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Article

Substitution of Mineral Fertilizer with Organic Fertilizer in Maize Systems: A Meta-Analysis of Reduced Nitrogen and Carbon Emissions

1
Center for Resources, Environment and Food Security, China Agricultural University, Beijing 100193, China
2
Department of Soil Quality, Wageningen University & Research, P.O. Box 47, 6700 AA Wageningen, The Netherlands
*
Author to whom correspondence should be addressed.
Agronomy 2020, 10(8), 1149; https://doi.org/10.3390/agronomy10081149
Submission received: 21 June 2020 / Revised: 4 August 2020 / Accepted: 5 August 2020 / Published: 6 August 2020

Abstract

:
Organic fertilizer is an effective substitute for mineral fertilizer that improves crop yield and is environmentally friendly. However, the effects of substitution often vary due to complicated interactions among the organic fertilizer substitution rate (Rs), total nutrient supply, and type of cropping system used. We performed a meta-analysis of 133 maize studies, conducted worldwide, to assess maize yield and environmental performance with substitution of mineral fertilizer with organic fertilizer. At an equivalent nitrogen (N) rate, substituting mineral fertilizer with organic fertilizer increased maize yield by 4.22%, reduced NH3 volatilization by 64.8%, reduced N leaching and runoff by 26.9%, and increased CO2 emissions by 26.8%; however, it had no significant effect on N2O or CH4 emissions. Moreover, substitution with organic fertilizer increased the soil organic carbon sequestration rate by 925 kg C ha−1 yr−1 and decreased the global warming potential by 116 kg CO2 eq ha−1 compared with mineral fertilizer treatment. The net global warming potential after organic fertilizer substitution was −3507 kg CO2 eq ha−1, indicating a net carbon sink. Furthermore, the effect of organic fertilizer substitution varied with the fertilization rate, Rs, and treatment duration. Maize yield and nitrogen use efficiency tended to increase with increasing N application rate following substitution of mineral fertilizer with organic fertilizer. Full substitution reduced N losses more than partial substitution. Further analysis revealed that the yield-optimal Rs for organic N in maize production was 40–60%. Moreover, maize yield and nitrogen use efficiency were further increased after long-term (≥ 3 years) combined use of organic and mineral fertilizers. These findings suggest that rational use of organic and mineral fertilizers improves maize productivity, increases soil organic carbon sequestration, and reduces N and C losses.

1. Introduction

Fertilizer has played a key role in global food safety over recent decades, which is necessary to meet the needs of the increasing world population [1]. However, overuse of mineral fertilizer introduces substantial reactive nitrogen (Nr) emissions into the environment, resulting in adverse effects such as air pollution [2,3], soil degradation and acidification [4], and water eutrophication [5,6]. The emitted Nr to air is a major precursor to form fine particular matter with the aerodynamic diameter less than 2.5 μm (PM2.5), which is a threat to human health [5]. The nitrate discharged to water could cause biodiversity losses [5,6]. Global annual production of livestock manure nitrogen (N) has reached nearly 100 Tg N [7]. Recycling of manure and other organic materials into the field could potentially create a “win-win” situation, by reducing mineral fertilizer input while simultaneously addressing sanitation problems [8,9]. However, the contaminants in it, such as antibiotics or heavy metals, could limit the widespread use of household and animal waste [10,11]. Many researchers have explored the effect of substituting mineral fertilizer with organic fertilizer. Organic fertilizer application is also regarded as an efficient way to increase soil organic carbon (SOC) [12], which not only enhances crop production [13], but also acts as a conditioner to improve soil resilience and health, reduce C (CO2) and N (N2O, nitrate) emissions to the environment and increase water retention [13,14]. A meta-analysis of studies performed in Africa demonstrated that combined use of organic and mineral fertilizers increased crop yield, but the substitution rates (Rs) used were not specified [15]. A study carried out in China analyzed the effect of organic fertilizer Rs on crop productivity and Nr losses and found that the yield-optimal Rs for manure N was 50–75% [16]. However, the usefulness of previous studies is limited by suboptimal N rates, and variation in application timing and duration [12,17]. Comparison of the agronomic and environmental effects of organic fertilizer substitution is difficult because the optimal N supply rate is highly variable among years and sites.
Substitution of mineral fertilizer with organic fertilizer has multiple effects on crop production, environmental emissions, and SOC sequestration. Most studies only evaluated one aspect, such as crop yield [18], nitrogen use efficiency (NUE) [19], SOC [12], or environmental emissions [17]. Xia et al. (2017) evaluated the net global warming potential (NGWP) associated with manure substitution; they found that substituting manure for mineral fertilizer increased the carbon (C) sink in upland fields [16], but they did not consider the indirect effects of NH3 emissions and runoff/leaching on NGWP. Moreover, most reviews of research on organic fertilizer substitution considered all crops in combination, thus providing data with limited utility for assessing the crop-specific effects of organic fertilizer substitution on yield and environmental emissions [17,18].
In this study, we performed a meta-analysis of studies conducted worldwide to quantitatively assess the effects of substituting organic fertilizers for mineral fertilizers on maize production, N and C emissions, and the soil organic carbon sequestration rate (SOCSR). We also evaluated the global warming potential (GWP) and NGWP, considering the indirect effects of NH3 emissions and runoff/leaching. The responses of these variables to organic fertilizer substitution were evaluated according to the fertilization rate (low, optimal, or high), Rs, and treatment duration. The underlying causes of the different responses of these variables to substitution of chemical with organic fertilizer are discussed.

2. Materials and Methods

2.1. Data Collection

Peer-reviewed articles were searched for to evaluate the effects of substitution of mineral fertilizer with organic fertilizer on maize yield, N and C losses, and SOC sequestration. Studies published before March 2020 were searched for in the Microsoft Academic (https://academic.microsoft.com/home), Google Scholar (https://scholar.google.com/), Baidu Scholar (http://xueshu.baidu.com/), and China National Knowledge Infrastructure (http://www.cnki.net/) databases. Search terms related to maize production, organic fertilizer substitution, manure application, and N and C emissions were combined.
The studies included in our analysis satisfied the following criteria: (1) Studies focused on maize production with substitution of mineral fertilizer with organic fertilizer, including animal manure (47%), compost (37%), commercial organic fertilizer (e.g., industrially processed, standardized poultry or livestock manure; 9%), digestate (5%), slurry (2%); (2) The amounts of applied organic material and the N content were clearly specified; (3) The mineral fertilizer treatment and “substitution treatments” (partial or full substitution of chemical with organic fertilizer) had identical total N rates, and phosphorus (P) and potassium (K) inputs were not major factors limiting maize growth; (4) The N application rates for each treatment were reported to allow calculation of the Rs, defined as organic N input/total N applied; (5) Field or lysimeter study, with articles reporting data from the same experiment excluded; and (6) Experimental duration of at least 3 years with respect to the effects of organic fertilizer on soil properties (e.g., SOC) [20]. In total, 133 published articles performed worldwide were included in the analysis (see supporting information for details).

2.2. Evaluated Variables and Data Treatment

Eight dependent/response variables were evaluated to determine the effects of substitution of mineral fertilizer with organic fertilizer, categorized as follows: (1) maize productivity: maize yield and NUE; (2) N losses: NH3 emissions, N2O emissions, and N runoff/leaching; and (3) C emissions (CO2 and CH4) and SOCSR. NUE, based on the N recovery rate, was calculated using the following equation:
NUE = (UfU0)/F
where Uf and U0 are the aboveground N uptake of maize in plots with and without fertilization, respectively; F indicates total fertilizer N input.
For studies that did not report SOCSR directly, it was calculated using the following equation [16]:
SOCSR (kg C ha−1 yr−1) = (SOCf × ρfSOC0 × ρ0) × H × 100/T
where SOCf and SOC0 are the soil organic content (kg C t−1) in plots with and without fertilization, respectively; ρf and ρ0 are the soil bulk density (t m−3) for the fertilizer and control treatments, respectively; H is the sampling depth (cm); and T is the treatment duration. In studies with missing ρ-values, they were estimated using the following equation [16]:
ρ = − 0.0048 ln SOC + 1.377
The effects of substitution of mineral fertilizer with organic fertilizer were evaluated according to fertilization rate, Rs, and treatment duration. The optimal total fertilizer and organic fertilizer Rs were determined in terms of their effects on maize yield and NUE. The N fertilization rate for maize production was categorized as low, optimal, or high, where these categories were region-specific: the optimal N rates for Africa [20,21], Asia [22], and other regions [23,24] were 50–80, 150–210, and 180–250 kg N ha−1, respectively. The Rs, defined as organic N input/total N input, was divided into four categories (0 < Rs ≤ 40, 40 < Rs ≤ 60, 60 < Rs < 100, and Rs = 100) when analyzing maize productivity and N emissions. Two Rs categories, i.e., full (Rs = 100) and partial (0 < Rs < 100), were used when analyzing C emissions and SOCRS, as these data were limited. Treatment duration was classified as short (< 3 years) or long (≥ 3 years) for all dependent variables.

2.3. Meta-Analysis

A standardized effect size, which reflects the magnitude of the substitution treatment effect compared with the control, was calculated for all studies to allow robust statistical comparison, given that the studies reported results based on different variables [17]. To derive this standardized effect size, the natural log of the response ratio (lnR) was calculated [25], except for CH4 and SOCSR, as follows:
lnRR = ln(Xo/Xm)
where Xo and Xm are the mean values of variable X (e.g., maize yield, NUE, N emissions, C emissions) in the organic and mineral fertilizer treatments, respectively. Log transformation of the response ratio was used to stabilize the variance. Results were exponentially back-transformed and converted to percentage change values relative to the control treatment [(RR − 1) * 100]. Negative and positive percentage changes indicate a decrease or increase, respectively, in the corresponding response variable due to organic fertilizer substitution. The 95% confidence intervals (CIs) not overlapping zero denote significant differences.
The CH4 emissions and SOCSR values can be positive or negative; thus, Equation (4) is undefined. The effect sizes for these two variables were calculated based on the mean difference (RR2):
RR2 = XoXm
Effect sizes were weighted by the inverse of the sampling variance [26,27]. For studies where neither the standard deviation (SD) nor standard error (SE) were reported, the approach of Bracken [28] was applied to estimate SD using in the “metagear” R (ver. 3.6.1; R Development Core Team, Vienna, Austria) package. A random-effect model was employed for the meta-analysis, generated using the “metafor” R package. Maize production and N and C emissions databases were generated based on the study data using Excel 2010 software (Microsoft Corp., Redmond, WA, USA).

2.4. Net Global Warming Potential

The GWP of organic fertilizer substitution for mineral fertilizer was calculated based on changes in emissions of CH4, N2O, and NH3, and leaching/runoff:
GWP (kg CO2 eq ha−1) = (NH3-Nchange × 0.01 + NO3-Nchange × 0.0075 + N2O-Nchange) × 298 × 44/28+ CH4-Cchange × 25 × 16/12
where NH3-Nchange, NO3-Nchange, N2O-Nchange, and CH4-Cchange are the emission changes (kg ha−1) induced by organic fertilizer substitution. The values 298 and 25 represent the GWP of N2O and CH4 in units of CO2 equivalents over a 100-year period according to the Intergovernmental Panel on Climate Change (IPCC) Fifth Assessment Report [29]. The values 0.01 and 0.0075 represent the indirect N2O emissions from volatilized NH3-N and leached NO3-N, according to IPCC methodology [30]. The values of 44/28 and 16/12 indicate mass conversion factors of N to N2O, and C to CH4.
The NGWP was calculated using the following equation:
NGWP = GWPSOCSRchange × 44/12
where SOCSRchange is the SOCSR change induced by substituting mineral fertilizer with organic fertilizer. A negative value for NGWP indicates a net C sink, whereas a positive value represents a net C source.
The changes in CH4, N2O, and NH3 emissions, as well as leaching/runoff and SOCSR, were calculated separately for the full and partial substitution groups, to determine the GWP and NGWP by organic fertilizer Rs.

3. Results

3.1. Effects of Organic Fertilizer Substitution on N and C Emissions by Fertilization Rate

Substitution of mineral fertilizer with organic fertilizer significantly increased maize yield (by 4.23%) but had no significant effect on NUE (Figure 1). We found that maize yield and NUE tended to increase with increasing N fertilization rate. The low fertilization rate had a negative impact on NUE (−17.3%) and did not significantly enhance maize yield. The optimal fertilization rate significantly increased maize yield, but compromised NUE to some extent. The high fertilization rate significantly increased maize yield (4.83%) and NUE (8.77%).
Organic fertilizer substitution significantly decreased NH3 emissions (by 64.8%) and N leaching and runoff (by 26.8%), whereas N2O emissions were decreased non-significantly (by 12.7%). Organic fertilizer substitution decreased N losses at all fertilization rates, except for N2O at the low rate, which was significantly increased (by 33.1%). The decrease in NH3 and N2O emissions tended to increase with increasing N fertilization rate. The maximum decrease in N runoff and leaching (by 45.5%) was achieved at the optimal fertilization rate. At the high fertilization rate, all three types of N loss (NH3, N2O, and runoff and leaching) were significantly decreased (by 71.7%, 37.1%, and 22.1%, respectively; Figure 2).
Organic fertilizer substitution significantly increased CO2 emissions (by 26.8%) and the SOCSR (by 925 kg C ha−1 yr−1) but had no effect on CH4 emissions. CO2 emissions showed a decreasing trend as the rate of N fertilization increased, whereas the SOCSR showed an increasing trend as the fertilization rate increased. CH4 emissions were not significantly affected by organic fertilizer substitution at any of the three fertilization rates (Figure 3).

3.2. Effects of Organic Fertilizer Substitution on N and C Emissions at Different Substitution Rates

The yield-optimal Rs for organic fertilizer was 40–60%, and gave rise to a statistically significant increase in maize yield (11.5%). For Rs values between 60% and 100%, the yield increases were not significant. Full substitution of chemical with organic fertilizer (Rs = 100) decreased the maize yield to some extent. NUE decreased gradually from 17.3% to −20.4% as the Rs increased. NUE was increased significantly at the low Rs, but was decreased significantly by full substitution (Figure 4).
At the optimal fertilization rate, the yield-optimal Rs was between 60% and 100%, whereas with the low and high fertilization rates the optimal Rs was between 40% and 60%. NUE tended to decrease as the Rs increased at the low and high fertilization rates, whereas it did not change consistently at the optimal fertilization rate. Maize yield and NUE were both low at the full Rs for all three fertilization rates (Figure 5).
Partial substitution (0 < Rs < 100) of organic with mineral fertilizer did not significantly affect N losses, except for N2O at a partial Rs of 0–40%, and runoff and leaching at a rate of 40–60%. N2O emissions were significantly increased (by 23.7%) when the Rs was between 0% and 40%. Runoff and leaching were significantly decreased (by 41.9%) when the Rs was between 40% and 60% (Figure 6). Full substitution of organic with mineral fertilizer significantly decreased all types of N loss (93.0% for NH3, 25.0% for N2O, and 50.0% for runoff and leaching).
The variation in C emissions by Rs was large, probably due to the limited amount of available data. Partial substitution of mineral fertilizer with organic fertilizer did not significantly affect CO2 emissions, while full substitution significantly increased CO2 emissions (by 41.9%). CH4 emissions were not significantly affected by the Rs. The SOCSR under partial substitution was 968 kg C ha−1 yr−1, which was slightly higher than that under full substitution (817 kg C ha−1 yr−1; Figure 7).

3.3. Effects of Organic Fertilizer Substitution on N and C Emissions by Treatment Duration

Long-term application (≥3 years) of organic fertilizer significantly increased maize yield (by 11.5%) without compromising NUE, whereas short-term application (<3 years) did not affect maize yield or NUE. NH3 and N2O emissions were promoted by long-term organic fertilizer substitution in comparison with short-term application. Runoff and leaching were significantly decreased, by 47%, following long-term organic fertilizer substitution; this was significantly greater than the 11.2% reduction under short-term treatments. CH4 emissions under long-term treatments decreased slightly, by 0.63 kg CH4-C ha−1, but increased by 0.69 kg CH4-C ha−1 over the short term. CO2 emissions were increased by 54.3% under long-term organic fertilizer substitution but did not change significantly over the short term (Figure 8).

3.4. Effects of Organic Fertilizer Substitution on GWP and NGWP

Organic fertilizer substitution reduced greenhouse gas emissions (Table 1). The overall GWP decreased by 116 kg CO2 eq ha−1 with organic fertilizer substitution compared with chemical fertilization. Full replacement of mineral fertilizer with organic fertilizer reduced greenhouse gas emissions (203 kg CO2 eq ha−1) to a greater extent than partial substitution (67.2 kg CO2 eq ha−1), because volatilized NH3 and leached NO3 were reduced by full substitution. However, when considering NGWP, more C was sequestered with partial substitution (3617 kg CO2 eq ha−1) than with full substitution (3200 kg CO2 eq ha−1), because the SOCSR for partial substitution was larger than that for full substitution. The higher rate of soil C sequestration with partial substitution outweighed its adverse effect on greenhouse gas emissions compared with full substitution. The overall NGWP with organic fertilizer substitution was −3507 kg CO2 eq ha−1, indicating that a net C sink was produced by substitution of chemical with organic fertilizer.

4. Discussion

4.1. Maize Productivity and Soil Conditions

Substitution of mineral fertilizer with organic fertilizer significantly increased maize yield, probably by improving soil properties, and increasing SOC and total N (Table 2). The SOC content increased from 10.37 g kg−1 for mineral fertilizer treatment to 13.28 g kg−1 for organic fertilizer treatment, which could explain the positive SOCSR following substitution of chemical with organic fertilizer. The soil TN content increased from 1.1 to 1.29 g kg−1 following organic fertilizer substitution (Table 2). Full substitution of chemical with organic fertilizer decreased maize yield to some extent (Figure 4 and Figure 5), mainly because the in-season utilization rate is lower for organic N than for chemical N [31]; this could also explain the low NUE following organic fertilizer substitution.
Organic fertilizer substitution also reduced soil acidification caused by mineral fertilizer application [4]. The soil pH increased from 6.47 with mineral fertilizer treatment to 6.77 with organic fertilizer substitution treatment according to our literature review; nevertheless, the soil pH still decreased after long-term organic inputs in calcareous soil (Table 2). This may be because the soil pHs reported in the included articles was high (7.68), while the pH values of some organic fertilizers, especially those based on pig and poultry manure, can be less than 6.5 [32]. As the abundant humic acid in some organic materials decomposes, it releases H+ into the soil [33], which in turn decreases the pH of alkaline soil. We noticed that, conversely, organic fertilizer substitution increased the pH of acid soil [34]. Organic inputs therefore improve soil pH resilience. Soil aggregation [35] and water-holding capacity [36,37] were also improved after long-term organic substitution. Improved water-holding capacity is extremely important for rain-fed, water-starved maize planting systems.

4.2. N and C emissions

Organic fertilizer substitution tended to decrease all types of reactive N loss (Figure 2 and Figure 5). This may have been due to reduced availability of Nr (the major type of N loss) with organic fertilizer substitution treatment. The increase in CO2 emissions seen after organic fertilizer substitution was related to soil respiration, which was enhanced by increased C input into the soil (Table 2). The variation in CH4 emissions by Rs was large, but not significant, probably due to the limited amount of available data. The complexity of the CH4 production and oxidation processes could also explain the lack of significance. On one hand, the increased C inputs from organic fertilizer treatment suggest that more substrate is available for CH4 formation [47]. On the other hand, organic fertilizer treatment generally leads to lower ammonium content in soil compared with mineral fertilizer treatment. Ammonium normally inhibits CH4 oxidation because it increases the population of nitrifiers relative to methanotrophs, and nitrifiers oxidize CH4 less efficiently than methanotrophs, such that CH4 oxidizing activity changes to nitrification; therefore, lower ammonium content induces more CH4 oxidation [48]. These two processes counteract each other, such that CH4 emissions are not significantly affected by organic fertilizer substitution.
The overall GWP decreased by 203 kg CO2 eq ha−1 with full organic fertilizer substitution compared with chemical fertilization (Table 2). When considering the production of greenhouse gases (GHG) throughout the entire life cycle of organic and mineral fertilizers, the result could be different. The life cycle GHG emissions during mineral N fertilizer production are 8.2 kg CO2 eq kg N−1 [49]. However, life cycle GHG emissions during organic fertilizer production are highly variable, ranging from −40 to 45 kg CO2 eq kg N−1, depending on the production processes and manure types [50]. Negative value means the potential to save CO2. For example, anaerobic digestion could potentially reduce CO2 emission by replacing fossil fuel-based energy with biogas [50]. It is hard to conclude which one is better when comparing the entire life cycle GHG emissions of organic and mineral fertilizers. This study focuses on emissions after fertilizer application, rather than the life cycle emissions.

4.3. SOCSR

Two approaches are used to estimate the SOCSR; the method employed depends on the time scale and available data [47]. In short-term experiments, the SOCSR can be estimated from the difference between organic inputs and soil CO2 emissions. Organic inputs include organic fertilizer and biomass remaining in the field. However, in long-term experiments, the SOCSR is generally calculated based on the inter-annual changes in SOC (Equation (2)). Our meta-analysis demonstrated that the SOCSR for partial organic fertilizer substitution treatment (968 kg C ha−1 yr−1) was higher than for full substitution treatment (817 kg C ha−1 yr−1) (Table 2). This could be explained by the significantly higher maize yield obtained with the partial substitution treatments (Figure 4), which in turn indicates a larger amount of belowground root and other biomass residue remaining in the field. Considering that the maize straw was removed from the field in most articles reviewed (data not shown), partial organic fertilizer substitution has the potential to sequester more C when straw recycling technology is used.

4.4. Fertilization and Substitution Rates

Our meta-analysis of 133 studies indicated that fertilization rate had a large influence on the effectiveness of organic fertilizer substitution (Figure 1, Figure 2 and Figure 3). Organic fertilizer substitution is most effective in combination with a high fertilization rate, but we cannot conclude that a high fertilization rate is better for organic fertilizer substitution. It is known that a high mineral fertilizer rate does not increase crop yield and has a higher environmental cost [51,52]. However, a moderately higher rate of organic fertilizer substitution is associated with a greater nutrient supply that might not exceed the optimal level (because the N fertilizer replacement value of organic fertilizer is normally less than 70%) [31]. Analyzing the effect of organic fertilizer substitution without considering the fertilization rate can be misleading.

4.5. Limitations of This Study

Although we searched for articles without imposing any geographic limitations, most of the included studies (~80%) were carried out in China. This was because most of the organic fertilizer substitution experiments performed in Europe and America were based on available N [31], which did not meet our criterion that studies must be based on total N. Moreover, most studies performed in Africa did not report the N contents of organic materials accurately [15], which prevented verification that the total N application rates of the organic and mineral fertilizer treatments were equal. Additionally, we did not take the effects of organic treatment (compost or digestate) on organic fertilizer substitution into account [17] due to the limited amount of available data on maize production. Moreover, even though P and K inputs were not major factors limiting maize growth in the included articles, micronutrients present in organic materials, particularly boron (B) and zinc (Zn), may have contributed to the higher maize yields observed under the organic fertilizer treatments [39]. Since most studies did not report the micronutrients in organic materials, further research is needed to quantify their contribution to increased crop yield.

5. Conclusions

Organic fertilizer substitution significantly enhanced maize yield, reduced N losses, and promoted SOC sequestration, but also increased CO2 emissions. It had no significant effect on NUE or CH4 emissions during maize production. The yield-optimal Rs of organic N was 40−60%, but it varied by fertilization rate. The yield and environmental benefits of organic fertilizer substitution were higher with a high fertilization rate. Long-term organic fertilizer substitution further increased maize yield compared with short-term application. The GWP of organic fertilizer substitution was −116 kg CO2 eq ha−1, and the NGWP was −3507 kg CO2 eq ha−1, with partial substitution of mineral fertilizer with organic fertilizer sequestering more C than full substitution.

Author Contributions

Z.C., F.Z. and Z.W. conceived the idea. Z.C., M.Z., F.Z. supervised the project. Z.W., H.Y. and X.G. established the database. Z.W. wrote the manuscript. Z.C. and M.Z. polished the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This study was funded by Qinghai Science and Technology Plan Project (2019-NK-A11), China Scholarship Council (No. 201913043).

Acknowledgments

We are grateful to Ellis Hoffland and Petra Hellegers for supervising the project. The first author appreciates Jie Lu for helping to tackle some technical matters on using R.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Zhang, X.; Davidson, E.A.; Mauzerall, D.L.; Searchinger, T.D.; Dumas, P.; Shen, Y. Managing Nitrogen for Sustainable Development. Nature 2015, 528, 51–59. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  2. Cui, Z.L.; Yue, S.C.; Wang, G.L.; Meng, Q.F.; Wu, L.; Yang, Z.P.; Zhang, Q.; Li, S.Q.; Zhang, F.S.; Chen, X.P. Closing the Yield Gap could Reduce Projected Greenhouse Gas Emissions: A Case Study of Maize Production in China. Glob. Chang. Biol. 2013, 19, 2467–2477. [Google Scholar] [CrossRef] [PubMed]
  3. Cui, Z.L.; Zhang, H.Y.; Chen, X.P.; Zhang, C.C.; Ma, W.Q.; Huang, C.D.; Zhang, W.F.; Mi, G.H.; Miao, Y.X.; Li, X.L.; et al. Pursuing Sustainable Productivity with Millions of Smallholder Farmers. Nature 2018, 555, 363–366. [Google Scholar] [CrossRef] [PubMed]
  4. Guo, J.H.; Liu, X.J.; Zhang, Y.; Shen, J.L.; Han, W.X.; Zhang, W.F.; Christie, P.; Goulding, K.W.T.; Vitousek, P.M.; Zhang, F.S. Significant Acidification in Major Chinese Croplands. Science 2010, 327, 1008–1010. [Google Scholar] [CrossRef] [Green Version]
  5. Sutton, M.A.; Howard, C.M.; Erisman, J.W.; Billen, G.; Bleeker, A.; Grennfelt, P.; Van Grinsven, H.; Grizzetti, B. The European Nitrogen Assessment: Sources, Effects and Policy Perspectives; Cambridge University Press: Cambridge, UK, 2011. [Google Scholar]
  6. Gu, B.J.; Ju, X.T.; Chang, J.; Ge, Y.; Vitousek, P.M. Integrated Reactive Nitrogen Budgets and Future Trends in China. Proc. Natl. Acad. Sci. USA 2015. [Google Scholar] [CrossRef] [Green Version]
  7. Oenema, O.; Oudendag, D.; Velthof, G.L. Nutrient Losses from Manure Management in the European Union. Livest. Sci. 2007, 112, 261–272. [Google Scholar] [CrossRef]
  8. Bai, Z.H.; Ma, L.; Jin, S.Q.; Ma, W.Q.; Velthof, G.L.; Oenema, O.; Liu, L.; Chadwick, D.; Zhang, F.S. Nitrogen, Phosphorus, and Potassium Flows through the Manure Management Chain in China. Environ. Sci. Technol. 2016, 50, 13409–13418. [Google Scholar] [CrossRef] [Green Version]
  9. Chadwick, D.; Jia, W.; Tong, Y.A.; Yu, G.H.; Shen, Q.R.; Chen, Q. Improving Manure Nutrient Management Towards Sustainable Agricultural Intensification in China. Agric. Ecosyst. Environ. 2015, 209, 34–46. [Google Scholar] [CrossRef]
  10. Chee-Sanford, J.C.; Mackie, R.I.; Koike, S.; Krapac, I.G.; Lin, Y.F.; Yannarell, A.C.; Maxwell, S.; Aminov, R.I. Fate and Transport of Antibiotic Residues and Antibiotic Resistance Genes Following Land Application of Manure Waste. J. Environ. Qual. 2009, 38, 1086–1108. [Google Scholar] [CrossRef] [Green Version]
  11. Cobo, S.; Dominguez-Ramos, A.; Irabien, A. Minimization of Resource Consumption and Carbon Footprint of a Circular Organic Waste Valorization System. ACS Sustain. Chem. Eng. 2018, 6, 3493–3501. [Google Scholar] [CrossRef]
  12. Maillard, E.; Angers, D.A. Animal Manure Application and Soil Organic Carbon Stocks: A Meta-Analysis. Glob. Chang. Biol. 2014, 20, 666–679. [Google Scholar] [CrossRef] [PubMed]
  13. Oldfield, E.E.; Bradford, M.A.; Wood, S.A. Global Meta-Analysis of the Relationship Between Soil Organic Matter and Crop Yields. Soil 2019, 5, 15–32. [Google Scholar] [CrossRef] [Green Version]
  14. Domingo-Olivé, F.; Bosch-Serra, À.D.; Yagüe, M.R.; Poch, R.M.; Boixadera, J. Long Term Application of Dairy Cattle Manure and Pig Slurry to Winter Cereals Improves Soil Quality. Nutr. Cycl. Agroecosyst. 2016, 104, 39–51. [Google Scholar] [CrossRef] [Green Version]
  15. Chivenge, P.; Vanlauwe, B.; Six, J. Does The Combined Application of Organic and Mineral Nutrient Sources Influence Maize Productivity? A Meta Analysis. Plant Soil 2011, 342, 1–30. [Google Scholar] [CrossRef] [Green Version]
  16. Xia, L.; Lam, S.K.; Yan, X.; Chen, D. How Does Recycling of Livestock Manure in Agroecosystems Affect Crop Productivity, Reactive Nitrogen Losses, and Soil Carbon Balance? Environ. Sci. Technol. 2017, 51, 7450–7457. [Google Scholar] [CrossRef] [PubMed]
  17. Zhang, X.; Fang, Q.; Zhang, T.; Ma, W.; Velthof, G.L.; Hou, Y.; Oenema, O.; Zhang, F. Benefits and Trade-offs of Replacing Synthetic Fertilizers by Animal Manures in Crop Production in China: A Meta-Analysis. Glob. Chang. Biol. 2019. [Google Scholar] [CrossRef]
  18. Hijbeek, R.; Ittersum, M.K.V.; Berge, H.F.M.T.; Gort, G.; Spiegel, H.; Whitmore, A.P. Do Organic Inputs Matter—A Meta-Analysis of Additional Yield Effects for Arable Crops in Europe. Plant Soil 2017, 411, 293–303. [Google Scholar] [CrossRef] [Green Version]
  19. Sileshi, G.W.; Jama, B.; Vanlauwe, B.; Negassa, W.; Harawa, R.; Kiwia, A.; Kimani, D. Nutrient Use Efficiency and Crop Yield Response to the Combined Application of Cattle Manure and Inorganic Fertilizer in Sub-Saharan Africa. Nutr. Cycl. Agroecosyst. 2019, 113, 181–199. [Google Scholar] [CrossRef]
  20. Tovihoudji, P.G.; Akponikpè, P.B.I.; Adjogboto, A.; Djenontin, J.A.; Agbossou, E.K.; Bielders, C.L. Combining Hill-Placed Manure and Mineral Fertilizer Enhances Maize Productivity and Profitability in Northern Benin. Nutr. Cycl. Agroecosyst. 2018, 110, 375–393. [Google Scholar] [CrossRef]
  21. Jjagwe, J.; Chelimo, K.; Karungi, J.; Komakech, A.J.; Lederer, J. Comparative Performance of Organic Fertilizers in Maize (Zea mays L.) Growth, Yield, and Economic Results. Agronomy 2020, 10, 69. [Google Scholar] [CrossRef] [Green Version]
  22. Wu, L.Q. Fertilizer Recommendations for Three Major Cereal Crops based on Regional Fertilizer Formula and Site Specific Adjustment in China. Ph.D. Thesis, China Agricultural University, Beijing, China, 1 May 2014. (In Chinese with English Abstract). [Google Scholar]
  23. Efthimiadou, A.; Bilalis, D.; Karkanis, A.; Froudwilliams, B. Combined Organic/Inorganic Fertilization Enhance Soil Quality and Increased Yield, Photosynthesis and Sustainability of Sweet Maize Crop. Aust. J. Crop. Sci. 2010, 4, 722–729. [Google Scholar]
  24. Diez, J.A.; Hernaiz, P.; Munoz, M.J.; La Torre, A.D.; Vallejo, A. Impact of Pig Slurry on Soil Properties, Water Salinization, Nitrate Leaching and Crop Yield in a Four-Year Experiment in Central Spain. Soil Use Manag. 2004, 20, 444–450. [Google Scholar] [CrossRef] [Green Version]
  25. Hedges, L.V.; Gurevitch, J.; Curtis, P.S. The Meta-Analysis of Response Ratios in Experimental Ecology. Ecology 1999, 80, 1150–1156. [Google Scholar] [CrossRef]
  26. Liu, Q.; Liu, B.; Zhang, Y.; Hu, T.; Lin, Z.; Liu, G.; Wang, X.; Ma, J.; Wang, H.; Jin, H.; et al. Biochar Application as a Tool to Decrease Soil Nitrogen Losses (NH3 Volatilization, N2O Emissions, and N Leaching) from Croplands: Options and Mitigation Strength in a Global Perspective. Glob. Chang. Biol. 2019. [Google Scholar] [CrossRef]
  27. Ying, H.; Yin, Y.; Zheng, H.; Wang, Y.; Zhang, Q.; Xue, Y.; Stefanovski, D.; Cui, Z.; Dou, Z. Newer and Select Maize, Wheat, and Rce Varieties can Help Mitigate N Footprint While Producing More Grain. Glob. Chang. Biol. 2019. [Google Scholar] [CrossRef]
  28. Bracken, M.B. Effective Care of the Newborn Infant; Oxford University Press: Oxford, UK, 1992. [Google Scholar]
  29. Feral, J.P. IPCC, 2014—Climate Change 2014. Synthesis Report; Intergovernmental Panel on Climate Change: Geneva, Switzerland, 2015. [Google Scholar]
  30. Paustian, K.; Ravindranath, N.H.; Amstel, A.V. Agriculture, forestry and other land use. In 2006 IPCC Guidelines for National Greenhouse Gas Inventories; International Panel on Climate Change: Hayama, Japan, 2006; Volume 4. [Google Scholar]
  31. Petersen, J. Nitrogen Fertilizer Replacement Value of Sewage Sludge, Composted Household Waste and Farmyard Manure. J. Agric. Sci. 2003, 140, 169–182. [Google Scholar] [CrossRef]
  32. Pagliari, P.H.; Laboski, C.A.M. Investigation of the Inorganic and Organic Phosphorus Forms in Animal Manure. J. Environ. Qual. 2012, 41, 901–910. [Google Scholar] [CrossRef]
  33. Jia, Z.T.; Wang, W.L.; Tang, J.H.; Liu, F.; Liu, H.E.; Liu, S.L.; Han, Y.L.; Zheng, J. Effect of Animal Manure Organic Fertilizer and Nitrogen Combined Application on Maize Soil Physical & Chemical Properties. Environ. Sci. Technol. 2015, 38, 34–39, (In Chinese with English Abstract). [Google Scholar] [CrossRef]
  34. Zhai, L.; Liu, H.; Zhang, J.; Huang, J.; Wang, B. Long-Term Application of Organic Manure and Mineral Fertilizer on N2O and CO2 Emissions in a Red Soil from Cultivated Maize-Wheat Rotation in China. Agric. Sci. China 2011, 10, 1748–1757. [Google Scholar] [CrossRef]
  35. Li, C. Effects of Long-Term Fertilization on Crop Productivity and Soil Fertility as well as Its Mechanisms under Upland Red Soil in Subtropical China. Ph.D. Thesis, Nanjing Agricultural University, Nanjing, China, 1 October 2009. (In Chinese with English Abstract). [Google Scholar]
  36. Guan, J.X.; Wang, Z.Y.; Wang, B.R.; Liu, S.J. Effects of Organic Fertilizer on Red Soil Upland Maize Yield and Soil Properties. Hunan Agric. Sci. 2016, 52–54, (In Chinese with English Abstract). [Google Scholar] [CrossRef]
  37. Feng, X.; Gao, H.; Lal, R.; Zhu, P.; Peng, C.; Deng, A.; Zheng, C.; Song, Z.; Zhang, W. Nitrous Oxide Emission, Global Warming Potential, and Denitrifier Abundances as Affected by Long-Term Fertilization on Mollisols of Northeastern China. Arch. Agron. Soil Sci. 2019, 65, 1831–1844. [Google Scholar] [CrossRef]
  38. Cai, A.; Zhang, W.; Xu, M.; Wang, B.; Wen, S.; Shah, S.A.A. Soil Fertility and Crop Yield after Manure Addition to Acidic Soils in South China. Nutr. Cycl. Agroecosyst. 2018, 111, 61–72. [Google Scholar] [CrossRef]
  39. Franke, A.C.; Schulz, S.; Oyewole, B.D.; Diels, J.; Tobe, O.K. The Role of Cattle Manure in Enhancing on-farm Productivity, Macro- and Micro-nutrient Uptake, and Profitability of Maize in the Guinea Savanna. Exp. Agric. 2008, 44, 313–328. [Google Scholar] [CrossRef] [Green Version]
  40. Guo, S.; Pan, J.; Zhai, L.; Khoshnevisan, B.; Wu, S.; Wang, H.; Yang, B.; Liu, H.; Lei, B. The Reactive Nitrogen Loss and GHG Emissions from a Maize System after a Long-Term Livestock Manure Incorporation in the North China Plain. Sci. Total Environ. 2020, 720, 137558. [Google Scholar] [CrossRef]
  41. Hong, Y.; Wang, F.; Liu, R.L.; Li, Y.H.; Zhao, T.C.; Chen, C. Effects of Long-Term Fertilization on Yield and Nitrogen Utilization of Spring Maize in Irrigation Silting Soils. J. Soil Water Conserv. 2017, 31, 248–261, (In Chinese with English Abstract). [Google Scholar]
  42. Liang, B. Effect of Long-Term Combined Application of Manure and Inorganic Fertilizers on Soil Nitrogen Availability and Its Mechanism. Ph.D. Thesis, Northwest A&F University, Yanglin, China, 1 April 2012. (In Chinese with English Abstract). [Google Scholar]
  43. Lou, Y.; Wang, J.; Liang, W. Impacts of 22-Year Organic and Inorganic N Managements on Soil Organic C Fractions in a Maize Field, Northeast China. Catena 2011, 87, 386–390. [Google Scholar] [CrossRef]
  44. Zhang, X.Z.; Gao, H.J.; Peng, C.; Li, Q.; Zhu, P. Effects of Combined Application of Organic Manure and Chemical Fertilizer on Maize Yield and Nitrogen Utilization under Equal Nitrogen Rates. J. Maize Sci. 2012, 20, 123–127, (In Chinese with English Abstract). [Google Scholar]
  45. Zhang, Y.R.; Li, Y.; Liu, Y.L.; Zhang, W.A.; Jiang, T.M. Effects of Long-Term Fertilization on Soil Organic Carbon Balance and Maize Yield in Yellow Soil. Acta Pedol. Sin. 2016, 53, 1275–1285, (In Chinese with English Abstract). [Google Scholar] [CrossRef]
  46. Zhao, Y.; Yan, Z.; Qin, J.; Ma, Z.; Zhang, Y.; Zhang, L. The Potential of Residues of Furfural and Biogas as Calcareous Soil Amendments for Corn Seed Production. Environ. Sci. Technol. 2016, 23, 6217–6226. [Google Scholar] [CrossRef]
  47. Wang, X.; Zhang, L.; Zou, J.; Liu, S. Optimizing Net Greenhouse Gas Balance of a Bioenergy Cropping System in Southeast China with Urease and Nitrification Inhibitors. Ecol. Eng. 2015, 83, 191–198. [Google Scholar] [CrossRef]
  48. Crill, P.M.; Martikainen, P.J.; Nykanen, H.; Silvola, J. Temperature and N Fertilization Effects on Methane Oxidation in a Drained Peatland Soil. Soil Biol. Biochem. 1994, 26, 1331–1339. [Google Scholar] [CrossRef]
  49. Zhang, W.F.; Dou, Z.X.; He, P.; Ju, X.T.; Powlson, D.; Chadwick, D.; Norse, D.; Lu, Y.L.; Zhang, Y.; Wu, L.; et al. New Technologies Reduce Greenhouse Gas Emissions from Nitrogenous Fertilizer in China. Proc. Natl. Acad. Sci. USA 2013, 110, 8375–8380. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  50. Lin, L.; Xu, F.; Ge, X.; Li, Y. Improving the Sustainability of Organic Waste Management Practices in the Food-Energy-Water Nexus: A Comparative Review of Anaerobic Digestion and Composting. Renew. Sust. Energ. Rev. 2018, 89, 151–167. [Google Scholar] [CrossRef]
  51. Chen, X.P.; Cui, Z.L.; Fan, M.S.; Vitousek, P.; Zhao, M.; Ma, W.Q.; Wang, Z.L.; Zhang, W.J.; Yan, X.Y.; Yang, J.C.; et al. Producing More Grain with Lower Environmental Costs. Nature 2014, 514, 486–489. [Google Scholar] [CrossRef]
  52. Zhang, C.; Ju, X.; Powlson, D.; Oenema, O.; Smith, P. Nitrogen Surplus Benchmarks for Controlling N Pollution in the Main Cropping Systems of China. Environ. Sci. Technol. 2019, 53, 6678–6687. [Google Scholar] [CrossRef]
Figure 1. Effects of substitution of mineral fertilizer with organic fertilizer (under three fertilization rates; see main text for definitions of the low, optimal, and high fertilization rates) on maize yield (a) and nitrogen use efficiency (NUE) (b). Error bars represent 95% confidence intervals. Numbers in parentheses indicate the numbers of observations.
Figure 1. Effects of substitution of mineral fertilizer with organic fertilizer (under three fertilization rates; see main text for definitions of the low, optimal, and high fertilization rates) on maize yield (a) and nitrogen use efficiency (NUE) (b). Error bars represent 95% confidence intervals. Numbers in parentheses indicate the numbers of observations.
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Figure 2. Effects of organic fertilizer substitution on NH3 emissions (a), N2O emissions (b), and runoff and leaching (c) under three fertilization rates (see main text for definitions of low, optimal, and high fertilization rates). Error bars represent 95% confidence intervals. Numbers in parentheses indicate the numbers of observations.
Figure 2. Effects of organic fertilizer substitution on NH3 emissions (a), N2O emissions (b), and runoff and leaching (c) under three fertilization rates (see main text for definitions of low, optimal, and high fertilization rates). Error bars represent 95% confidence intervals. Numbers in parentheses indicate the numbers of observations.
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Figure 3. Effects of organic fertilizer substitution on CO2 emissions (a), CH4 emissions (b), and SOCSR (c) under three fertilization rates (see main text for definitions of the low, optimal, and high fertilization rates). SOCSR indicates soil organic carbon sequestration rate. Error bars represent 95% confidence intervals. Numbers in parentheses indicate the numbers of observations.
Figure 3. Effects of organic fertilizer substitution on CO2 emissions (a), CH4 emissions (b), and SOCSR (c) under three fertilization rates (see main text for definitions of the low, optimal, and high fertilization rates). SOCSR indicates soil organic carbon sequestration rate. Error bars represent 95% confidence intervals. Numbers in parentheses indicate the numbers of observations.
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Figure 4. Effects of four rates of organic fertilizer substitution on maize yield (a) and nitrogen use efficiency (NUE) (b). Rs, substitution rate, defined as organic nitrogen (N) input/total N applied (%). Error bars represent 95% confidence intervals. Numbers in parentheses indicate the numbers of observations.
Figure 4. Effects of four rates of organic fertilizer substitution on maize yield (a) and nitrogen use efficiency (NUE) (b). Rs, substitution rate, defined as organic nitrogen (N) input/total N applied (%). Error bars represent 95% confidence intervals. Numbers in parentheses indicate the numbers of observations.
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Figure 5. Effects of combined organic fertilizer substitution on maize yield (a) and nitrogen use efficiency (NUE) (b). Rs, substitution rate, defined as organic nitrogen (N) input/total N applied (%). See main text for definitions of low, optimal, and high fertilization rates. Error bars represent 95% confidence intervals. Numbers in parentheses indicate the numbers of observations.
Figure 5. Effects of combined organic fertilizer substitution on maize yield (a) and nitrogen use efficiency (NUE) (b). Rs, substitution rate, defined as organic nitrogen (N) input/total N applied (%). See main text for definitions of low, optimal, and high fertilization rates. Error bars represent 95% confidence intervals. Numbers in parentheses indicate the numbers of observations.
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Figure 6. Effects of organic fertilizer substitution on NH3 emissions (a), N2O emissions (b), and runoff and leaching (c) under four substitution rates. Rs, substitution rate, defined as organic nitrogen (N) input/total N applied (%). Error bars represent 95% confidence intervals. Numbers in parentheses indicate the numbers of observations.
Figure 6. Effects of organic fertilizer substitution on NH3 emissions (a), N2O emissions (b), and runoff and leaching (c) under four substitution rates. Rs, substitution rate, defined as organic nitrogen (N) input/total N applied (%). Error bars represent 95% confidence intervals. Numbers in parentheses indicate the numbers of observations.
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Figure 7. Effects of organic fertilizer substitution on CO2 emissions (a), CH4 emissions (b), and the soil organic carbon sequestration rate (SOCSR) (c) for maize production under four substitution rates. Rs, substitution rate, defined as organic nitrogen (N) input/total N applied (%). Error bars represent 95% confidence intervals. Numbers in parentheses indicate the numbers of observations.
Figure 7. Effects of organic fertilizer substitution on CO2 emissions (a), CH4 emissions (b), and the soil organic carbon sequestration rate (SOCSR) (c) for maize production under four substitution rates. Rs, substitution rate, defined as organic nitrogen (N) input/total N applied (%). Error bars represent 95% confidence intervals. Numbers in parentheses indicate the numbers of observations.
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Figure 8. Effects of organic fertilizer substitution on maize yield and nitrogen use efficiency (NUE) (a), nitrogen (N) losses (b), CO2 emissions (c), and CH4 emissions (d) under two treatment durations (short: <3 years, long: ≥3 years). N losses include NH3 emissions, N2O emissions, and runoff and leaching. Error bars represent 95% confidence intervals. Numbers in parentheses indicate the numbers of observations.
Figure 8. Effects of organic fertilizer substitution on maize yield and nitrogen use efficiency (NUE) (a), nitrogen (N) losses (b), CO2 emissions (c), and CH4 emissions (d) under two treatment durations (short: <3 years, long: ≥3 years). N losses include NH3 emissions, N2O emissions, and runoff and leaching. Error bars represent 95% confidence intervals. Numbers in parentheses indicate the numbers of observations.
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Table 1. Net global warming potential parameter values according to organic fertilizer substitution amount.
Table 1. Net global warming potential parameter values according to organic fertilizer substitution amount.
ParameterOverallFull SubstitutionPartial Substitution
NH3 (kg N ha−1)−14.6−31.6−4.13
N2O (kg N ha−1)−0.06−0.05−0.05
Leaching/runoff (kg N ha−1)−5.63−13.5−2.15
CH4 (kg C ha−1)0.000.52−0.47
SOCSR (kg C ha−1 yr−1)925817968
GWP (kg CO2 eq ha−1)−116−203−67.2
NGWP (kg CO2 eq ha−1)−3507−3200−3617
SOCSR, soil organic carbon sequestration rate; GWP, global warming potential; NGWP, net global warming potential; Negative NGWP values indicate a net carbon sink as a result of organic fertilizer substitution.
Table 2. Effect of chemical and organic fertilizers on soil properties.
Table 2. Effect of chemical and organic fertilizers on soil properties.
Soil PropertyControlMineral FertilizerOrganic Fertilizer
MeanSDnMeanSDnMeanSDn
SOC (g kg−1) [20,34,35,36,37,38,39,40,41,42,43,44,45,46] 9.692.162210.372.873013.284.3830
TN (g kg−1) [34,35,37,38,39,41,42,44,46]1.090.15141.100.26191.290.3619
pH [34,35,37,38,39,41,44,46]7.681.12136.471.66186.771.2718
BD (g cm−3) [36,41,46]1.350.0981.320.10111.260.0511
All data were from long-term experiments (≥3 years). SOC, soil organic carbon; TN, soil total nitrogen; BD, soil bulk density; SD, standard deviation.

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Wei, Z.; Ying, H.; Guo, X.; Zhuang, M.; Cui, Z.; Zhang, F. Substitution of Mineral Fertilizer with Organic Fertilizer in Maize Systems: A Meta-Analysis of Reduced Nitrogen and Carbon Emissions. Agronomy 2020, 10, 1149. https://doi.org/10.3390/agronomy10081149

AMA Style

Wei Z, Ying H, Guo X, Zhuang M, Cui Z, Zhang F. Substitution of Mineral Fertilizer with Organic Fertilizer in Maize Systems: A Meta-Analysis of Reduced Nitrogen and Carbon Emissions. Agronomy. 2020; 10(8):1149. https://doi.org/10.3390/agronomy10081149

Chicago/Turabian Style

Wei, Zhibiao, Hao Ying, Xiaowei Guo, Minghao Zhuang, Zhenling Cui, and Fusuo Zhang. 2020. "Substitution of Mineral Fertilizer with Organic Fertilizer in Maize Systems: A Meta-Analysis of Reduced Nitrogen and Carbon Emissions" Agronomy 10, no. 8: 1149. https://doi.org/10.3390/agronomy10081149

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