loss as NH₃ can occur, the exact quantity is not known for accurate N balance calculations for many managed agricultural systems including the rice-based cropping patterns of South Asia. Previously, Uddin et al. (2021) evaluated the impact of Conservation Agriculture along with different N fertilization rates on NH₃ volatilization in winter rice (Boro rice). They reported that NH₃ volatilization accounted for 16–21% of the applied N. However, there is no baseline data of NH₃ volatilization in the other two rice growing seasons when temperature is higher (Aus and Aman rice), nor on the impacts of reduced N fertilizer application when co-applied with organic amendments (i.e., integrated plant nutrition system (IPNS) approach) on NH₃ volatilization. We hypothesize that co-application of organic fertilizer such as biochar, rice mill ash (RMA) and compost together with inorganic N fertilizers, which together provide the same amount of N as chemical fertilizer alone, would reduce NH₃ volatilization loss without changing the soil N status. Thus, the study was conducted to evaluate the effects of rice husk ash, biochar alone or with compost (IPNS basis) on seasonal and annual NH₃ emissions, rice yields and soil quality.

2. Materials and methods

2.1. Experimental site description

The study was carried out on the Soil Science Field Laboratory (24° 71.59′ N, 90° 42.50′ E) of Bangladesh Agricultural University (BAU) in Mymensingh, Bangladesh. The experiment was done with an annual irrigated rice– pre-monsoon rice – monsoon rice cropping sequence, which is a common cropping sequence followed by the farmers of this country. The irrigated rice season, pre- monsoon rice season and monsoon rice season were occupied by Boro, Transplanted Aus (T. Aus), and Transplanted Aman (T. Aman) rice growing seasons, respectively. The field site was characterized as a Non-calcareous Dark Gray Floodplain soil (Aeric Haplaquept in US Soil Taxonomy), and belongs to agro-ecological zone-9, Old Brahmaputra Floodplain soil (FAO/UNDP, 1988). The soil is moderately drained with a silt loam texture and near neutral pH (6.5). The region has a sub-tropical monsoon climate with a mean annual temperature of 26°C, average annual rainfall of 1,800 mm, and relative humidity of 85% (Uddin et al., 2021, Supplementary Data 1).

2.2. Experimental design and crop management

The experiment was conducted with the same treatment combinations for Boro – T. Aus – T. Aman rice crops in sequence, but with different levels of a nutrient based on the requirements of individual crop and their target yields. That experiment was conducted under integrated plant nutrition system (IPNS; nutrient contents in organic amendments were subtracted from the full recommended fertilizer dose, i.e., RD of chemical fertilizers) where six treatments with four replications were applied in each season. The treatments were: (T₁) no fertilizer (control), (T₂) RD, (T₃) poultry manure biochar + decreased dose of recommended fertilizer (DRD), (T₄) rice husk ash + DRD, (T₅) compost + DRD, and (T₆) compost + biochar + DRD, laid out in a randomized complete block design (RCBD) with four replications. Total plot number was twenty-four for each season and the same plots were used for consecutive rice growing seasons and the unit plot size was 5 m × 4 m, with a 0.75 m inter-plot space, and 1 m inter-block space. The varieties were BRRI dhan28 for Boro, BINA dhan19 for T. Aus and BRRI dhan49 for T. Aman rice, respectively. Boro rice was grown during January–April (winter season), followed by T. Aus rice as a rainfed crop from May to August (pre-monsoon), and then T. Aman rice from August to November (monsoon).

The rate of chemical fertilizer application was based on Fertilizer Recommendation Guide (FRG, 2018) for the test crops. The nutrient contents of used organic amendments are presented in Table 1 while the recommended doses of nutrients for three seasons were presented in Table 2. Urea, triple super phosphate, muriate of potash, gypsum and zinc sulfate were used for N, phosphorus (P), potassium (K), sulfur (S) and zinc (Zn) sources, respectively. Except urea all the nutrients were applied during land preparation. For both Boro and T. Aman rice nitrogenous fertilizer (urea) was applied in equal three splits, followed interval for Boro rice was at 10, 31, and 53 Days After Transplanting (DAT) and for T. Aman that interval was at 9, 24, and 39 DAT. In T. Aus rice two splits of urea application were followed, at 11 and 29 DAT. Compost was collected from Mazim Agro Industries Ltd and rice husk ash from a local rice mill. Biochar was produced using poultry manure by an anaerobic pyrolysis process at 450°C for 4 hr. The organic materials were air dried to 15% moisture content, pulverized and sieved with a 2 mm mesh. In T₃, T₄, and T₅ treatments organic materials were applied at the rate of 3 t ha⁻¹ where T₆ was balanced by applying 1.5 t ha⁻¹ compost and 1.5 t ha⁻¹ biochar, the remaining nutrients were applied from chemical fertilizer based on FRG under IPNS approach. Glyphosate (Round up^®) was sprayed over the field at a rate of 1.85 kg ha⁻¹ 3 days before final land preparation. The field was irrigated to maintain 3 cm standing water throughout rice growing seasons.

TABLE 1

Table 1. Chemical properties of organic amendments (poultry manure biochar, cattle compost, rice husk ash) used in three rice growing seasons.

TABLE 2

Table 2. Amounts of nutrients added from each source of organic amendments used in three rice growing seasons.

2.3. NH₃ gas sampling and analysis

Field measurements of NH₃ were conducted during January 2020–November 2021 in the rice field. A low-cost chamber was deployed in field conditions for NH₃ volatilization measurements (Nichols et al., 2018) and used for monitoring NH₃ fluxes in crop fields (Martins et al., 2021a,b; Zaman et al., 2021). The open chamber method was used to measure NH₃ fluxes in the field site on a daily basis. In the laboratory, the amount of NH₃ trapped in acid solution was estimated using the Kjeldahl principle (Keeney and Nelson, 1982). Measurements were done on the soil shortly after urea application and it was carried out until the fluxes were below the detection limit in each case.

2.4. NH₃ fluxes and emission factor calculation

The NH₃ fluxes were calculated following Equation 1.

$\begin{array}{l}\text{N}{\text{H}}_3\text{fluxes}(\text{mg}\text{N}{\text{m}}^{-2}{\text{d}}^{-1})\\ =\frac{(\text{FBR}-\text{IBR})\times 14.01\times 0.01\times 1000}{\text{Surface}\text{Area}({\text{m}}^2)\times 1000}& (1)\end{array}$

Where, NH₃ flux was measured as mg N m⁻² d⁻¹; FBR, Final Burette Reading (ml); IBR, Initial Burette Reading (ml); molecular weight of N = 14.01 g; normality of H₂SO₄ = 0.01 N; and 1000 = unit conversion factor. The sum of NH₃ fluxes on sampling days across the whole sampling period was used to estimate cumulative NH₃ fluxes.

We derived EF (%) according to Equation 2 (Mazzetto et al., 2020).

$\begin{array}{ll}\text{EF}(\%)=\frac{\text{Fluxes}\text{FT}-\text{Fluxes}\text{C}}{\text{Applied}\text{Fert}}\times 100& (2)\end{array}$

Where EF (%) = Emission Factor, in%; Fluxes FT, Fluxes from fertilizer treatment (in kg N ha⁻¹); Fluxes C, Fluxes from control treatment (in kg N ha⁻¹); Applied Fert, Amount of fertilizer applied (in kg N ha⁻¹).

Yield-scaled NH₃ fluxes were determined following the Equation 3.

$\begin{array}{l}\text{Yield}\text{-}\text{scaled}\text{N}{\text{H}}_3\text{fluxes}(\text{kg}\text{N}\text{t}\text{grai}{\text{n}}^{-1})\\ =\frac{\mathrm{Total}\text{fluxes}\text{from}\text{a}\text{plot}(\text{kg})}{\text{Yield}\mathrm{obtained}\text{from}\text{the}\text{plot}(\text{t})}& (3)\end{array}$

2.5. Measurement of grain yield

Before the final harvest of each rice growing season, plants from 1 m² area were collected from each plot, weighed and then oven dried to determine yield and system productivity i.e., pooling together the grain yields of the three rice seasons. For oven drying, 1000 grain samples of each plot were placed in an oven at 65°C until it reached constant weight to determine moisture content. After drying, rice grain samples were weighed and yields were estimated as tonne per hectare.

2.6. Soil sample collection and laboratory analysis

Composite soil samples were collected with an auger at 0–15 cm soil depth from the sites next to each NH₃ gas sampling chamber and preserved in sealable plastic bags in a cooler box. The field-moist soil was air-dried for 2 weeks in the shade at room temperature (25°C) and processed (2 mm sieved) for analysis of major soil physico-chemical parameters. During the NH₃ loss measurement, the pH of the soil was monitored in the field every seven days using a portable pH meter (HI12923; Hanna Instruments). The Kjeldahl method was used to determine total nitrogen (TN) content in the soil (Fawcett, 1954) and the wet oxidation method (Walkley and Black, 1934) was used for soil organic carbon (SOC) determination. Soil samples were extracted with 2 M KCl (1: 2.5; w/w) and ${\text{NH}}_4^{+}$ and ${\text{NO}}_3^{-}$ contents were measured using the method described by Keeney and Nelson (1982).

2.7. Statistical analysis

One-way ANOVA was performed using treatments as fixed factors. The normality test on the NH₃ data was checked before analysis. Post-hoc tests were performed to separate differences among the treatments using the Tukey-Kramer multiple comparison Test. All statistical analyses were considered significant at p ≤ 0.05, unless otherwise mentioned. All the statistical analyses were performed on Statistics 10 and Jamovi1.0.0.0 (R Package). Correlation among the parameters studied was tested by using Pearson's correlation coefficient comparison test.

3. Results

3.1. Time course of NH₃ fluxes after urea application

Ammonia fluxes reached their peaks at 2–3 days after each split of urea application in all seasons. The highest NH₃ fluxes were recorded during the second split application of urea in boro season but that was higher from first split application in both T. Aus and T. Aman seasons (Figure 1). In T. Aman rice, the NH₃ fluxes were 1.5–2.0 times higher in the first split compared to the second and third splits, while the latter two results were almost the same. The NH₃ flux peaks returned to background level at 7–10 days after each split urea application (Figure 1). The highest peak in all splits at each season ranked in the order of chemical fertilizer > RMA > compost > compost + biochar > biochar > control (Figure 1B). On the peak period at 1st, 2nd, and 3rd splits of urea fertilization the NH₃ fluxes from RD treatment were 117, 305, 160 mg N m⁻²d⁻¹ in Boro season and that were 193, 165 mg N m⁻²d⁻¹ in T. Aus and 289, 138 and 136 mg N m⁻²d⁻¹ in T. Aman season, respectively.

FIGURE 1

Figure 1. Daily NH₃ fluxes (mean ± SE; R = 4) from different plots treated with organic and inorganic fertilizers throughout the year [(A) Boro, (B) T. Aus, (C) T. Aman]. Arrows indicate the day of split urea application.

3.2. Effects on mean and cumulative ammonia fluxes

The effect of organic and inorganic fertilizers on mean and cumulative ammonia fluxes of all three rice crops was significant. In Boro rice, the highest mean and cumulative NH₃ fluxes were observed in chemical fertilizer treated plot, which was statistically similar to RMA, and the lowest emission was observed in control (Table 3). Integrated use of organic and inorganic fertilizers reduced NH₃ emissions by 6–23% compared to the RD treatment. Either biochar or biochar plus compost reduced N loss via volatilization by 16–23%, while compost alone reduced it by 13%. Likewise, organic and inorganic fertilization also significantly influenced mean and cumulative NH₃ fluxes in T. Aus rice. Mean and cumulative NH₃ fluxes were higher in RD than in other treatments. Reduction in NH₃ fluxes ranged from 10% in rice husk ash to 52% in biochar. Disregarding the control, the highest mean and cumulative NH₃ fluxes were measured in chemical fertilizer treated plots, whereas the lowest emissions were measured in compost plus biochar treated plots. Combined application of organic and inorganic fertilizers reduced NH₃ volatilization by 20–45% compared to the RD application. Pooling the three rice growing seasons together, treatments comprised of biochar or biochar plus compost under IPNS basis reduced N loss via volatilization by 36–37% while biochar alone reduced it by 23% over sole application of full dose of recommended fertilizer as a treatment.

TABLE 3

Table 3. Effects of organic and inorganic fertilizers on mean and cumulative ammonia fluxes in the Boro - T. Aus - T. Aman rice cropping pattern.

3.3. Effects on NH₃ emission factor and yield scaled NH₃ emissions

The NH₃ emission factor (EF) was significantly influenced by the application of organic and inorganic fertilizers. The NH₃ EF ranged from 12% in compost + biochar to 16% in chemical fertilizer-treated plots in Boro rice, from 21% in biochar to 29% in sole chemical fertilizer treated plots in T. Aus rice, and from 22% in biochar to 28% in chemical fertilizer-treated plots in T. Aman rice (Table 4). Yield-scaled NH₃ emissions in Boro rice varied from 0.17 kg t⁻¹ in control to 2.88 kg t⁻¹ in chemical fertilizer treated plots (Table 4). Except for the control treatment, yield scaled NH₃ emissions were similar among treatments in Boro rice. Mixture of biochar and compost reduced the NH₃ EF and yield-scaled NH₃ emission in all rice fields. Similarly, yield-scaled NH₃ emissions in T. Aus rice varied between 1.04 kg t⁻¹ in control and 5.83 kg t⁻¹ in chemical fertilizer treated plots (Table 4). Ignoring the control treatment, the highest yield-scaled NH₃ emissions were noted in chemical fertilizer, which was similar to RMA, and the lowest value was in biochar with or without compost treatment. Yield-scaled NH₃ emissions in T. Aus rice were 1 to 6 times higher than that in Boro rice. Similarly, yield-scaled NH₃ emissions in T. Aman rice ranged from 0.47 kg t⁻¹ in control to 4.43 kg t⁻¹ in chemical fertilizer-treated plots (Table 4). Discounting the control treatment, the highest yield-scaled NH₃ emission was recorded in chemical fertilizer, and the lowest value was in biochar with or without compost. Yield-scaled NH₃ emissions in T. Aman rice were 1.0 to 2.7 times higher than that in Boro rice, and 0.5 to 1.0 times that of T. Aman rice (Table 4).

TABLE 4

Table 4. Effects of organic and inorganic fertilizers on emission factor and yield-scaled ammonia emissions in rice crops.

3.4. Effects on crop yields and system productivity

Organic and inorganic fertilizers influenced the grain yield of Boro, T. Aus, and T. Aman rice (p < 0.05, Table 5), and system productivity of Boro – T. Aus – T. Aman rice cropping pattern (p < 0.01, Table 5). All the treatments were similar to each other in term of crop yield except T₁. Treatments under RD or IPNS had no statistical variation for crop yield and system production. In Boro and T. Aman rice, grain yields were the highest for application of compost and likely the system productivity was the highest for compost application and the lowest for rice husk ash, excluding the control treatment.

TABLE 5

Table 5. Effects of organic and inorganic fertilizers on the grain yield of crops and system productivity in the Boro - T. Aus - T. Aman cropping pattern.

3.5. Effects on soil properties

Organic and inorganic fertilizers had a significant impact on soil organic carbon (SOC) during rice cultivation (p < 0.05, Table 6). Soil organic carbon increased by 6–14% over the control in plots treated with different amendments (Table 6). Biochar and RMA significantly increased soil total nitrogen (TN) content compared to the other treatments including control except in T. Aus season (Table 6). Likewise, organic and inorganic fertilizers significantly influenced soil C:N ratio only in Boro season but not in T. Aus and T. Aman seasons (p < 0.05, Table 6). The highest soil pH was measured in biochar-treated plots, which was similar to other treatments except for compost with biochar and control. Likewise, ${\text{NH}}_4^{+}$ concentrations in soil were significantly influenced by different organic and inorganic fertilizers (p < 0.001, Table 6). The highest ${\text{NH}}_4^{+}$ concentrations were found in plots treated with only chemical fertilizer and were lowest in control.

TABLE 6

Table 6. Effects of organic and inorganic fertilizer on soil properties after urea application in Boro, T. Aus and T. Aman rice.

The relationship between the NH₃ fluxes and soil pH was positive and significant in all rice seasons (Figure 2). NH₃ fluxes had a strong correlation with soil pH in Boro rice (R² = 0.79; p < 0.01). Likewise, NH₃ fluxes had a moderate correlation with soil pH in T. Aus rice (R² = 0.36; p < 0.05) and in T. Aman rice (R² = 0.50; p < 0.05) (Figure 2). Like soil pH, the relationship between NH₃ fluxes and soil ${\text{NH}}_4^{+}$ content was also positive and significant in all rice seasons (Figure 2). Ammonia fluxes had a strong correlation with soil ${\text{NH}}_4^{+}$ content in Boro rice (R² = 0.68; p < 0.01), T. Aus rice (R² = 0.86; p < 0.001), and T. Aman rice (R² = 0.91; p < 0.001) (Figure 2).

FIGURE 2

Figure 2. Relationship between NH₃ fluxes and soil pH (A) or soil ${\text{NH}}_4^{+}$ content (B) in the rice crops; n = 24.

4. Discussion

In accord with our hypothesis, the co-application of biochar, RMA and compost together with N fertilizer, while suppling the same amount of N as N fertilizer alone, decreased NH₃ volatilization loss by 16–28% without changing the soil N status. In the following discussion, we first examine the dynamics of NH₃ fluxes, the NH₃ emission factors for treatments and the IPNS treatment co-benefits for soil properties and crop yield.

4.1. Peak of NH₃ fluxes

The NH₃ flux peak was within 2–3 days after urea application indicating that NH₃ volatilization was a rapid progress that was almost completed within 1 week after each split fertilizer application. The NH₃ volatilization flux patterns were consistent among treatments, suggesting that they were primarily driven by the urea applied. The NH₃ emission patterns were consistent with previous studies in the same (Uddin et al., 2021) and dissimilar geographical areas (Fan et al., 2006) as our experiment. The NH₃ flux from urea hydrolysis usually peaks at 3–7 days after application (Rochette et al., 2009) which is in line with our results but not to Drury et al. (2017) who stated that the peak emissions can take up to 9–15 days if rain occurs after N application. That fluxes were highest from T₂ may be attributed to the highest rate of urea applied which rapidly converted into ${\text{NH}}_4^{+}$ through the ammonification process, which was the first step of ammonia volatilization (Frimpong et al., 2016; Uddin et al., 2021). As NH₃ is in a dynamic equilibrium with ${\text{NH}}_4^{+}$ and H⁺, urea treatment elevates soil pH through urease hydrolysis (Sommer et al., 2004). Following the peak on day 2–4 after urea application, the NH₃ fluxes rapidly declined. While organic amendments did not alter the timing of the peak of NH₃ fluxes, they decreased the magnitude of the peak which could be attributed to the lower rate of chemical N-fertilizer based on the IPNS approach. The decrease in soil ${\text{NH}}_4^{+}$ content and a drop in pH with the organic amendments helps explain the decrease in NH₃ volatilization (Adviento-Borbe et al., 2010). Other processes leading to a decrease in NH₃ volatilization could be the infiltration of mineral N into the crop rooting zone, and increased nitrification over time (Adviento-Borbe et al., 2010). When the NH₃ fluxes for Boro, Aus and Aman seasons were examined in relation to the soil chemical properties, the closest positive correlation was with soil pH followed by soil ${\text{NH}}_4^{+}$ as found in previous studies (Sommer et al., 2004; Rochette et al., 2013).

4.2. Ammonia fluxes, emission factor, and rice yields

While NH₃ volatilization is a major N loss from paddy fields, the rate of N loss is dependent on the fertilization type, time of application, environmental conditions and N application rate (Wang et al., 2016). Pan et al. (2016) stated that about 30% of the applied urea was lost through NH₃ fluxes which were consistent with our result that the N loss via volatilization ranged from 16% in Boro to 28% in T. Aman rice season. When N supplied in the urea fertilizer was adjusted based on the N content in the organic amendments, NH₃ fluxes were reduced. In this study biochar alone and with compost reduced the NH₃ loss during three rice growing seasons. The NH₃ fluxes of N fertilizer was higher for Aman rice than for Aus and Boro rice which is most likely due to the seasonal variations in temperature being the lowest in Boro season (15–25°C) and the highest in T. Aman season (25–35°C) while in T. Aus the temperature was moderate (20–30°C). High temperature in standing water in rice fields induces rapid urea hydrolysis and higher ammonia volatilization (Sun et al., 2017). While the Aus season in the Indo-Gangetic plain has high rainfall and moderate temperature, the urea application rate in this season was lower than the other two seasons due to lower yield potential, which may lower volatilization.

Biochar was very effective in reducing NH₃ emissions by reducing chemical N input but may also control the N releases. Our results also showed consistency with Sun et al. (2017) and Asada et al. (2002), where their meta-analysis suggested that NH₃ fluxes were reduced with the application of biochar pyrolyzed at ~400°C. Ammonia adsorbed onto the biochar surface directly reduces the substrate concentration of NH₃ for the volatilization process (Clough et al., 2013). However, the liming effect of alkaline biochar may increase NH₃ fluxes (Sun et al., 2017; Sha et al., 2019). The pH increase in soil amended with biochar in the present study was not high enough to enhance NH₃ fluxes (Kelly et al., 2015). Among the amended plots biochar required the lowest rate of urea fertilizer to equalize total N input with recommended chemical fertilizer dose, which may explain the lower NH₃ fluxes than in compost amended plots. Co-application of biochar with compost has the potential to reduce NH₃ emissions due to high surface area to adsorb NH₄, high internal porosity to trap ${\text{NH}}_4^{+}$ ions but this will depend on N mineralization rate and their inherent N content which varies among biochar and compost products.

All the treatments, except control without N fertilizer applied, had the same yield in all three rice seasons even though the urea application rates were different. Moreover, the N uptake was also the same in each treatment (data not presented). Therefore, questions arise of how biochar-treated soils provided similar N for plant uptake in comparison to a full dose of urea. A moderate substitution (<40%) of N fertilizer by manure has been reported to significantly increase N use efficiency by 14 and 25% for upland crops and rice, respectively (Xu et al., 2016; Zhang et al., 2020). In the present study, rice plants were initially paler green in biochar-treated plots suggesting that it decreased initial N mineralization rate. In addition, N from urea in biochar-treated plots may have been used more efficiently due to better synchronization of N supply and demand.

Rice husk ash had less efficiency in ${\text{NH}}_4^{+}$ retention in all seasons and in controlling NH₃ fluxes than biochar, but still decreased N losses relative to the urea fertilizer alone. While ashes are often alkaline, the present RMA did not alter soil pH and was effective in decreasing NH₄ content in soil except in Aman season and in decreasing NH₃ losses, except in the Boro season. As an abundant biowaste in the Indo-Gangetic Plain, RMA can be used to reduce N fertilizer input and to reduce atmospheric NH₃ emissions. However, as the ashing conditions are likely to vary with farm-produced RMA, more study is needed to determine the consistency of the effects reported here.

4.3. Integrated plant nutrition system effects on soil properties

In addition to their effects on NH₃ losses, organic amendments had significant effects on some soil properties. In the current research, sole biochar application increased soil pH compared to control treatment, however compost + biochar combination and sole compost application decreased soil pH. Poultry manure biochar may have increased soil pH through its liming effect over the sole compost and chemical fertilizers application but when the mixture of compost and biochar was applied, soil pH decreased relative to the sole biochar application. Herein, soils treated with solitary biochar had the highest pH (7.78) which is not enough to raise NH₃ loss, followed by soils treated with both biochar and compost (7.42). Slight increase in soil pH in biochar treated plots could have increased NH₃ emissions but the lower ${\text{NH}}_4^{+}$ contents in soils resulted in lower NH₃ emissions.

Application of biochar solely or in combination with compost at a rate of 3 t ha⁻¹ has increased SOC in our study, which is in line with previous research (Liu et al., 2021). Biochar is distinguished from compost by its larger proportion of more stable organic carbon molecules (Mahmoud et al., 2018; Eissa, 2019) making it more efficient in enhancing soil physicochemical parameters (Eissa, 2019). Furthermore, Trupiano et al. (2017) also reported that the application of compost and biochar to soils, either alone or in combination, enhanced soil SOC content compared to un-amended soils, implying that biochar and/or compost is a potential source of soil carbon sequestration.

5. Conclusion

Volatilization loss of N from paddy fields in floodplain soils causes economic losses and is a major concern for air and water quality. Application of biochar alone or in combination with compost on an integrated plant nutrition system basis reduced the rate of N-fertilizer application as well as ammonia volatilization. The NH₃ emission factor ranged from 12% in compost plus biochar to 16% in chemical fertilizer-treated plots in Boro rice, from 21% in biochar to 29% in compost treated plots in Aus rice, and from 22% in biochar to 28% in chemical fertilizer-treated plots in Aman rice. Pooling the three rice growing seasons together, either biochar or biochar plus compost mixture reduced N volatilization by 36–37% while compost alone can reduce it by 23%. All the treatments had same crop yield except the control without N fertilizer. Hence, biochar with or without compost mixture has a great potential for mitigating year-round NH₃ volatilization in the triple rice cropping system along with a decrease in the rate of applied N-fertilizer in floodplain soils without losing crop yield and system productivity.

Data availability statement

The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.

Author contributions

MJ and MAH worked on research planning and paper editing. CM worked on research planning, calculation, and paper editing. RB worked on planning and paper editing. MZ contributed in research planning and methodological development. MBH worked on research planning. JF conducted field and laboratory work, data processing, analysis, and paper draft preparation. NM worked in draft preparation. MMJ worked on research planning, data interpretation and paper editing. All authors contributed to the article and approved the submitted version.

Funding

The research was funded by a Krishi Gobeshona Foundation (KGF) project administered by Bangladesh Agriculture Research Council (BARC) in association with the Australian Center for International Agricultural Research (ACIAR: Project LWR 2016/136).

Acknowledgments

We acknowledge the technical support of the Soil and Water Management and Crop Nutrition, Joint FAO/IAEA Division of Nuclear Techniques in Food and Agriculture, Vienna, Austria.

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Publisher's note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

Supplementary material

The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fsufs.2022.1067112/full#supplementary-material

Supplementary data 1. Environmental weather data of the experimental site registered during the experimental period (January 2021 to December 2021).

References

Adviento-Borbe, M. A. A., Kaye, J. P., Bruns, M. V., Mcdaniel, M., McCoy, M., Harkcom, S., et al. (2010). Soil greenhouse gas and ammonia emissions in long-term maize-based cropping systems. Soil Biol. Biochem. 74, 1623–1634. doi: 10.2136/sssaj2009.0446

CrossRef Full Text | Google Scholar

Ali, M., Haruna, A. O., Majid, N. M. A., Primus, W. C., Asap, A., Maikol, N., et al. (2019). Mitigating ammonia volatilization from waterlogged acids soils using organic amendments. Sustain. Agric. Res. 8, 12–22. doi: 10.5539/sar.v8n3p12

CrossRef Full Text | Google Scholar

Asada, T., Ishihara, S., Yamane, T., Toba, A., Yamada, A., Oikawa, K., et al. (2002). Science of bamboo charcoal: study on carbonizing temperature of bamboo charcoal and removal capability of harmful gases. Health Sci. 48, 473–479. doi: 10.1248/jhs.48.473

CrossRef Full Text | Google Scholar

Banik, C., Koziel, J. A., Bonds, D., Singh, A., and Licht, M. (2021). Comparing biochar-swine manure mixture to conventional manure impact on soil nutrient availability and plant uptake - A greenhouse study. Land. 10, 372. doi: 10.3390/land10040372

CrossRef Full Text | Google Scholar

Battaglia, M., Groover, G., and Tomason, W. (2018). Harvesting and Nutrient Replacement Costs Associated With Corn Stover Removal in Virginia. Virginia: Virginia Cooperative Extension Publication CSES-229NP.

Google Scholar

Battaglia, M., Thomason, W., Fike, J. H., Evanylo, G. K., von Cossel, M., Babur, E., et al. (2021). The broad impacts of corn stover and wheat straw removal for biofuel production on crop productivity, soil health and greenhouse gas emissions: a review. GCB Bioen. 13, 45–57. doi: 10.1111/gcbb.12774

CrossRef Full Text | Google Scholar

BBS (2021). Statistical Year Book Bangladesh 2020. Dhaka: Bangladesh Bureau of Statistics (BBS).

Google Scholar

Bouwman, A. F. (1996). Direct emission of nitrous oxide from agricultural soils. Nutr. Cycl. Agroecosyst. 46, 53–70. doi: 10.1007/BF00210224

CrossRef Full Text | Google Scholar

Brolley, M. (2015). Rice security is food security for much of the world. IRRI 7777, 30–32.

Google Scholar

Cantarella, H., Otto, R., Soares, J. R., and de Brito Silva, A. G. (2018). Agronomic efficiency of NBPT as a urease inhibitor: A review. J. Adv. Res. 13, 19–27. doi: 10.1016/j.jare.2018.05.008

PubMed Abstract | CrossRef Full Text | Google Scholar

Chu, L., Hennayake, H. D., and Sun, H. (2019). Biochar effectively reduces ammonia volatilization from nitrogen-applied soils in tea and bamboo plantations. Phyton. 88, 261–267. doi: 10.32604/phyton.2019.07791

CrossRef Full Text | Google Scholar

Clough, T. J., Condron, L. M., Kammann, C., and Müller, C. (2013). A review of biochar and soil nitrogen dynamics. Agron. 3, 275–293. doi: 10.3390/agronomy3020275

PubMed Abstract | CrossRef Full Text | Google Scholar

Diatta, A. A., Fike, J. H., Battaglia, M. L., Galbraith, J. M., and Baig, M. B. (2020). Efects of biochar on soil fertility and crop productivity in arid regions: a review. Arab. J. Geosci. 13, 595. doi: 10.1007/s12517-020-05586-2

CrossRef Full Text | Google Scholar

Drury, C. F., Yang, X., Reynolds, W. D., Calder, W., Oloya, T. O., Woodley, A. L., et al. (2017). Combining urease and nitrification inhibitors with incorporation reduces ammonia and nitrous oxide emissions and increases corn yields. J. Environ. Qual. 46, 939–949. doi: 10.2134/jeq2017.03.0106

PubMed Abstract | CrossRef Full Text | Google Scholar

Eissa, M. A. (2019). Effect of compost and biochar on heavy metals phyto stabilization by the halophytic plant old man saltbush [Atriplex nummularia Lindl]. Soil Sed. Contam. Int. J. 28, 135–147. doi: 10.1080/15320383.2018.1551325

CrossRef Full Text | Google Scholar

Fan, X. H., Song, Y. S., Lin, D. X., Yang, L. Z., and Luo, J. F. (2006). Ammonia volatilization losses and 15N balance from urea applied to rice on a paddy soil. J. Environ. Sci. 18, 299–303.

PubMed Abstract | Google Scholar

FAO/UNDP (1988). Land Resources Appraisal of Bangladesh for Agricultural Development, Vol 2, Agroecological Regions of Bangladesh. FAO: Rome, 1–570.

Google Scholar

Fawcett, J. K. (1954). The semi-micro Kjeldahl method for the determination of nitrogen. J. Med. Lab. Technol. 12, 1–22.

PubMed Abstract | Google Scholar

Feng, Y., Sun, H., Xue, L., Liu, Y., Gao, Q., Lu, K., et al. (2017). Biochar applied at an appropriate rate can avoid increasing NH3 volatilization dramatically in rice paddy soil. Chemosphere. 168, 1277–1284. doi: 10.1016/j.chemosphere.2016.11.151

PubMed Abstract | CrossRef Full Text | Google Scholar

FRG (2018). Fertilizer Recommendation Guide-2018. Farmgate: Bangladesh Agricultural research Council (BARC).

Google Scholar

Frimpong, K. A., Amoakwah, E., Osei, B. A., and Arthur, E. (2016). Changes in soil chemical properties and lettuce yield response following incorporation of biochar and cow dung to highly weathered acidic soils. J. Org. Agric. Environ. 4, 28–39. Available online at: http://hdl.handle.net/123456789/2138

Google Scholar

He, T., Yuan, J., Luo, J., Lindsey, S., Xiang, J., Lin, Y., et al. (2018). Effects of application of inhibitors and biochar to fertilizer on gaseous nitrogen emissions from an intensively managed wheat field. Sci. Total Environ. 629, 121–130. doi: 10.1016/j.scitotenv.2018.02.048

PubMed Abstract | CrossRef Full Text | Google Scholar

IQAir. (2021). Air Quality in Delhi. Staad: IQAir. Available online at: https://www.iqair.com/india/delhi

Google Scholar

Jahangir, M. M. R., Rahman, S., Mumu, N. J., Biswas, C., Jahiruddin, M., Mueller, C., et al. (2022). Crop residue interactions with fertilizer rate enhances volatilization loss and reduces nitrogen use efficiency in irrigated maize and potato. Arch. Agron. Soil Sci. 1, 1–13. doi: 10.3389/fenvs.2022.853655

CrossRef Full Text | Google Scholar

Keeney, D. R., and Nelson, D. W. (1982). “Nitrogen-inorganic forms,” in Methods of Soil Analysis, Part 2. Chemical and Microbiological Propertie, eds. AL Page, RH Miller, DR Keeney (Madison, WI: Soil Science Society of America), 643–698.

Google Scholar

Kelly, C. N., Calderon, F. C., Acosta-martinex, V., Mikha, M. M., Benjamin, J., Rutherford, D. W., et al. (2015). Switchgrass biochar effects on plant biomass and microbial dynamics in two soils from different regions. Pedosphere. 25, 329–342. doi: 10.1016/S1002-0160(15)30001-1

CrossRef Full Text | Google Scholar

Kuttippurath, J., Singh, A., Dash, S. P., Mallick, N., Clerbaux, C., Van Damme, M., et al. (2020). Record high levels of atmospheric ammonia over India: spatial and temporal analyses. Sci. Total Environ. 740, 139986. doi: 10.1016/j.scitotenv.2020.139986

PubMed Abstract | CrossRef Full Text | Google Scholar

Lehmann, J., and Joseph, S. (2009). “Biochar for environmental management: An introduction,” in Biochar for Environmental Management, Science and Technology, eds J. Lehmann, S. Joseph (London: Earthscan), 1–12.

Google Scholar

Linquist, B. A., Anders, M. M., Adviento-Borbe, M. A., Chaney, R. L., Nalley, L. L., Rosa, D. A., et al. (2015). Reducing greenhouse gas emissions, water use, and grain arsenic levels in rice systems. Glob. Change Biol. 21, 407–417. doi: 10.1111/gcb.12701

PubMed Abstract | CrossRef Full Text | Google Scholar

Liu, D., Ding, Z., Ali, E. F., Kheir, A. M. S., Eissa, M. A., Ibrahim, O. H. M., et al. (2021). Biochar and compost enhance soil quality and growth of roselle (Hibiscus sabdariffa L.) under saline conditions. Sci. Rep. 11, 1–11. doi: 10.1038/s41598-021-88293-6

PubMed Abstract | CrossRef Full Text | Google Scholar

Mahmoud, E., Ibrahim, M., Ali, N., and Ali, H. (2018). Spectroscopic analyses to study the effect of biochar and compost on dry mass of canola and heavy metal immobilization in soil. Commun. Soil Sci. Plant Anal. 49, 1990–2001. doi: 10.1080/00103624.2018.1492601

CrossRef Full Text | Google Scholar

Malińska, K., Zabochnicka, M., and Dach, J. (2014). Effects of biochar amendment on ammonia during composting of sewage sludge. Ecol. Eng. 71, 478. doi: 10.1016/j.ecoleng.2014.07.012

PubMed Abstract | CrossRef Full Text | Google Scholar

Martins, M. R., Sarkis, L. F., Guareschi, R. F., Santos, C. A., Sant'anna, S. A., Zaman, M., et al. (2021a). A simple and easy method to measure ammonia volatilization: accuracy under field conditions. Pedosphere 31, 225–264. doi: 10.1016/S1002-0160(20)60077-7

CrossRef Full Text | Google Scholar

Martins, M. R., Sarkis, L. F., Sant'Anna, S. A. C., Santos, C. A., Araujo, K. E., Santos, R. C., et al. (2021b). Optimizing the use of open chambers to measure ammonia volatilization in field plots amended with urea. Pedosphere 31, 243–254. doi: 10.1016/S1002-0160(20)60078-9

CrossRef Full Text | Google Scholar

Mazzetto, A. M., Styles, D., Gibbons, J., Arndt, C., Misselbrook, T., Chadwick, D., et al. (2020). Region-specific emission factors for Brazil increase the estimate of nitrous oxide emissions from nitrogen fertiliser application by 21%. Atmos Environ. 230, 117506. doi: 10.1016/j.atmosenv.2020.117506

CrossRef Full Text | Google Scholar

Mosier, A., Kroeze, C., Nevison, C., Oenema, O., Seitzinger, S., Cleemput, O., et al. (1998). Closing the global N₂O budget: nitrous oxide emissions through the agricultural nitrogen cycle inventory methodology. Nutrient Cycl. Agroecosyst. 52, 225–248. doi: 10.1023/A:1009740530221

CrossRef Full Text | Google Scholar

Nichols, K. L., Del Grosso, S. J., Derner, J. D., Follett, R. F., Archibeque, S. L., Delgado, J. A., et al. (2018). Nitrous oxide and ammonia emissions from cattle excreta on shortgrass steppe. J. Environ. Qual. 47, 419–426. doi: 10.2134/jeq2017.12.0463

PubMed Abstract | CrossRef Full Text | Google Scholar

Pan, B., Lam, S. K., Mosier, A., Luo, Y., and Chen, D. (2016). Ammonia volatilization from synthetic fertilizers and its mitigation strategies: a global synthesis. Agric Ecosyst. Environ. 232, 283–289. doi: 10.1016/j.agee.2016.08.019

CrossRef Full Text | Google Scholar

Rahaman, M. A., Zhan, X., Zhang, Q., Li, S., Long, Y., Zeng, H., et al. (2020). Ammonia volatilization reduced by combined application of biogas slurry and chemical fertilizer in maize–wheat rotation system in North China Plain. Sustainability. 12, 4400. doi: 10.3390/su12114400

CrossRef Full Text | Google Scholar

Rochette, P., Angers, D. A., Chantigny, M. H., Gasser, M. O., MacDonald, J. D., and Pelster, D. E. (2013), NH3. volatilization, soil NH4+ concentration soil pH following subsurface banding of urea at increasing rates. Can. J. Soil Sci. 93, 261–268. doi: 10.4141/cjss2012-095.

CrossRef Full Text | Google Scholar

Rochette, P., Angers, D. A., Chantigny, M. H., MacDonald, J. D., Bissonnette, N., Bertrand, N., et al. (2009). Ammonia volatilization following surface application of urea to tilled and no-till soils: a laboratory comparison. Soil Till. Res. 103, 310–315. doi: 10.1016/j.still.2008.10.028

CrossRef Full Text | Google Scholar

Saarnio, S., Heimonen, K., and Kettunen, R. (2013). Biochar addition indirectly affects N₂O emissions via soil moisture and plant N uptake. Soil Biol. Biochem. 58, 99–106. doi: 10.1016/j.soilbio.2012.10.035

CrossRef Full Text | Google Scholar

Sha, Z., Li, Q., Lv, T., Misselbrook, T., and Liu, X. (2019). Response of ammonia volatilization to biochar addition: A meta-analysis. Sci. Total Environ. 655, 1387–1396. doi: 10.1016/j.scitotenv.2018.11.316

PubMed Abstract | CrossRef Full Text | Google Scholar

Sommer, S. G., Schjoerring, J. K., and Denmead, O. T. (2004). Ammonia emission from mineral fertilizers and fertilized crops. Adv. Agron. 82, 557–622. doi: 10.1016/S0065-2113(03)82008-4

CrossRef Full Text | Google Scholar

Stokstad, E. (2014). Ammonia pollution from farming may exact hefty health costs. Science. 343, 238. doi: 10.1126/science.343.6168.238

PubMed Abstract | CrossRef Full Text | Google Scholar

Sun, H., Lu, H., Chu, L., Shao, H., and Shi, W. (2017). Biochar applied with appropriate rates can reduce N leaching, keep N retention and not increase NH₃ volatilization in a coastal saline soil. Sci. Total Environ. 575, 820–825. doi: 10.1016/j.scitotenv.2016.09.137

PubMed Abstract | CrossRef Full Text | Google Scholar

Trupiano, D., Cocozza, C., Baronti, S., Amendola, C., Vaccari, F. P., Lustrato, G., et al. (2017). The effects of biochar and its combination with compost on lettuce (Lactuca sativa L.) growth, soil properties, and soil microbial activity and abundance. Hindawi Int. J. Agron. 12, 3158207. doi: 10.1155/2017/3158207

CrossRef Full Text | Google Scholar

Uddin, S., Nitu, T. T., Milu, U. M., Nasreen, S. S., Hossenuzzaman, M., Haque, M. E., et al. (2021). Ammonia fluxes and emission factors under an intensively managed wetland rice ecosystem. Environ. Sci. Proc Impacts. 23, 132–143. doi: 10.1039/D0EM00374C

PubMed Abstract | CrossRef Full Text | Google Scholar

Walkley, A., and Black, I. A. (1934). An examination of Degtjareff method for determining soil organic matter and a proposed modification of the chromic acid titration method. Soil Sci. 37, 29–37. doi: 10.1097/00010694-193401000-00003

CrossRef Full Text | Google Scholar

Wang, C., Sun, H., Zhang, J., Zhang, X., Lu, L., Shi, L., et al. (2021). Effects of different fertilization methods on ammonia volatilization from rice paddies. J. Cleaner Prod. 295, 126299. doi: 10.1016/j.jclepro.2021.126299

CrossRef Full Text | Google Scholar

Wang, H., Zhang, Y., Han, Q., Xu, Y., Hu, G., Xing, H., et al. (2016). The inflammatory injury of heart caused by ammonia is realized by oxidative stress and abnormal energy metabolism activating inflammatory pathway. Sci Total Environ. 742, 140532. doi: 10.1016/j.scitotenv.2020.140532

PubMed Abstract | CrossRef Full Text | Google Scholar

Wolfe, A. H., and Patz, J. A. (2002). Reactive Nitrogen and human health: acute and long-term implications. Ambio. 31, 120–125. doi: 10.1579/0044-7447-31.2.120

PubMed Abstract | CrossRef Full Text | Google Scholar

Xia, L., Ti, C., Li, B., Xia, Y., and Yan, X. (2016). Greenhouse gas emissions and reactive nitrogen releases during the lifecycles of staple food production in China and their mitigation potential. Sci. Total Environ. 556, 116–125. doi: 10.1016/j.scitotenv.2016.02.204

PubMed Abstract | CrossRef Full Text | Google Scholar

Xia, Y., and Yan, X. (2012). Ecologically optimal nitrogen application rates for rice cropping in the Taihu Lake region of China. Sustain. Sci. 7, 33–44. doi: 10.1007/s11625-011-0144-2

CrossRef Full Text | Google Scholar

Xu, L., and Penner, J. E. (2012). Global simulations of nitrate and ammonium aerosols and their radiative effects. Atmos. Chem. Phys. 12, 9479–9504. doi: 10.5194/acp-12-9479-2012

CrossRef Full Text | Google Scholar

Xu, N., Tan, G., Wang, H., and Gai, X. (2016). Effect of biochar additions to soil on nitrogen leaching, microbial biomass and bacterial community structure. Soil Biol. 74, 1–8. doi: 10.1016/j.ejsobi.2016.02.004

CrossRef Full Text | Google Scholar

Xu, R. T., Tian, H., Pan, S., Prior, S. A., Feng, Y., Batchelor, W. D., et al. (2019). Global ammonia emissions from synthetic nitrogen fertilizer applications in agricultural systems: Empirical and process-based estimates and uncertainty. Global Change Biol. 25, 314–326. doi: 10.1111/gcb.14499

PubMed Abstract | CrossRef Full Text | Google Scholar

Zaman, M., Kleineidam, K., Bakken, L., Berendt, J., Bracken, C., Butterbach-Bahl, K., et al. (2021). “Methodology for measuring greenhouse gas emissions from agricultural soils using non-isotopic techniques,” in Measuring Emission of Agricultural Greenhouse Gases and Developing Mitigation Options Using Nuclear and Related Techniques, eds M Zaman, L Heng, C Müller (Cham: Springer), 82–89.

Google Scholar

Zhang, X., Fang, Q., Zhang, T., Ma, W., Velthof, G. L., Hou, Y., et al. (2020). Benefits and trade-offs of replacing synthetic fertilizers by animal manures in crop production in China: a meta-analysis. Global Change Biol. 26, 888–900. doi: 10.1111/gcb.14826

PubMed Abstract | CrossRef Full Text | Google Scholar

Zhao, Z. Q., Bai, Z. H., Winiwarter, W., Kiesewetter, G., Heyes, C., Ma, L., et al. (2017). Mitigating ammonia emission from agriculture reduces PM_2.5 pollution in the Hai River Basin in China. Sci. Total Environ. 609, 1152–1160. doi: 10.1016/j.scitotenv.2017.07.240

PubMed Abstract | CrossRef Full Text | Google Scholar

Zheng, X., Fu, C., Xu, X., Yan, X., Huang, Y., Han, S., et al. (2002). The asian nitrogen cycle case study. J. Hum. Environ. 31, 79–87. doi: 10.1579/0044-7447-31.2.79

PubMed Abstract | CrossRef Full Text | Google Scholar