Next Article in Journal
Soil and Plant Nitrogen Management Indices Related to Within-Field Spatial Variability
Previous Article in Journal
Balancing Yield and Environmental Impact: Nitrogen Management and Planting Density for Rice in Southwest China
Previous Article in Special Issue
Straw Returning Proves Advantageous for Regulating Water and Salt Levels, Facilitating Nutrient Accumulation, and Promoting Crop Growth in Coastal Saline Soils
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Agronomy
Volume 14
Issue 8
10.3390/agronomy14081844
agronomy-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Influence of Biogas Slurry and a Nitrification Inhibitor Application in Nitrous Oxide Emissions by Soil

by
Jilin Lei
1,
Yingying Sun
1,
Junhui Yin
1,2,
Rui Liu
1,* and
Qing Chen
1
1
Beijing Key Laboratory of Farmyard Soil Pollution Prevention-Control and Remediation, College of Resources and Environmental Sciences, China Agricultural University, Beijing 100193, China
2
School of Agriculture, Sun Yat-sen University, Shenzhen 518107, China
*
Author to whom correspondence should be addressed.
Agronomy 2024, 14(8), 1844; https://doi.org/10.3390/agronomy14081844 (registering DOI)
Submission received: 22 July 2024 / Revised: 18 August 2024 / Accepted: 19 August 2024 / Published: 20 August 2024
(This article belongs to the Special Issue Nutrient Cycling and Environmental Effects on Farmland Ecosystems)
Browse Figures
Review Reports Versions Notes

Abstract

:
As global efforts to combat climate change intensify, agricultural emissions are increasingly scrutinized. Biogas slurry (BS), a by-product of agricultural waste, not only provides essential nutrients for crops but can also elevate soil nitrous oxide (N2O) emissions. This study investigates the immediate and long-term impacts of BS application on N2O emissions, taking into account the frequency of application and evaluating the effectiveness of nitrification inhibitor 3,4-dimethylpyrazole-phosphate (DMPP) in reducing emissions. Through a microcosm incubation experiment with a 108 h robotized incubation-monitoring system, it was found that N2O emissions spiked immediately following a single BS application, with emissions decreasing within 30 days. Repeated BS applications yielded lower cumulative emissions. Elevated N2O emissions were linked to higher soil pH and ammonium (NH4+) levels, along with reduced nitrate (NO3−) concentrations after a single BS application. The combined application of BS and DMPP proved most effective in inhibiting nitrification and cumulative N2O emissions, achieving reductions of 63.0% and 94.6%, respectively. High soil pH, NH4+, and low NO3− were identified as pivotal factors in this effect. These findings highlight the need for mitigation strategies such as dilution or splitting applications to reduce emissions. Integrating BS with DMPP offers a sustainable approach to achieving both agricultural and environmental goals.

1. Introduction

Biogas slurry (BS), as a by-product of anaerobic digestion of livestock manures for biogas production, is produced in staggering quantities, reaching billions of tons globally [1,2]. Rich in macro- and micronutrients, BS is commonly used as a substitute for manufactured fertilizers in agriculture soils [3,4]. The use of BS as an organic fertilizer not only decreases disposal costs but also enhances crop yields when integrated into a nutrient management plan [5]. Proper management of BS applications would improve waste resource utilization and stimulate agricultural sustainability.
The utilization of BS in soil, while potentially beneficial, also introduces ammonium (NH4+), dissolved organic carbon (DOC), and organic compounds [6]. These additions can significantly alter the physicochemical properties of the soil and subsequently impact nitrogen (N) transformation and greenhouse gas emissions, particularly nitrous oxide (N2O) [7,8]. The chosen method and rate of BS application are key questions, when considering mitigation of potential negative environmental outcomes [9]. On the one hand, a single BS application would result in a temporary increase in soil fertility due to a sudden influx of nutrients and organic matter into the soil. However, excessive nutrient application beyond crop requirements could disturb the balance of soil microorganisms and affect soil N cycling-related processes [9,10]. On the other hand, multiple applications of BS may lead to a different microbial response because of N accumulation in the soil after BS replenishment over time [11,12]. Therefore, the difference between single and multiple applications could be represented in the cumulative effects on soil properties over time [13,14]. However, whether these variations in soil physicochemical properties affect N2O emissions remains unclear. Unraveling the potential differences in N2O emissions arising from the different application practices of BS is crucial for improving agricultural sustainability and mitigating greenhouse gas emissions.
3,4-dimethylpyrazole phosphate (DMPP) is a nitrification inhibitor (NI), which can effectively reduce soil N2O production through slowing down the conversion of NH4+ to NO3− [15,16]. Several studies have demonstrated that DMPP has an inhibitory effect on BS-induced N2O emissions, but the efficacy varied with soil conditions, for example, the inorganic N and organic C contents [17]. Martin et al. [18] and Guo et al. [19] have emphatically highlighted the remarkable capacity of DMPP to significantly diminish the release of N2O from soil subsequent to slurry injection. However, Van Nguyen et al. [20] found that the effect of DMPP on BS-induced N2O emissions was non-significant. Previous studies have demonstrated that the inhibitory effects of DMPP on nitrification and N2O emissions are dependent on various soil properties, such as soil pH and NH4+ content [21,22]. Combined application of DMPP and BS would possibly be proper BS management for sustainable agriculture and environmental management. However, different BS application frequencies would contribute to variations in soil physicochemical properties and also influence DMPP efficacy [23]. It is essential to explore the optimal practices for DMPP addition in relation to different BS application frequencies.
Therefore, the current study aims to: (1) explore the immediate and long-term impacts of BS application on N2O emissions and the influence of application frequency; (2) identify the key soil variables correlated significantly to the N2O emissions with BS application; and (3) determine the optimal practice of the DMPP concerning BS application frequency. Based on the above information, it was hypothesized that a single application of BS would initially lead to higher N2O emissions from the soil compared to multiple BS applications. We anticipated that this initial emission spike could be attributed to changes in soil properties resulting from the single application, such as increased soil pH and NH4+ content, along with decreased NO3− levels. Additionally, the simultaneous application of BS with DMPP would exert the best inhibitory efficacy in N2O emissions.

2. Materials and Methods

2.1. Experimental Soil and Biogas Slurry

Soil samples (0–20 cm) were collected from a greenhouse vegetable field (37°54′53″ N, 121°31′55″ E) located in Shouguang, Shandong province, China. The soil was a fluvo-aquic (IUSS Working Group WRB, 2015) with the following soil chemical characteristics: pH, 7.86; total organic carbon (TOC), 7.01 g·kg−1; total nitrogen (TN), 0.517 g·kg−1; Olsen P, 25.9 mg·kg−1; available potassium (K), 88.9 mg·kg−1, and water holding capacity (WHC), 28.6%. The sampled soil was homogenized through a 2 mm mesh and air dried for the incubation experiments.
The BS, chicken manure as raw material fermented for 20 days, was collected from a biogas plant with an up-flow solid reactor (USR) located in Penglai City, Shandong Province, China (Shandong Minhe Biological Technology Co., Ltd., Penglai, Shandong, China). Details of the basic chemical properties of the tested BS are shown in Table 1. The nitrification inhibitor DMPP (3,4-dimethylpyrazole phosphate, Lianyungang YC International Trade Co., Ltd., Lianyungang, Jiangsu, China) was dissolved in deionized water before use.

2.2. Experimental Design

2.2.1. Soil Incubation

For this, 500 g (dry weight) of soil were placed into 1 L cylindrical incubation containers with a height of 13 cm and a diameter of 11.5 cm. Two main treatments were applied: (i) study control (CK), deionized water addition alone, and (ii) BS addition (B). All assays were performed in triplicate. For treatment (iii), the BS was homogeneously applied at a rate of 125 mL kg−1 (714 mg N kg−1) to the soil, which is equivalent to a rate of 300 m3 ha−1, according to the actual local application rate of BS as fertilizer. Throughout the incubation period, soil moisture content was consistently maintained at 70% of WHC in all treatments by the addition of deionized water, which was replenished every 2 to 3 days according to the weight loss of the samples. The containers were covered with perforated parafilm and then incubated in darkness in an artificial climate chamber with a constant temperature of 25 °C and a constant humidity of 70% for 60 days. Moreover, 100 g of soil in each container were destructively sampled on days 0, 30, and 60, and the sampling time is set as a sub-treatment, which are referred to as treatments CK0, CK1, CK2, B0, B1, and B2. Among these, the B0 and B1 treatments were designed to examine the immediate and long-term effects of single BS application, and the B2 treatment represents a repeated application of BS after the initial 30-day incubation period, allowing for the assessment of the cumulative impact on N2O emissions after an additional 30 days. Furthermore, 30 g of each soil sample were used to measure gas emissions, while the remaining soil was analyzed to determine the pH, DOC content, and mineral N contents (NH4+ and NO3−).

2.2.2. Gas Kinetics Analysis

A 108 h robotized incubation-monitoring (Robot) system was conducted to observe the characteristics of soil N2O, nitrogen (N2), oxygen (O2), and CO2 emissions. There are three main treatments: control; BS; BS + nitrification inhibitor DMPP, and then the sampling time is set as a sub-treatment. This investigation employed 30 g of soil after 0-, 30-, and 60-day treatments, as outlined in Section 2.2.1 of the experiment. To specifically assess the efficacy of DMPP addition, an additional 30 g of soil from treatments B0, B1, and B2 underwent parallel monitoring of gas emissions. The incubation was established in 120 mL serum bottles, featuring nine specific treatments: CK0, CK1, CK2, B0, B0 + DMPP, B1, B1 + DMPP, B2, and B2 + DMPP, with each treatment replicated three times. A schematic representation of the experimental design in this study is shown in Figure 1. Prior to incubation, for treatments involving DMPP addition, the DMPP solution was evenly dripped onto the surface of the soil at a rate of 1% of N contained in BS (i.e., the commercially recommended rate). The volume of DMPP solution and deionized water addition was determined to adjust the soil water content of all treatments to 70% WHC. Once prepared, all bottles were immediately sealed with a rubber plug and an aluminum cap (Macherey-Nagel, Düren, Germany). The background gas was removed from the bottles using a 21% O2 (v/v)-containing helium–oxygen mixture (Beijing Shuaien Technology Co., Ltd., Beijing, China) through 5 vacuum-replenishing cycles. A non-piston syringe filled with distilled water was inserted to modify the pressure in the headspace to atmospheric pressure after 3 min of overpressure in the bottle [24].
All serum bottles were transferred to the robot system to monitor the gas dynamics. Detailed information about the system and the principle of gas measurement was provided in the Supplementary Material, referring to Molstad et al. [25] and McMillan et al. [26]. In the present study, the denitrification product ratio N2O/(N2O + N2) was also calculated.

2.3. Soil Properties Analysis

In the Section 2.2.1 incubation experiment, the soil designated for mineral N content analysis was extracted using 1 M KCl solution at a ratio of 1:5 (w/v, soil/KCl). The contents of NH4+-N and NO3−-N in the extracts were determined using a continuous flow analyzer (AA3, Seal Analytical, Norderstedt, Germany). Similarly, a 0.5 M K2SO4 solution was used to extract the soil at a ratio of 1:5 (w/v, soil/K2SO4 solution) immediately after incubation, and concentrations of DOC in the extracts were measured by a TOC/TN analyzer (TOC-VCSH, Shimadzu, Kyoto, Japan). Soil pH was measured using a pH meter (MP522 version 3, SANXIN, Shenyang, China). Upon completion of the gas kinetics analysis phase (Section 2.2.2), soil samples from each treatment in the serum bottles were immediately extracted for NO3− content analysis. The nitrification inhibition rate was calculated to investigate the efficacy of DMPP in suppressing nitrification and NO3− accumulation, drawing on previous studies such as Li et al. [27] and Zhang et al. [28], according to Equation (1) [29] as follows:
Nitrification inhibition rate = (A − B)/A × 100%
where A is the difference in NO3−-N content before and after soil incubation without DMPP addition (mg kg−1), and B is the difference in NO3−-N content before and after soil incubation with DMPP addition (mg kg−1).

2.4. Statistical Analysis

All statistical data were conducted using Excel 2016 and one-way analysis of variance (ANOVA) by IBS SPSS Statistics 20. The significance of the results across the treatments was estimated using the least significant difference (LSD) test at p < 0.05 level. All figures were drawn using Origin 2021 Software.

3. Results

3.1. Effect of BS Application Frequency on Soil pH, Dissolved Organic Carbon, and Mineral Nitrogen

The soil pH varied remarkably with different BS application frequencies (Figure 2A). Specifically, the soil pH of the B1 and B2 treatments was significantly lower than that of the B0 treatment (p < 0.05). The contents of DOC in different treatments are shown in Figure 2B. In general, the application of BS significantly increased soil DOC contents and presented remarkably different effects under different application frequencies. The content of DOC was 108 mg kg−1 in the B0 treatment, decreasing to 62.9 mg kg−1 in treatment B1. After the repeated application of BS, the DOC content in the B2 treatment increased to 104 mg kg−1 and showed no significant difference in comparison with B0.
The contents of NH4+ and NO3− in different treatments are shown in Figure 2C,D. The highest NH4+ content occurred in the B0 treatment amongst all treatments, while relatively lower NO3− content appeared compare to thatin the B1 and B2 treatments. The content of NH4+ in the B1 and B2 treatments showed insignificant change compared with that of their corresponding CK series (CK1 and CK2), while the NO3− content in these two treatments was notably higher than that in CK1 and CK2 (Figure 2C,D).

3.2. Emission Characteristics of N2O and N2

Figure 3 shows the measured N2O and N2 concentrations in different treatments during the 108 h robotized incubation and monitoring period. After BS addition, especially in the B0 treatment, soil N2O emissions increased considerably compared with the treatments without BS addition (Figure 3A,C). Among all treatments, B0 had the highest cumulative N2O emissions up to 2.59 nmol N g−1, while the cumulative N2O emissions of CK1 and CK2 were the lowest (Table 2). The cumulative N2O emissions in the B0-DMPP and B1-DMPP treatments were significantly lower than those in B0 and B1 (p < 0.05), while the N2O emission characteristic showed no remarkable difference between B2 and B2-DMPP.
The trend of N2 emissions over the incubation period was similar for all treatments (Figure 3). Notably, DMPP addition brought a great increase to N2 emissions in B0 + DMPP treatment (Figure 3A,B). The cumulative N2 emissions of the B0 and B2-DMPP treatments were the lowest, at 55.4 and 43.3 nmol N g−1, respectively, while there was no significant difference amongst the other treatments (Table 2). Table 2 shows the denitrification product ratio N2O/(N2O+N2) in different treatments, and the ratio was much higher in the treatments with BS addition than in others. The highest denitrification product ratio occurred in B0, which went up to 38.3 × 10−3 and decreased strongly following DMPP addition.

3.3. Cumulative CO2 Emissions and O2 Consumption

The CO2 emissions of the CK0, CK1, and CK2 treatments were stable and relatively lower than those of treatments with BS additions, which all showed an upward trend (Figure 4). The CO2 emission of the B0 treatment kept rising over time and was significantly higher than that of other treatments after 78 h, while it decreased after DMPP addition (Figure 4A). The O2 concentration decreased over time, and the highest O2 consumption occurred in the B0 and B2-DMPP treatments (Figure 4A).

3.4. Nitrification Inhibition and Cumulative N2O Emissions Inhibition Rate

Figure 5 illustrates the nitrification inhibition and cumulative N2O emission inhibition efficacy of DMPP under different BS application frequencies. The highest inhibition rate occurred in the B0-DMPP treatment. There was no obvious difference between the B1-DMPP and B2-DMPP treatments in the nitrification inhibition rate.

3.5. The Relationship between Gas Emission Characteristics, DMPP Efficacy, and Soil Variables

The correlation between soil variables and the gas emission characteristics of BS amended soils under different application frequencies is shown in Figure 6A. Soil NH4+ and pH were strong positive predictors of cumulative N2O emissions, CO2 emissions, N2O/(N2O + N2), and O2 consumption (p < 0.05). While these gas emissions were negatively correlated with soil NO3− content (p < 0.01). The emission characteristics of N2 and CO2 were significantly associated with soil DOC content (p < 0.05; Figure 6A), where N2 emissions exhibited a negative correlation with DOC content, while CO2 emissions showed a positive correlation with DOC content.
The varying soil properties, as influenced by different BS application frequencies, had a notable impact on the effectiveness of DMPP (Figure 6B). The inhibitory efficacy of DMPP in nitrification and cumulative N2O emissions was significantly and positively related to soil pH (p < 0.05; Figure 6B). Both soil NH4+ and NO3− contents influenced DMPP efficacy, which was demonstrated by a significant positive correlation between NH4+ and nitrification inhibition rate and an inverse correlation between NO3− and nitrification inhibition rate (p < 0.05; Figure 6B). The present trial also illustrates a positive relationship between the N2O inhibition rate and the nitrification inhibition rate after the DMPP addition (p < 0.05, Figure 6B).

4. Discussion

4.1. Regulation of Gas Emission Characteristics by Frequency of BS Application and Influencing Soil Factors

As can be seen from these study results, different application frequencies of BS exerted varying effects on soil N2O emissions. It was observed that a single application of BS led to the highest levels of short-term N2O emissions. Repeated applications of BS resulted in the lowest overall N2O emissions over the study period. Many previous studies have shown that N2O emissions reached higher levels after initial BS fertilization in comparison to subsequent applications; this was mostly attributed to the substantial influx of nutrients and instant changes in physicochemical soil properties upon BS incorporation [9,30]. Furthermore, while the single application of BS leads to an immediate spike in N2O emissions, the intensity of N2O emissions decreases as the duration of the application increases. A similar result was found in a study conducted by [20]. After applying cattle slurry, an early peak of N2O emission occurred in slurry-treated soils on day 1, which was attributed to denitrification of soil NO3−. A temporary surge in N2O emissions at the beginning of BS application could alternatively be due to the priming effect, the stimulation of soil mineralization, nitrification, and denitrification, and changes of the soil conditions such as mineral nitrogen contents and DOC sources [7,31]. Other studies demonstrated that inconsistent N2O emissions from different BS application frequencies largely depend on soil properties [9,32].
Soil NH4+ content correlated positively with cumulative N2O emissions (Figure 6A), which indicated that soil NH4+ would be a dominant substrate for N2O emissions. Well et al. [33] also concluded that N2O emissions were governed by NH4+ availability, which stimulates nitrification and denitrification processes. In the present study, the highest N2O emissions would potentially attribute to the elevated soil NH4+ content after the initial BS application. It possibly contributed to the abundant NH4+ in BS or soil NH4+ release due to stimulated mineralization of soil organic nitrogen by BS application [34], and nitrification would be the main source of N2O emissions induced by the single BS application. The negative relationship between NO3− content and N2O emissions also supports this. Shi et al. [10] similarly reported that N2O emissions from soils with BS addition were attributed to nitrification. Following a 30-day interval of BS application, nitrification had consistently occurred, NH4+ was consumed, and NO3− was produced. Consequently, over the time of monitoring gaseous emissions, N2O emissions decreased significantly. Soil pH emerged as another dominant factor positively related to N2O emissions under different BS application frequencies (p < 0.05; Figure 6A). Soil pH was shown to be amplified with the simple application of BS (Figure 2A). The higher N2O emission intensity in the B0 treatment would also be attributed to higher soil pH, which can influence microbial activity by creating a more favorable environment for certain microbial groups involved in nitrification and is generally more conducive to related N2O emissions [5]. The decreased pH in the B1 and B2 treatments could be explained by the rich, weakly acidic functional groups such as polysaccharides and humic acid in BS [35]. The accumulation of such functional groups could not only reduce soil pH but also improve the buffering performance against changes in pH [36,37]. The depletion of NH4+ due to its conversion to NO3− after long-term BS application could also reduce soil pH [38]. These factors all contribute to relatively low N2O emissions in the B1 and B2 treatments.
Critically, N2O can be further reduced to N2 via the microbial-mediated process of denitrification [16]. This study also included the simultaneous quantification of N2O and N2 to assess the effects of BS application. The current findings reveal a positive correlation between the denitrification product ratio N2O/(N2 + N2O) in the soil and the concentrations of NH4+ and pH (Figure 6A). This is in line with the conclusions drawn by Zhang et al. [39] and Shi et al. [10]. This accumulation of evidence suggests that the single application of BS likely bears the risk of strongly promoting denitrifying conditions and N losses. The application of BS supplies readily decomposable organic carbon, fostering microbial growth [40], especially fungi, that preferentially reduce NO2− or NO3− to N2O rather than N2 [41]. This explains the inverse relationship between DOC and N2 production (Figure 6A), indicating that higher DOC levels induced by the single application of BS reduced cumulative N2 emissions. In contrast, previous studies have linked increased labile carbon to greater N2 emissions during complete denitrification [42,43]. Further research into how microbes respond to DOC levels during different denitrification processes is needed in order to mitigate N2O emissions more successfully in agriculture.

4.2. Factors Influencing DMPP Efficacy Under Different BS Application Frequencies

The efficacy of DMPP in inhibiting N2O emissions and nitrification varied with BS application frequency, due to changes in soil factors. Among all treatments, DMPP had the highest N2O emissions inhibition and nitrification inhibition rate of 94.6% and 63.0% separately when applied with initial BS addition (Figure 5), which is in line with results of other studies reporting suppression of N2O emissions after DMPP addition in BS-amended soil [18,19]. The N2O inhibition rate related positively to the nitrification inhibition rate (Figure 6B), demonstrating that N2O derived mostly from nitrification under the single application of BS. The positive relationship between DMPP efficacy in inhibiting nitrification rate and soil NH4+ contents was shown (Figure 6A). Previous studies have demonstrated that DMPP is most effective in suppressing the activity of nitrifying bacteria when NH4+ concentrations are high [19,44]. After the single application of BS, NH4+ levels are elevated, which facilitates the rate-limiting step in nitrification—the oxidation of NH4+ to NO2- [45]. However, the presence of DMPP interferes with this process by inhibiting the activity of the specific enzymes involved in this conversion, thereby effectively minimizing the nitrification rate [46]. The multiple application of BS in the B2 treatment possibly resulted in high N immobilization and limited the NH4+ availability for nitrification [47], which likely weakened the efficacy of DMPP. Many studies had similar results [48,49].
In the present study, there was an obvious positive relationship between soil pH and DMPP efficacy in inhibiting N2O emissions and the nitrification rate. Previous studies have reported that BS-amended soil is generally characterized by an elevated pH [50]. In the present study, it was observed that when the BS was initially applied, the soil pH increased significantly due to the alkaline nature of the BS. However, with the incubation and the repeated application of BS, the soil pH decreased, contributing to the low DMPP efficacy in the B2-DMPP. Poor DMPP performance in soils with relatively low pH is well documented in previous studies [51,52]. These all support the results from the current trial, where DMPP proved more effective at nitrification and N2O emission inhibition in relatively more alkaline soils. The increase in pH and an input of NH4+ substrate via BS addition facilitated microbial activity, especially ammonia-oxidizing bacteria [53], which DMPP inhibited effectively [52].

5. Conclusions

A single application of BS showed the highest N2O emissions compared to multiple applications, due to the abundant NH4+ and high pH in the treated soil. Combining an application of the nitrification inhibitor DMPP with a single BS application gives the best environmental outcomes. The elevated soil pH, NH4+ contents, and lower NO3− contents were conducive to better DMPP performance in decreasing N2O emissions produced by single application of BS. Further research should delve into the specific mechanism by which BS influences soil N2O emissions, particularly in the context of microbial N transformation processes. Such insights would facilitate the development of more effective measures aimed at achieving environmentally sustainable utilization of BS.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/agronomy14081844/s1. Detailed information about the system and the principle of gas measurement in provided in Section 2.2 Experimental design: Section 2.2.2 Gas kinetics analysis [54].

Author Contributions

Conceptualization, R.L.; methodology, J.L. and J.Y.; software, J.L. and Y.S.; validation, Y.S. and J.Y.; formal analysis, J.L.; investigation, Y.S. and J.L.; data curation, J.Y.; writing—original draft preparation, J.L.; writing—review and editing, J.L., Q.C., and R.L.; visualization, J.L. and J.Y.; supervision, R.L. and Q.C.; project administration, R.L.; funding acquisition, R.L. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the National Natural Science Foundation of China, grant number 42277234, the Chinese Universities Scientific Fund, grant number 15054009, and the National Key Research and Development Program “Intergovernmental Cooperation in International Science and Technology Innovation”, grant number 2023YFE0104700.

Data Availability Statement

The data presented in this study are available on request from the corresponding author.

Acknowledgments

The authors would like to thank the anonymous reviewers for their insightful and constructive comments, which greatly improved the manuscript.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Chadwick, D.; Wei, J.; Yan’An, T.; Guanghui, Y.; Qirong, S.; Qing, C. Improving manure nutrient management towards sustainable agricultural intensification in China. Agric. Ecosyst. Environ. 2015, 209, 34–46. [Google Scholar] [CrossRef]
  2. Rahaman, M.A.; Zhan, X.; Zhang, Q.; Li, S.; Lv, S.; Long, Y.; Zeng, H. Ammonia Volatilization Reduced by Combined Application of Biogas Slurry and Chemical Fertilizer in Maize–Wheat Rotation System in North China Plain. Sustainability 2020, 12, 4400. [Google Scholar] [CrossRef]
  3. Tang, Y.; Wen, G.; Li, P.; Dai, C.; Han, J. Effects of Biogas Slurry Application on Crop Production and Soil Properties in a Rice–Wheat Rotation on Coastal Reclaimed Farmland. Water Air Soil Pollut. 2019, 230, 51. [Google Scholar] [CrossRef]
  4. Chen, Z.; Wang, Q.; Ma, J.; Chapman, S.; Zou, P.; Ye, J.; Yu, Q.; Sun, W.; Lin, H.; Jiang, L. Soil microbial activity and community composition as influenced by application of pig biogas slurry in paddy field in southeast China. Paddy Water Environ. 2020, 18, 15–25. [Google Scholar] [CrossRef]
  5. Kong, F.; Li, Q.; Yang, Z.; Chen, Y. Does the application of biogas slurry reduce soil N2O emissions and increase crop yield? –A systematic review. J. Environ. Manag. 2023, 342, 118339. [Google Scholar] [CrossRef]
  6. Chen, Q.; Liu, T. Biogas system in rural China: Upgrading from decentralized to centralized? Renew. Sustain. Energy Rev. 2017, 78, 933–944. [Google Scholar] [CrossRef]
  7. Lourenço, K.S.; Cantarella, H.; Soares, J.R.; Gonzaga, L.C.; Menegale, P.L.D.C. DMPP mitigates N2O emissions from nitrogen fertilizer applied with concentrated and standard vinasse. Geoderma 2021, 404, 115258. [Google Scholar] [CrossRef]
  8. Tang, J.; Davy, A.J.; Wang, W.; Zhang, X.; Wu, D.; Hu, L.; Yin, J. Effects of Biogas Slurry on Crop Yield, Physicochemical Properties and Aggregation Characteristics of Lime Concretion Soil in Wheat–Maize Rotation in the North China Plain. J. Soil Sci. Plant Nutr. 2022, 22, 2406–2417. [Google Scholar] [CrossRef]
  9. Rahaman, M.A.; Zhang, Q.; Shi, Y.; Zhan, X.; Li, G. Biogas slurry application could potentially reduce N2O emissions and increase crop yield. Sci. Total Environ. 2021, 778, 146269. [Google Scholar] [CrossRef] [PubMed]
  10. Shi, Y.; Rahaman, M.A.; Zhang, Q.; Zhan, X.; Zheng, L. Effects of partial substitution of chemical fertilizer with biogas slurry on nitrous oxide emissions and the related nitrifier and denitrifier in a saline–alkali soil. Environ. Technol. Innov. 2022, 28, 102900. [Google Scholar] [CrossRef]
  11. Odlare, M.; Pell, M.; Svensson, K. Changes in soil chemical and microbiological properties during 4 years of application of various organic residues. Waste Manag. 2008, 28, 1246–1253. [Google Scholar] [CrossRef]
  12. Abubaker, J.; Risberg, K.; Jönsson, E.; Dahlin, A.S.; Cederlund, H.; Pell, M.; Clemente, R. Short-Term Effects of Biogas Digestates and Pig Slurry Application on Soil Microbial Activity. Appl. Environ. Soil Sci. 2015, 2015, 658542. [Google Scholar] [CrossRef]
  13. Xu, M.; Xian, Y.; Wu, J.; Gu, Y.; Yang, G.; Zhang, X.; Peng, H.; Yu, X.; Xiao, Y.; Li, L. Effect of biogas slurry addition on soil properties, yields, and bacterial composition in the rice-rape rotation ecosystem over 3 years. J. Soils Sediments 2019, 19, 2534–2542. [Google Scholar] [CrossRef]
  14. Liu, C.; Chen, Y.; Li, X.; Zhang, Y.; Ye, J.; Huang, H.; Zhu, C. Temporal effects of repeated application of biogas slurry on soil antibiotic resistance genes and their potential bacterial hosts. Environ. Pollut. 2020, 258, 113652. [Google Scholar] [CrossRef] [PubMed]
  15. Di, H.J.; Cameron, K.C.; Sherlock, R.R.; Shen, J.; He, J.; Winefield, C.S. Nitrous oxide emissions from grazed grassland as affected by a nitrification inhibitor, dicyandiamide, and relationships with ammonia-oxidizing bacteria and archaea. J. Soils Sediments 2010, 10, 943–954. [Google Scholar] [CrossRef]
  16. Friedl, J.; Scheer, C.; Rowlings, D.W.; Deltedesco, E.; Gorfer, M.; De Rosa, D.; Grace, P.R.; Müller, C.; Keiblinger, K.M. Effect of the nitrification inhibitor 3,4-dimethylpyrazole phosphate (DMPP) on N-turnover, the N2O reductase-gene nosZ and N2O:N2 partitioning from agricultural soils. Sci. Rep. 2020, 10, 2399. [Google Scholar] [CrossRef]
  17. Li, H.; Song, X.; Bakken, L.R.; Ju, X. Reduction of N2O emissions by DMPP depends on the interactions of nitrogen sources (digestate vs. urea) with soil properties. J. Integr. Agric. 2023, 22, 251–264. [Google Scholar] [CrossRef]
  18. Huf, M.; Olfs, H. Effect of the nitrification inhibitor DMPP on nitrous oxide emissions and the stabilization of ammonium following the injection of dairy slurry and digestate in a soil-column experiment. J. Plant Nutr. Soil Sci. 2020, 183, 129–135. [Google Scholar] [CrossRef]
  19. Guo, Y.; Anjum, A.; Khan, A.; Naeem, A.; Mühling, K.H. Comparative Effectiveness of Biogas Residue Acidification and Nitrification Inhibitors in Mitigating CO2 and N2O Emissions from Biogas Residue-Amended Soils. Water Air Soil Pollut. 2021, 232, 345. [Google Scholar] [CrossRef]
  20. Van Nguyen, Q.; Wu, D.; Kong, X.; Bol, R.; Petersen, S.O.; Jensen, L.S.; Liu, S.; Brüggemann, N.; Glud, R.N.; Larsen, M.; et al. Effects of cattle slurry and nitrification inhibitor application on spatial soil O2 dynamics and N2O production pathways. Soil Biology and Biochemistry 2017, 114, 200–209. [Google Scholar] [CrossRef]
  21. Di, H.J.; Cameron, K.C. Inhibition of ammonium oxidation by a liquid formulation of 3, 4-Dimethylpyrazole phosphate (DMPP) compared with a dicyandiamide (DCD) solution in six new Zealand grazed grassland soils. J. Soils Sediments 2011, 11, 1032–1039. [Google Scholar] [CrossRef]
  22. Lei, J.; Fan, Q.; Yu, J.; Ma, Y.; Yin, J.; Liu, R. A meta-analysis to examine whether nitrification inhibitors work through selectively inhibiting ammonia-oxidizing bacteria. Front. Microbiol. 2022, 13, 962146. [Google Scholar] [CrossRef]
  23. Gao, J.; Luo, J.; Lindsey, S.; Shi, Y.; Wei, Z.; Wang, L.; Zhang, L. Effects of soil properties on urea-N transformation and efficacy of nitrification inhibitor 3, 4-dimethypyrazole phosphate (DMPP). Soil Sci. Plant Nutr. 2022, 68, 228–237. [Google Scholar] [CrossRef]
  24. Wu, D.; Dong, W.; Oenema, O.; Wang, Y.; Trebs, I.; Hu, C. N2O consumption by low-nitrogen soil and its regulation by water and oxygen. Soil Biol. Biochem. 2013, 60, 165–172. [Google Scholar] [CrossRef]
  25. Molstad, L.; Dorsch, P.; Bakken, L.R. Robotized incubation system for monitoring gases (O2, NO, N2O, N2) in denitrifying cultures. J. Microbiol. Methods 2007, 71, 202–211. [Google Scholar] [CrossRef]
  26. Mcmillan, A.; Phillips, R.; Berben, P.; Palmada, T.; Jha, N.; Saggar, S. Automated N2O/N2 analysis—A new tool for studying denitrification dynamics and testing mitigation strategies. In Nutrient Management for the Farm, Catchment and Community; Occasional Report 27; Currie, L.D., Christensen, C.L., Eds.; Palmerston North, Fertilizer and Lime Research Centre, Massey University: Wellington, New Zealand, 2014; 14p, Available online: http://flrc.massey.ac.nz/publications.html (accessed on 23 October 2014).
  27. Li, X.; Sardans, J.; Gargallo-Garriga, A.; Asensio, D.; Vallicrosa, H.; Peñuelas, J. Nitrogen reduction processes in paddy soils across climatic gradients: Key controlling factors and environmental implications. Geoderma 2020, 368, 114275. [Google Scholar] [CrossRef]
  28. Zhang, Z.; Zhao, X.; Gao, Q.; Zhao, H.; Wang, G.; Tian, G.; Liu, J.; Yang, J. Study on the mechanism of nitrapyrin microcapsule suspension effectively improving nitrification inhibition rate in black soil. Ecotox. Environ. Saf. 2023, 265, 115539. [Google Scholar] [CrossRef]
  29. Mccarty, G.W.; Bremner, J.M. Inhibition of nitrification in soil by heterocyclic nitrogen compounds. Biol. Fertil. Soils 1989, 8, 204–211. [Google Scholar] [CrossRef]
  30. Liao, X.; Chen, Y.; Ruan, H.; Malghani, S. Incapability of biochar to mitigate biogas slurry induced N2O emissions: Field investigations after 7 years of biochar application in a poplar plantation. Sci. Total Environ. 2021, 794, 148572. [Google Scholar] [CrossRef] [PubMed]
  31. Cheng, J.; Chen, Y.; He, T.; Liu, R.; Yi, M.; Yang, Z. Effects of biogas slurry irrigation DOC/N ratios on the fate of soil nitrogen and GHG emissions: A laboratory study. Geoderma 2020, 375, 114458. [Google Scholar] [CrossRef]
  32. Tierling, J.; Kuhlmann, H. Emissions of nitrous oxide (N2O) affected by pH-related nitrite accumulation during nitrification of N fertilizers. Geoderma 2018, 310, 12–21. [Google Scholar] [CrossRef]
  33. Well, R.; Flessa, H.; Xing, L.; Xiaotang, J.; Römheld, V. Isotopologue ratios of N2O emitted from microcosms with NH4+ fertilized arable soils under conditions favoring nitrification. Soil Biol. Biochem. 2008, 40, 2416–2426. [Google Scholar] [CrossRef]
  34. Coban, H.; Miltner, A.; Elling, F.J.; Hinrichs, K.U.; Kästner, M. The contribution of biogas residues to soil organic matter formation and CO2 emissions in an arable soil. Soil Biol. Biochem. 2015, 86, 108–115. [Google Scholar] [CrossRef]
  35. Zhu, Y.; Yuan, G.; Zhao, Z.; Tang, Y.; Li, P.; Han, J. Pig farm biogas slurry can effectively reduce the pH of saline-alkali soils. Environ. Technol. 2023, 44, 1415–1425. [Google Scholar] [CrossRef]
  36. Terhoeven-Urselmans, T.; Scheller, E.; Raubuch, M.; Ludwig, B.; Joergensen, R.G. CO2 evolution and N mineralization after biogas slurry application in the field and its yield effects on spring barley. Appl. Soil Ecol. 2009, 42, 297–302. [Google Scholar] [CrossRef]
  37. Orlova, N.; Abakumov, E.; Orlova, E.; Yakkonen, K.; Shahnazarova, V. Soil organic matter alteration under biochar amendment: Study in the incubation experiment on the Podzol soils of the Leningrad region (Russia). J. Soils Sediments 2019, 19, 2708–2716. [Google Scholar] [CrossRef]
  38. Niyungeko, C.; Liang, X.; Liu, C.; Zhou, J.; Chen, L.; Lu, Y.; Tiimub, B.M.; Li, F. Effect of biogas slurry application on soil nutrients, phosphomonoesterase activities, and phosphorus species distribution. J. Soils Sediments 2020, 20, 900–910. [Google Scholar] [CrossRef]
  39. Zhang, Y.; Niu, H.; Wang, S.; Xu, K.; Wang, R. Application of the DNDC model to estimate N2O emissions under different types of irrigation in vineyards in Ningxia, China. Agric. Water Manag. 2016, 163, 295–304. [Google Scholar] [CrossRef]
  40. Azam, F.; Müller, C.; Weiske, A.; Benckiser, G.; Ottow, J. Nitrification and denitrification as sources of atmospheric nitrous oxide—role of oxidizable carbon and applied nitrogen. Biol. Fertil. Soils 2002, 35, 54–61. [Google Scholar] [CrossRef]
  41. Jirout, J. Nitrous oxide productivity of soil fungi along a gradient of cattle impact. Fungal Ecol. 2015, 17, 155–163. [Google Scholar] [CrossRef]
  42. Giles, M.E.; Daniell, T.J.; Baggs, E.M. Compound driven differences in N2 and N2O emission from soil; the role of substrate use efficiency and the microbial community. Soil Biol. Biochem. 2017, 106, 90–98. [Google Scholar] [CrossRef]
  43. Xiao, Q.; Huang, Y.; Wu, L.; Tian, Y.; Wang, Q.; Wang, B.; Xu, M.; Zhang, W. Long-term manuring increases microbial carbon use efficiency and mitigates priming effect via alleviated soil acidification and resource limitation. Biol. Fertil. Soils 2021, 57, 925–934. [Google Scholar] [CrossRef]
  44. Qiao, C.; Liu, L.; Hu, S.; Compton, J.E.; Greaver, T.L.; Li, Q. How inhibiting nitrification affects nitrogen cycle and reduces environmental impacts of anthropogenic nitrogen input. Glob. Change Biol. 2015, 21, 1249–1257. [Google Scholar] [CrossRef]
  45. Guo, Y.; Geng, J.; Cheng, S.; Fang, H.; Li, X.; Yang, Y.; Li, Y.; Zhou, Y. Soil acidification and ammonia-oxidizing archaeal abundance dominate the contrasting responses of soil N2O emissions to NH4+ and NO3- enrichment in a subtropical plantation. Eur. J. Soil Biol. 2023, 116, 103491. [Google Scholar] [CrossRef]
  46. Shi, X.; Hu, H.; Müller, C.; He, J.; Chen, D.; Suter, H.C. Effects of the Nitrification Inhibitor 3,4-Dimethylpyrazole Phosphate on Nitrification and Nitrifiers in Two Contrasting Agricultural Soils. Appl. Environ. Microbiol. 2016, 82, 5236–5248. [Google Scholar] [CrossRef]
  47. Sørensen, P.; Amato, M. Remineralisation and residual effects of N after application of pig slurry to soil. Eur. J. Agron. 2002, 16, 81–95. [Google Scholar] [CrossRef]
  48. Abalos, D.; Sanz-Cobena, A.; Andreu, G.; Vallejo, A. Rainfall amount and distribution regulate DMPP effects on nitrous oxide emissions under semiarid Mediterranean conditions. Agric. Ecosyst. Environ. 2017, 238, 36–45. [Google Scholar] [CrossRef]
  49. Di, H.J.; Cameron, K.C. Inhibition of nitrification to mitigate nitrate leaching and nitrous oxide emissions in grazed grassland: A review. J. Soils Sediments 2016, 16, 1401–1420. [Google Scholar] [CrossRef]
  50. Möller, K.; Müller, T. Effects of anaerobic digestion on digestate nutrient availability and crop growth: A review. Eng. Life Sci. 2012, 12, 242–257. [Google Scholar] [CrossRef]
  51. Bachtsevani, E.; Papazlatani, C.V.; Rousidou, C.; Lampronikou, E.; Menkissoglu-Spiroudi, U.; Nicol, G.W.; Karpouzas, D.G.; Papadopoulou, E.S. Effects of the nitrification inhibitor 3, 4-dimethylpyrazole phosphate (DMPP) on the activity and diversity of the soil microbial community under contrasting soil pH. Biol. Fertil. Soils 2021, 57, 1117–1135. [Google Scholar] [CrossRef]
  52. Kleineidam, K.; Košmrlj, K.; Kublik, S.; Palmer, I.; Pfab, H.; Ruser, R.; Fiedler, S.; Schloter, M. Influence of the nitrification inhibitor 3,4-dimethylpyrazole phosphate (DMPP) on ammonia-oxidizing bacteria and archaea in rhizosphere and bulk soil. Chemosphere 2011, 84, 182–186. [Google Scholar] [CrossRef] [PubMed]
  53. Kaveney, B.; Condon, J.; Doran, G.; Galea, F.; Rigg, J. The distribution of soil nitrifiers and efficacy of 3, 4-dimethylpyrazole phosphate changes with soil depth and calcium carbonate application. Soil Biol. Biochem. 2020, 150, 108009. [Google Scholar] [CrossRef]
  54. Cao, W.; Liu, S.; Qu, Z.; Song, H.; Qin, W.; Guo, J.; Chen, Q.; Lin, S.; Wang, J. Contribution and driving mechanism of N2O emission bursts in a Chinese vegetable greenhouse after manure application and irrigation. Sustainability 2019, 11, 1624. [Google Scholar] [CrossRef]
Agronomy 14 01844 g001
Figure 1. Schematic representation of the experimental design in this study. The blue arrows indicate the addition of the solution and the incubation period, while the brown arrows represent the destructive sampling of the soil.
Figure 1. Schematic representation of the experimental design in this study. The blue arrows indicate the addition of the solution and the incubation period, while the brown arrows represent the destructive sampling of the soil.
Agronomy 14 01844 g001
Agronomy 14 01844 g002
Figure 2. Soil properties in different treatments (mean ± SE, n = 3). Soil pH (A), dissolved organic carbon (B), NH4+ (C), and NO3− (D) contents. The same lowercase letters indicate no significant differences among different treatments.
Figure 2. Soil properties in different treatments (mean ± SE, n = 3). Soil pH (A), dissolved organic carbon (B), NH4+ (C), and NO3− (D) contents. The same lowercase letters indicate no significant differences among different treatments.
Agronomy 14 01844 g002
Agronomy 14 01844 g003
Figure 3. Measured N2O and N2 emissions from soil during the incubation period in different treatments (mean ± SE, n = 3). Gas emissions characteristics in B0 (A), B0-DMPP (B), CK0 (C), B1 (D), B1-DMPP (E), CK1 (F), B2 (G), B2-DMPP (H), and CK2 (I) treatments.
Figure 3. Measured N2O and N2 emissions from soil during the incubation period in different treatments (mean ± SE, n = 3). Gas emissions characteristics in B0 (A), B0-DMPP (B), CK0 (C), B1 (D), B1-DMPP (E), CK1 (F), B2 (G), B2-DMPP (H), and CK2 (I) treatments.
Agronomy 14 01844 g003
Agronomy 14 01844 g004
Figure 4. Effect of BS and DMPP on measured O2 concentration and CO2 emissions from soil during the incubation period (mean ± SE, n = 3). The O2 concentration and CO2 emissions in B0 and B0-DMPP treatments (A), B1 and B1-DMPP treatments (B), B2 and B2-DMPP treatments (C), and Control (CK0, CK1, and CK2) treatments (D).
Figure 4. Effect of BS and DMPP on measured O2 concentration and CO2 emissions from soil during the incubation period (mean ± SE, n = 3). The O2 concentration and CO2 emissions in B0 and B0-DMPP treatments (A), B1 and B1-DMPP treatments (B), B2 and B2-DMPP treatments (C), and Control (CK0, CK1, and CK2) treatments (D).
Agronomy 14 01844 g004
Agronomy 14 01844 g005
Figure 5. The cumulative N2O emissions inhibition and nitrification inhibition rate by DMPP under different BS application frequencies (mean ± SE, n = 3). The same uppercase and lowercase letters indicate no significant differences among different soils in N2O inhibition (uppercase) and nitrification inhibition (lowercase) after the DMPP application, according to the least significant difference test at p < 0.05.
Figure 5. The cumulative N2O emissions inhibition and nitrification inhibition rate by DMPP under different BS application frequencies (mean ± SE, n = 3). The same uppercase and lowercase letters indicate no significant differences among different soils in N2O inhibition (uppercase) and nitrification inhibition (lowercase) after the DMPP application, according to the least significant difference test at p < 0.05.
Agronomy 14 01844 g005
Agronomy 14 01844 g006
Figure 6. Heatmap of Pearson’s correlation between gas emission characteristics and soil variables in soils with different BS application frequencies (A), and Pearson’s correlation between the efficacy of DMPP and soil variables in different treatments (B). The positive correlations are shown in a red circle, and the negative correlations are shown in a blue circle. The circle size is proportional to the Pearson correlation.
Figure 6. Heatmap of Pearson’s correlation between gas emission characteristics and soil variables in soils with different BS application frequencies (A), and Pearson’s correlation between the efficacy of DMPP and soil variables in different treatments (B). The positive correlations are shown in a red circle, and the negative correlations are shown in a blue circle. The circle size is proportional to the Pearson correlation.
Agronomy 14 01844 g006
Table 1. Chemical properties of the experimental BS.
Table 1. Chemical properties of the experimental BS.
pH
 		EC
(ms cm−1)		NO3−
(mg L−1)		NH4+
(g L−1)		TP
(mg L−1)		TOC
(g L−1)		COD
(g L−1)		Humic Acid
(%)		TN
(g L−1)
8.5841.886.84.782868.0924.41.035.71
Note: EC = electrical conductivity, TP = total phosphorus, TOC = total organic carbon, COD = chemical oxygen demand, TN = total N. Units are given in the text.
Table 2. Effect of BS and DMPP on soil cumulative N2O emissions, N2 emissions, and the ratio of N2O/(N2O+N2) (mean ± SE, n = 3).
Table 2. Effect of BS and DMPP on soil cumulative N2O emissions, N2 emissions, and the ratio of N2O/(N2O+N2) (mean ± SE, n = 3).
TreatmentCumulative N2O Emissions
(nmol N g−1)		Cumulative N2 Emissions
(nmol N g−1)		N2O/(N2O + N2)
(×10−3)
CK0Not detected85.2 ± 4.25 ab0 d
CK1Not detected73.8 ± 3.29 ab0 d
CK20.15 ± 0.02 c89.5 ± 10.3 a1.81 ± 0.38 d
B02.59 ± 0.06 a55.4 ± 13.8 b38.3 ± 2.31 a
B10.63 ± 0.11 b84.1 ± 3.56 ab7.30 ± 0.96 c
B20.54 ± 0.04 b71.2 ± 2.48 ab7.52 ± 0.25 c
B0-DMPP0.14 ± 0.001 cd76.0 ± 10.7 ab1.91 ± 0.24 d
B1-DMPP0.10 ± 0.001 cd70.2 ± 6.43 ab1.45 ± 0.20 d
B2-DMPP0.53 ± 0.05 b43.3 ± 3.27 c12.1 ± 0.57 b
Note: The same lowercase letters indicate no significant differences among different treatments in cumulative N2O emissions, cumulative N2 emissions, and N2O/(N2O + N2), according to the least significant difference test at p < 0.05.
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Lei, J.; Sun, Y.; Yin, J.; Liu, R.; Chen, Q. Influence of Biogas Slurry and a Nitrification Inhibitor Application in Nitrous Oxide Emissions by Soil. Agronomy 2024, 14, 1844. https://doi.org/10.3390/agronomy14081844

AMA Style

Lei J, Sun Y, Yin J, Liu R, Chen Q. Influence of Biogas Slurry and a Nitrification Inhibitor Application in Nitrous Oxide Emissions by Soil. Agronomy. 2024; 14(8):1844. https://doi.org/10.3390/agronomy14081844

Chicago/Turabian Style

Lei, Jilin, Yingying Sun, Junhui Yin, Rui Liu, and Qing Chen. 2024. "Influence of Biogas Slurry and a Nitrification Inhibitor Application in Nitrous Oxide Emissions by Soil" Agronomy 14, no. 8: 1844. https://doi.org/10.3390/agronomy14081844

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop