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Net nitrogen mineralization delay due to microbial regulation following the addition of granular organic fertilizer
Geoderma 359 (2020) 113994
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Net nitrogen mineralization delay due to microbial regulation following the addition of granular organic fertilizer
T
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Xinyi Yanga, Guitong Lia, , Xiaohong Jiab, Xiaorong Zhaoa, Qimei Lina a Department of Soil and Water Science, College of Land Science and Technology, China Agricultural University, No. 2 West Road of Yuanmingyuan, Haidian, Beijing 100193, PR China b Beijing Soil & Fertilizer Extension Service Center, No. 6 Yumin Zhong Road, Xicheng, Beijing 100029, PR China
A R T I C LE I N FO
A B S T R A C T
Handling Editor: Junhong Bai
The transformation processes and fate of nitrogen (N) in organic fertilizer are particularly important for N supply to crop in agricultural soils. However, the dynamic of the N release process of granular organic fertilizer to soil is not as clear as that of the powdery form. In this study, granular (G) and powdery (P) forms of a manure compost, which were well mixed with maize straw powders (MS) in 5% or 15%, respectively, were applied to soil and incubated for 105 days. The differences in soil N mineralization-immobilization turnover (N-MIT) between the two forms were compared. Our results showed that, 1) soil mineral N content was similar in the two soil mixtures at day 105 (the end of the incubation), while granules released more mineral N after day 45; 2) granulizing the powdery mixtures of MS and mature compost released more N from the fresh MS than those in the powdery form; and 3) structural equation model indicated that divers of the microbial N transformation in the granules amended soil were significantly different from that in the powdery form amended soil. In terms of N management in crop production, our results suggest that granular organic fertilizer could delay N release for about 1 month, which may reduce N loss risk during crop seedling stage and increase soil N supply during the rapid growth period of most crops. We therefore propose that making organic fertilizer into granules is a hopeful way to synchronize fertilizer N release to the maximal uptake of crops, which improve N use efficiency and alleviate the negative impact on environment.
Keywords: Organic fertilizer form 15 N labeling N mineralization Structural equation model
1. Introduction Nitrogen (N) is a main limiting factor for crop production in agricultural ecosystems, and one optimal organic N fertility management practice was determined by the extent of soil N supply fitting with crop demand (Reganold and Wachter, 2016). The application of organic fertilizer (OF), such as poultry manure, crop straws and their compost products, can increase crop yield, improve soil quality, and alleviate greenhouse gas emissions as well (Bodirsky et al., 2014; Gu et al., 2015). The bio-availability of N in OF is the result of the mineralizationimmobilization turnover (MIT) process of N-containing components , and application method is one of the main factors affecting the MIT process. Currently, the common way to apply OF is to incorporate with the form of small powders (smaller than 1 mm) into soil, and then mix them well to evenly distribute them among soil matrix. The advantage of this method is the evenly distributed nutrient that making roots more chance to contact. However, this powder form maybe not suitable for the adjustment of C:N ratio using two or more materials, as the different
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kinds of powders separately existed among microsites, and the un-intertouched powders could not contact with each other and the C:N ratio adjustment fail (Singh et al., 2007; Stieglmeier et al., 2014). Alternatively, applying OF in locally-concentrated forms (such as in granule, pellet, or tablet, etc.) will give another story of MIT. Generally, pelletized materials released more inorganic N than that in powder form under the same condition (Hadas et al., 1983). Meanwhile, the bigger physical forms reduce the specific contact area between OF and soil matrix, making NH4+ and NO3− a slow release to the surrounding soil (Cox, 1995; Rao et al., 2007). However, all the above effects were integrative effect of the mixture of pellets and soil. What happened in the MIT process within the pellets was not known at all. N-rich organic matter such as manure and legume crop residues and C-rich organic matter such as most crop residues are often mixed to get a suitable C:N ratio for rapid decomposition and N release (Berglund and Ågren, 2012; Harguindeguy et al., 2008; Redin et al., 2014), but the mixing effect can be synergistic (Singh et al., 2007), antagonistic, or additive (Stieglmeier et al., 2014). The main reason for this contradicts
Corresponding author. E-mail address: [email protected] (G. Li).
https://doi.org/10.1016/j.geoderma.2019.113994 Received 22 January 2019; Received in revised form 24 September 2019; Accepted 26 September 2019 0016-7061/ © 2019 Elsevier B.V. All rights reserved.
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treatment. To set up the incubation, a modified device was used (Fig. S1). For 5-G and 15-G treatments, granules were put into the middle of Box b, and surrounded by incubated soil B. According to the designed size of box b, the surrounding soil B was within 1 cm to the granule surface, and separated by the mesh (1.5 mm in diameter). When the 14 granules were put into the middle soil layer (soil B and C), the N application rate of 165 mg kg−1 was reached. To protect the incubated soil, two soil layers, 5 cm soil layer on the above and 10 cm soil layer under the bottom of the middle layer (Fig. S1), were used and separated by nylon net (to be easily moved). All soil used was the same soil with the same water content of 60% of Water holding Capacity (WHC) of the soil and filled with bulk density of 1.4 g cm−3. For 5-P and 15-P treatments, operation was same as that in 5-G and 15-G treatments, except for putting mixture of MS and OF powders in the middle layer. After all replications (21 replications for each treatment) were prepared, each replication was put into a 3000 ml plastic jar and the incubation started under 25 °C and dark condition. During the 105 days incubation, water content of the soil–OF mixture was adjusted by dropping the required amount of deionized water when the loss was greater than 0.05 g (Fig. S1). The other replications (18 for each treatment) were used for sampling soil and fertilizer granules on days 5, 15, 30, 45, 75 and 105. Three replications were destroyed for sampling at each sampling time. To do the sampling, the 5 cm protect soil layer was first removed by picking up the nylon net a. Then fertilizer granules were picked out from the soil B by tweezers in the 5-G and 15-G treatments (Fig. S1) and all soil B in each replication were thoroughly mixed to make a composted sample. Meanwhile, all fertilizer granules in each replication were mixed together to make a composted sample. In the 5-G and 15-G treatment, samples of soil B and fertilizer granules were analyzed separately. In the 5-P and 15-P treatments, the mixture of soil and fertilizer powders in the middle layer (including soil C) were sampled and measured.
result maybe lie in the fact that the single particles of different materials were dispersed among the soil matrix and actually did not interact each other. In other words, the adjustment of C:N ratio was failed. Then the final N release process was just a simple sum of various materials without any or less interaction. This spatial separation between the different types of materials is just the distribution pattern for the powdery OF application to soil. On the other hand, if two or more materials are mixed into a granular, i.e. into a tight combination of “N” and “C” materials, the real C:N ratio will be obtained and a new MIT will be created. N supply from granular OF may preferentially mineralize in the interior of the granule and then gradually release N into the surrounding soil, thus the peak of soil N supply could be delayed. Of course, smaller contact area of granular fertilizer also slows down the release of N. From this, we can expect a new MIT process of N in the granular OF applied to soil. In this study, we made granular OF by mixing powders of composted cow manure and fresh maize straw (MS) with 5% and 15%. Then we incubated these granules and those powders mixtures with soil for 105 days, respectively. The objectives of the experiment were: 1) to clarify the different patterns of N release between the powdery and granular forms of OF; 2) to explore the MIT process happened in the OF granular; and 3) to explain the difference in N transformation between the powdery and granular forms. 2. Materials and methods 2.1. Soil and organic material Soil was collected from the upper layers (0–15 cm) of a Fluvisol (FAO system), which grown winter wheat and summer maize for many years. The fresh soil was thoroughly mixed, sieved (< 2 mm) and stored at 25 °C for 1 week before used. Fresh maize straw powder (< 2 mm) used in this experiment was derived from a 15N-labeled corn leaves. Fresh cow manure and ammonium sulfate were co-composted for 90 days and the product was made into < 2 mm powders (OF). Basic properties of soil and organic materials are shown in Table 1.
2.3. Analysis method Total N and organic C concentrations of the OF and soil samples were determined by dry combustion using an Elementary CN Analyzer (elemental analyzer vario PYRO cube). To determine NH4+ and NO3− concentrations and their stable isotope ratio (δ15N), incubated soil samples and original samples were extracted with a 0.5 mol L−1 K2SO4 solution at a 1:5 (w/v) soil to extracting ratio. The samples were shaken at 250 rpm on a mechanical shaker for 1 h before being filtered through Whatman No. 42 filter papers. We used the NH3-diffusion technique (Holmes et al., 1998; Sigman et al., 1997) to determine the 15N natural abundance of NO3− and NH4+. Ammonium was diffused as NH3 after addition of MgO, while NO3− was reduced by adding Devarda’s alloy and subsequently diffused as NH3 onto a second filter. Each diffusion step was conducted at 35 °C under continuous shaking for 7 days. Pure KCl (1 M) solution was added to make standard 90 ml solutions. Standard NH4+ and NO3− solutions were analyzed using the same procedures and showed δ15N values within 0.2% of their expected values. Previous findings by Holmes et al. (1998) indicated that volumes less than 200 ml recorded accurate diffusion of N standards. For our analysis, samples were analyzed for 15N using a stable isotope ratio mass spectrometer (Isoprime 100) linked to a CN analyzer (elemental analyzer vario PYRO cube). Microbial biomass C (MBC) and N (MBN) were determined using chloroform fumigation extraction (Jenkinson et al., 2004). Fresh samples were fumigated with ethanol-free chloroform for 24 h in an evacuated desiccator. Fumigated and unfumigated samples were extracted with 0.5 mol L−1 K2SO4 solutions at a 1:10 (w/v) soil to potassium sulfate solution ratio and filtered using Whatman No. 42 filter papers. Chloroform (CHCl3) fumigation-extraction method was employed to estimate the amount of MBN and MBC by using the equation:
2.2. Experiment design and sampling The incubation experiment included 5 treatments: 1) 5% MS + 95% OF, in powdery form (5-P); 2) 15% MS + 85% OF, in powdery form (15-P); 3) 5% MS + 95% OF, in granular form (5-G); 4) 15% MS + 85% OF, in granular (15-G); and 5) a control treatment (CK). The 5% and 15% were the ratio of N in the maize straw to the total N in the mixture of MS and OF. To make granular form, moist powders (water mass content 30%) of MS and OF were thoroughly mixed, then inserted into cylinders (made with wire mesh) which diameter and height was 1 cm respectively (Fig. S1). Each cylinder (fertilizer granule) was filled with 0.964 g (calculated dry weight) of powdery mixture. According to the application rate of N, 14 granules were added to each replication in the 5-G and 15-G Table 1 The basic properties of the soil and organic material. Items
Soil
Sand (> 0.05 mm), g kg−1 Silt (0.05–0.02 mm), g kg−1 Clay (< 0.02 mm), g kg−1 Organic C, g kg−1 Total N, g kg−1 15 N, atom% NH4+-N, mg kg−1 NO3–-N, mg kg−1
280 ± 14.00
Maize straw
Organic fertilizer
44.14 ± 5.21 1.51 ± 0.03 1.25 ± 0.01 341.11 ± 21.46 172.34 ± 12.12
24.52 ± 1.41 4.80 ± 0.32 0.37 ± 0.01 584.56 ± 34.53 263.78 ± 22.08
520 ± 26.00 200 ± 10.00 4.32 ± 0.08 0.82 ± 0.02 0.37 ± 0.01 15.32 ± 0.61 16.38 ± 3.07
2
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Fig. 1. The dynamics of NH4+-N and NO3−-N contents during the 105-days incubation. (a) and (b) are the NH4+-N and NO3−-N content in the soil mixtures of the 5 treatments, respectively; (c) and (d) are the NH4+-N and NO3−-N content in the surrounding soils and OF granules in the G treatments, respectively. Error bars show the standard error of the mean of each treatment (n = 9). In some cases, error bars are smaller than the symbols.
Glucosidase activity was measured according to Ekenler and Tabatabai (2003) and protease activity was analyzed following the method of Geisseler and Horwath (2008). All measurements were undertaken in triplicate from the independent replications. N transformation was calculated as the net N mineralization rate (Nmin), where Nmin (mg N kg−1 d−1) was calculated by divided the difference in mineral N between start and end of each period with the duration in the day. Extractable NH4+-N and NO3−-N (Mineral N) was determined calorimetrically on an auto–analyzer (AA3, Bran & Luebbe, Germany).
MBN = EN/KEN and MBC = EC/KEC, where EN and EC are the N and C extracted by 0.5 M K2SO4 from fumigated soil minus that extracted from non-fumigated soil, and KEN and KEC are the conversion factors for MBN (0.68) (Brookes et al., 1985) and MBC (0.35) (Voroney et al., 1991). To measure δ15N in MBN, freeze-drying method was used to get the measuring samples from the extracts of fumigated and non-fumigated. The 15N samples were prepared using a method proposed by Shen et al. (1984), and 15N/14N ratio was measured by a stable isotoperatio mass spectrometer (Isoprime 100). The mass of maize-derived N and 15N recovery in different N pools were calculated according to the Eq. (1) and Eq. (2), and the 15N at.% excess was corrected for the corresponding background abundance.
MAB
P I = B B IA
2.4. Statistical analysis Multiple comparisons of N components and enzyme activity among different treatments were performed by LSD method, while repeated variance analysis was performed for sampling time, fertilization method and ratio, and statistical analysis was performed by SPSS 20.0. Structural equation modeling (SEM) was used to disentangle direct and indirect effects of P and G treatment, soil physicochemical properties, the ratio of substrate C and N and enzyme activities on soil mineral N by using AMOS PFtware (IBM SPSS AMOS 20.0.0). Prior to modeling, all data were normalized (ensuring all data in a standard normal distribution with a mean value of 0 and standard deviation of 1) and an a priori model was established based on the known effects and relationships among the drivers that had a significant effect on soil mineral N in previous analysis (Doncaster, 2010). SEM was employed instead of multiple regressions because directions can be assigned to several relationships, resulting in multiple explanatory as well as multiple response variables in one model (Doncaster, 2010). Furthermore, the structure of such a model can reveal whether a significant bivariate relationship occurs due to a significant relationship between two given variables and a third variable. The following criteria were used to evaluate the fit of the models: The root mean squared error of
(1)
where MAB is the maize-derived N in a given N pool (mg kg−1); IA is the 15 N at.% excess of maize, PB is the N mass of the given N pool (mg kg−1); and IB is the 15N at.% excess of the given N pool. 15N
recovery = 100 15
PB IB PA IA
(2) 15
where N recovery is the N recovered in a given N pool (%); PA is the application rate of maize-derived N (Dawson et al., 2002). Extractable C and N were determined using a vario TOC select analyzer (Elementar, Germany). Extractable C in the unfumigated samples was used to represent DOC. DON was calculated as the difference between the extractable N and the sum of NH4+-N and NO3−-N in the un-fumigated samples. Extracellular enzyme activities (β-glucosidase, protease and dehydrogenase) were determined using the following methods. Dehydrogenase activity was assayed through colorimetric determination of triphenyl formazan formed when soils were incubated with 2, 3, 5-triphenyltetrazolium chloride at 37 °C for 24 h (Moldenke, 1994). Β3
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approximation (RMSEA; the model has a good fit when RMSEA is low (< 0.05)), chi–square value (CHI/DF; the model has a good fit when CHI/DF is low), Fisher's P statistic (the model has a good fit when 0.05 < P ≤ 1.00) and the Akaike information criterion (AIC; the model has a good fit when AIC is low) (Schermelleh-Engel et al., 2003).
Although MBN and MBC of the soil mixture in G treatments were higher than that in P treatments after day 45, they were distributed differently, even in P treatments and concentrated in granules in G treatments. 3.3. Factors of soil N mineralization
3. Results SEM was used to explore the direct and indirect effects of the powdery and granular OF application forms on soil mineral N dynamics through net N mineralization (Fig. 3). Parameters in the SEM included OF parameters (C:N, enzyme activities, DON, and MBN) and soil properties (C:N, enzyme activities, MBN, DON and net N mineralization (Table S1)). In total, 32% and 29% of the soil mineral N in the P and G treatments could be explained by these parameters (Fig. 3). When OF applied in powdery form, soil mineral N dynamics was driven by a clear way which made up by a set of steps: C:N ratio of OF determined enzyme activities, then the DOC/DON ratio and the net N mineralization (Fig. 3a). Here the microbial biomass (MBN) was not a determined factor. However, the driven process of soil mineral N in the granulesamended soil was totally different (Fig. 3b). Two processes occurred under this condition, in granules first and then in the surrounding soil. In granules, both C:N ratio of OF and MBN equally important to the enzyme activities, then the enzyme activities determined the DON concentration. After the DON diffused into the surrounding soil, it positively determined the C:N ratio of the soil and the MBN. But only MBN positively determined the enzyme activities in soil, and then enzyme activities positively determined the net N mineralization. There were three aspects were difference between the powdery form and the granular form, that the MBN was important for the enzyme activities both in the granules and in the corresponding surrounded soil, but not related the enzyme activities in the powdery form; that net N mineralization was determined by the DOC/DON ratio in the powdery form, but by the enzyme activities in the granular form; and that DON was the linking pool between the granules and the surrounding soil.
3.1. Mineral N Dynamics of NH4+ and NO3− in the soil mixture showed different patterns between the powdery and granular forms of OF application (Fig. 1a and b). The NH4+ in the soil mixture rapidly increased after the powders addition at day 0 and peaked at day 15, then decreased rapidly to day 75 and un-changed to day 105. But for 5-G and 15-G, NH4+ remained the same level through the 105-day incubation. After day 45, NH4+ in G treatments were always higher than that in P treatments, and ending at ca. 40 mg kg−1 in G treatments and ca. 15 mg kg−1 in P treatments (which was also same as in CK), respectively. At day 15, NH4+ in 5-P peaked at 116 mg kg−1 whereas in 15-P it was only 86 mg kg−1. For NO3−, powdery form application increased the NO3− content quickly and peaked at day 30, then kept constant till the end of the incubation. But for G treatments, the NO3− content increased gradually till day 75, then kept constant to the end. At the end of the incubation, NO3− was ca. 160 mg kg−1 and ca. 120 mg kg−1 in P and G treatments, respectively, all significantly higher than that in the CK. For granular application, dynamics of NH4+ and NO3− in granules and the surrounding soil were shown in Fig. 1c and d. NH4+ contents in granules decreased from ca. 550 mg kg−1 just after the granules addition at day 0 to ca. 210 mg kg−1 at day 105 (Fig. 1c). Meanwhile, NO3− in granules increased correspondingly from ca. 250 mg kg−1 at day 0 to ca. 590 mg kg−1 at day 105 (Fig. 1d). Influenced by the granules, the surrounding soil got more NH4+ and NO3− (Fig. 1c and d). At the end of the incubation, the extra mineral N in the soil mixture (the sum of NH4+-N and NO3−-N in treatments minus that in CK) was ca.120 mg kg−1 and ca 110 mg kg−1 in P and G treatments, respectively, meaning no difference in the apparent net N mineralization between the two OF application forms. But the N distribution pattern was different, evenly distributed in P treatments and concentrated distributed in granules in G treatments.
3.4. Transformation of N in maize straw The N in the 15N-labeled maize straw transformed into NH4+, NO3−, DON and MBN during the incubation (Fig. S2), and the total recovery ratios into these 4 pools could be found in Table 2. The total N recovered in the 4 pools was 80.3% and 27.5% after 105 days incubation in 5-G and 15-G treatments, respectively, about 2 times higher than the 44.7% and 14.5% in 5-P and 15-P treatments (Table 2), indicating that applied OF in granular form increased its N transformation. Meanwhile, the more maize straw added, the less proportion of transformed N during the incubation. For granular form, although more the transformed N located in the granules, a small proportion of the transformed N moved into the surrounding soil.
3.2. Microbial biomass C and N There were significant differences of MBN and MBC dynamics in the soil mixture between the powdery and granular forms of OF application (Fig. 2a and b). For MBN, firstly it rapidly increased after the powders addition at day 0 and peaked at day 15, then decreased rapidly to day 45 and slowly to day 105. But for 5-G and 15-G, MBN kept constant till day 30, then increased till day 75, and kept stable to the end of the incubation (Fig. 2a). Secondly, after day 45, MBN in G treatments were always higher than that in P treatments, and ending at ca. 65 mg kg−1 in G treatments and ca. 25 mg kg−1 in P treatments (which was also higher than that in CK), respectively. Thirdly, at day 15, MBN in 5-P and 15-P peaked at the same value, ca 110 mg kg−1. In general, dynamics of MBC were nearly as same as that of MBN (Fig. 2a and b). At the end of the incubation, MBC was ca. 90 mg kg−1 and ca. 35 mg kg−1 in G and P treatments, respectively, all significantly higher than that in the CK. For granular application, dynamics of MBN and MBC in granules and the surrounding soil were shown in Fig. 2c and d. MBN contents in granules kept constant till day 45, then increased rapidly till day 75, and kept constant again (Fig. 2c). On the other hand, MBC in granules increased rapidly till day 45, and then slowly to the end of the incubation (Fig. 2d). In the surrounding soil, MBN and MBC kept constant till day 45, then increased rapidly till day 75. After day 75, MBN kept constant while MBC decreased (Fig. 2c and d).
4. Discussion 4.1. Difference in N transformation between the two application methods After 105-days incubation, no difference in mineral N of soil mixture (120 vs 110 mg kg−1) between the powdery and the granular forms (Fig. 1a and b), indicating that these two OF application forms provided similar amount of soil mineral N during the experimental period. This was similar with some of the previous studies (Hadas et al., 1983; Cabrera et al., 1994), but different to the study which fresh (but not well composted) poultry litter used (Reiter et al., 2014). Meanwhile, more NH4+-N, ca 25 mg kg−1, presented in the soil mixtures amended with granular OF, consisted with the previous studies (Hadas et al., 1983; Reiter et al., 2014). This more NH4+ would be favorable to plants which prefer to use NH4+ form of the mineral N as plant uptake. The C:N ratios in powders-amended soil mixture and in granules were 6.1–6.9:1 and 6.5–7.6:1, respectively. They were similar and less 4
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Fig. 2. The dynamics of MBN and MBC contents during the 105-days incubation. (a) and (b) are the MBN and MBC contents in the soil mixtures of the 5 treatments, respectively; (c) and (d) are the MBN and MBC contents in the surrounding soils and OF granules of the G treatments. Error bars show the standard error of the mean of each treatment (n = 9). In some cases, error bars are smaller than the symbols.
Fig. 3. Possible effects of changes in soil mineral N driven by properties of soil and OF and N components. (a) Powdery treatments (5-P and 15-P) and (b) Granular treatments (5-G and 15-G). The “Fer” in (b) represents the OF, and the “soil” in (b) represents the “surrounding soil”. The width of the arrows is proportional to the strength of the path coefficients adjacent with numbers. Solid and dashed lines represent positive and negative paths, respectively. The R2 denotes the proportion of variance that could be explained by the corresponding variable in the structural equation model. Significance levels are as follows: *p < 0.05, **p < 0.01 and ***p < 0.001. Goodness-of-fit statistics are shown underneath the modeling frames. Nmin: net N mineralization.
5
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Table 2 The total N recovery (%) of the Day (d)
Soil mixtures 5-P
5 15 30 45 75 105
N-labeled maize straw in the pools of NH4+, NO3−, MBN and DON.
15
51.1 74.8 63.8 49.1 44.8 44.7
Surrounding soils 15-P
± ± ± ± ± ±
2.6 3.7 3.2 2.5 2.2 2.2
17.7 23.3 18.9 16.5 15.2 14.5
5-G ± ± ± ± ± ±
0.9 1.2 1.0 0.8 0.8 0.7
68.8 68.7 71.1 71.4 86.4 80.3
15-G ± ± ± ± ± ±
4.1 4.1 4.3 4.3 5.2 4.8
22.1 26.0 25.8 26.5 30.7 27.5
5-G ± ± ± ± ± ±
1.1 1.3 1.3 1.3 1.5 1.4
19.0 21.9 21.2 20.4 19.7 17.7
± ± ± ± ± ±
1.0 1.1 1.1 1.0 1.0 0.9
OF granules 15-G
5-G
3.1 ± 0.2 4.1 ± 0.2 4.7 ± 0.2 6.1 ± 0.3 11.0 ± 0.6 9.8 ± 0.5
60.4 55.9 54.2 51.3 52.2 48.6
15-G ± ± ± ± ± ±
3.0 2.8 2.7 2.6 2.6 2.4
8.4 ± 0.4 12.8 ± 0.6 17.0 ± 0.9 20.1 ± 1.0 34.2 ± 1.7 31.7 ± 1.6
4.2. Potential mechanism for the difference between different OM form
than the typical C:N ratio of 25:1, meaning net N mineralization occurred (Norton and Schimel, 2011), especially during the early period of incubation. In fact, these similar C:N ratios in the powders-amended soil mixtures and the granules gave out nearly the same amount of net N mineralization during the first 15 days (Fig. 1). But in the granules, ca 200 mg kg−1 DON lost during the first 15 days, whereas only ca 20 mg kg−1 DON lost in the powders-amended soil mixture (Fig. S3a and c). The minor loss of DON in the powders-amended soil mixture meant that more un-dissolved organic N (other than the original DON) mineralized during the first 15 days, which showed the powdery OF caused more stable organic N to be mineralized in the soil mixture than that in the granules. In granules-amended soil mixture, the NH4+-N, NO3−-N, DON, and MBN distributed un-evenly. Concentrations of these N forms was about 36, 21, 7, and 22 times higher in the granules than those in the surrounding soil during the first 15 days (Figs. 1c, d, 2c and Fig. S3c). Surprisingly, although MBN in granules was higher than that in the powders-amended soil mixtures (5-P and 15-P), they did not increase rapidly during the first 15 days as expected. This may be due to the relatively lack of r-type microorganisms in the granules than that in the soil, as k-type microorganisms was more dominant in the mature compost (Meng et al., 2019; Silva et al., 2016) and also could be due to the low relative water content (30%) in the OF granules, because the water potential of this water content for the composted material and fresh maize straw was too low for an active microbial growth (Da Silva et al., 2016; Miller, 1989; Sinegani and Maghsoudi, 2011). Additionally, in powders-amended soil mixtures (5-P and 15-P), although the water content of the OF powders was also 30%, the small powders and the big surface area made the powders quickly contact to the soil matrix and then water moved into the powders, because the water potential of the soil matrix, 60% of WHC, was much higher than the water potential of the powders (Miller, 1989). This made an increase of MBN in powders-amended soil mixtures before day 15 (Fig. 2a). But for the later period of the incubation (day 45 to day 105), MBN in granules increased rapidly while decreased slowly in the powders-amended soil mixtures. The enzyme activities in granules were similar with that in the powders-amended soil mixtures during the first 15 days of incubation, but much higher afterwards (Fig. S4), becoming hotspot of the microbial activity in the soil mixture (Kuzyakov and Blagodatskaya, 2015). These higher enzyme activities after day 30, especially the protease (Fig. S4c), directly co-related to the decrease of DON and DOC (Fig. S3c and d) and the increase of MBN and MBC (Fig. 2c and d) in the granules. Meanwhile, with more DON and DOC mineralized into the surrounding soil (Fig. S3c and d), MBN and MBC increased (Fig. 2c and d), resulting in an increase in enzyme activities (Fig. S4), and then an increase in mineral N in the surrounding soil (Fig. 1c and d). Therefore, in the granular OF application way, the N transformation started first within the granules and then transmitted to the surrounding soil via DON (Fig. 3).
Powdery OF rapidly increased the NH4+ and NO3− contents in the soil mixture than granular OF did (Fig. 1a and b), which was similar with the previous researches (Cabrera et al., 1994; Hadas et al., 1983). The common reason for this difference was attributed to the large surface area of powdery OF and the slow diffusion of organic N out of the OF pellets (Cabrera et al., 1994; Hadas et al., 1983), hinting that organic N must be contacted to soil microorganism to be mineralized. However, this conclusion was just based on the experiment in which NH4+, NO3− and DON contents in the pellets were not measured (Hadas et al., 1983). In the current study, we measured them in the pellets. Results showed that high concentration of NH4+ and NO3− existed in the pellets during the first 15 days (Fig. 1c and d). Most importantly, net N mineralization occurred (the sum of NH4+-N and NO3−-N increased in Fig. 1c and d) in the pellets. In fact, if we take the soil mixture as the whole calculation base of soil mineral N content, the pellet surface was not the reason for the difference in mineral N content between the soil mixtures amended with powdery or granular OF, because NH4+-N and NO3−-N both in pellets and their surrounding soil are included in the calculation. For organic N, we measured the DON in the pellets and the surrounding soil (Fig. S3c). There was high DON in the pellets, and more importantly, this DON decreased rapidly during the first 15 days, indicating a net N mineralization occurred (Fig. S3c). Therefore, DON in the pellets cannot be diffused to the surrounding soil to be mineralized, and it could be mineralized within the pellets. As a result, the difference in surface area between the powdery and granular OF and the less diffusion of organic N out of the pellets seemed not directly related to the difference in mineral N between the soil mixtures amended with powdery or granular OF during the first 15 days of the incubation. Based on the above analysis, we attributed the reason for this difference to the difference in microbial transformation of N between the soil mixtures amended with powdery or granular OF. In powdersamended soil mixture, soil mineral N increased ca 120–210 mg kg−1 (Fig. 1a and b) and soil MBN increased ca 60 mg kg−1 (Fig. 2a) before day 15, but in the granules amended soil mixture only soil mineral N increased ca 60 mg kg−1 (Fig. 1c and d). This meant that the net N mineralization processes in the two soil mixtures were nearly the same, but microbial N immobilization (MNI) occurred in the powdersamended soil mixture and no MNI in the granules-amended soil mixture. The comparative net N mineralization in the two soil mixtures could also be proofed by the similar proteinase activity on day 15 (Fig. Scc). Based on the MIT theory (Norton and Schimel, 2011), the similar net N mineralization and the difference in microbial immobilization meant that difference in gross N mineralization existed between the two mixtures. Conditions for N transformation in granules were totally different with that in the powders-amended soil mixture. Firstly, the microbial community was mostly from the mature compost, which was significantly different with those from soil (Gattinger et al., 2004; Xu et al., 2019); Secondly, available C and N sources were relatively rich and contacted each other in space, more easy for microorganism to get 6
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(Agrawal et al., 2015; Webster et al., 1997); and thirdly, concentrations of substrate (DON) and products (NH4+ and NO3−) of organic N mineralization process were very high, which had strong feedback effects (positive or negative) on the MIT process. With the high concentrations of DON (Fig. S3cFig. S3c) and microbial biomass (Fig. 2c and d) in the granules, organic N mineralization was just determined by the enzyme activities as the substrate and microbial driver were not the limited factors for the mineralization in the granules (Fig. 3b). General speaking, making OF into granules would increase OF producing cost (Zafari and Kianmehr, 2014; Ikenganyia et al., 2015). But if we want to improve OF’s fertilizer value (especially for N), or to synchronize the N supply and crop absorb under only OF applied condition (Singh et al., 2007; Loecke et al., 2012; St. Luce et al., 2016), granulizing or pelleting the original compost product could be a good choice.
Da Silva, A.M.F., Boukhdoud, N., Gros, R., 2016. Distance from the sea as a driving force of microbial communities under water potential stresses in litters of two typical Mediterranean plant species. Geoderma 269, 1–9. Dawson, T.E., Mambelli, S., Plamboeck, A.H., Templer, P.H., Tu, K.P., 2002. Stable isotopes in plant ecology. Annu. Rev. Ecol. Syst. 33, 507–559. Doncaster, C.P., 2010. Structural equation modeling and natural systems. Fish Fish. 8, 368–369. Ekenler, M., Tabatabai, M.A., 2003. Effects of liming and tillage systems on microbial biomass and glycosidases in soils. Biol. Fert. Soils 39, 51–61. Gattinger, A., Bausenwein, U., Bruns, C., 2004. Microbial biomass and activity in composts of different composition and age. J. Plant Nutr. Soil Sci. 167, 556–561. Geisseler, D., Horwath, W.R., 2008. Regulation of extracellular protease activity in soil in response to different sources and concentrations of nitrogen and carbon. Soil Biol. Biochem. 40, 3040–3048. Gu, B., Ju, X., Chang, J., Ge, Y., Vitousek, P.M., 2015. Integrated reactive nitrogen budgets and future trends in China. Proc. Natl. Acad. Sci. U.S.A. 112, 8792. Hadas, A., Bar-Yosef, B., Davidov, S., Sofer, M., 1983. Effect of pelleting, temperature, and soil type on mineral nitrogen release from poultry and dairy manures. Soil Sci. Soc. Am. J. 47, 1129–1133. Harguindeguy, N.P., Blundo, C.M., Gurvich, D.E., Díaz, S., Cuevas, E., 2008. More than the sum of its parts? Assessing litter heterogeneity effects on the decomposition of litter mixtures through leaf chemistry. Plant Soil 303, 151–159. Holmes, R.M., Mcclelland, J.W., Sigman, D.M., Fry, B., Peterson, B.J., 1998. Measuring ja:math –NH4+ in marine, estuarine and fresh waters: An adaptation of the ammonia diffusion method for samples with low ammonium concentrations. Mar. Chem. 60, 235–243. Ikenganyia, E., Ndubuaku, U., Onyeonagu, C., Ukonze, U., 2015. Influence of pelleted and unpelleted composted organic waste materials on growth, dry matter accumulation and yield of three varieties of cucumber (Cucumis sativus) in the greenhouse. Am. J. Exp. Agric. 6, 147. Jenkinson, D.S., Brookes, P.C., Powlson, D.S., 2004. Measuring soil microbial biomass. Soil Biol. Biochem. 36, 5–7. Kuzyakov, Y., Blagodatskaya, E., 2015. Microbial hotspots and hot moments in soil: concept & review. Soil Biol. Biochem. 83, 184–199. Loecke, T.D., Cambardella, C.A., Liebman, M., 2012. Synchrony of net nitrogen mineralization and maize nitrogen uptake following applications of composted and fresh swine manure in the Midwest US. Nutr. Cycl. Agroecosyst. 93, 65–74. Meng, Q., Yang, W., Men, M., Bello, A., Xu, X., Xu, B., Deng, L., Jiang, X., Sheng, S., Wu, X., 2019. Microbial community succession and response to environmental variables during cow manure and corn straw composting. Front. Microbiol. 10, 529. Miller, F.C., 1989. Matric water potential as an ecological determinant in compost, a substrate dense system. Microb. Ecol. 18, 59–71. Moldenke, A.R., 1994. Methods of Soil Analysis: Part 2—Microbiological and Biochemical Properties. Soil Enzymes 63, 131–133. Norton, J.M., Schimel, J.P., 2011. Nitrogen mineralization immobilization turnover. Handbook of Soil Science, Huang PM, Li Y, Summers ME (eds). Second edn. CRC Press, Boca Raton, FL,, pp. 8–18. Rao, J.R., Watabe, M., Stewart, T.A., Millar, B.C., Moore, J.E., 2007. Pelleted organo-mineral fertilisers from composted pig slurry solids, animal wastes and spent mushroom compost for amenity grasslands. Waste Manage. 27, 1117–1128. Redin, M., Recous, S., Aita, C., Dietrich, G., Skolaude, A.C., Ludke, W.H., Schmatz, R., Giacomini, S.J., 2014. How the chemical composition and heterogeneity of crop residue mixtures decomposing at the soil surface affects C and N mineralization. Soil Biol. Biochem. 78, 65–75. Reganold, J.P., Wachter, J.M., 2016. Organic agriculture in the twenty-first century. Nat. Plants 2, 15221. Reiter, M.S., Daniel, T.C., Slaton, N.A., Norman, R.J., 2014. Nitrogen availability from granulated fortified poultry litter fertilizers. Soil Sci. Soc. Am. J. 78, 861. Schermelleh-Engel, K., Moosbrugger, H., Müller, H., 2003. Evaluating the fit of structural equation models: tests of significance and descriptive goodness-of-fit measures. Methods Psychol. Res. Online 8, 23–74. Shen, S., Pruden, G., Jenkinson, D., 1984. Mineralization and immobilization of nitrogen in fumigated soil and the measurement of microbial biomass nitrogen. Soil Biol. Biochem. 16, 437–444. Sigman, D.M., Altabet, M.A., Michener, R., Mccorkle, D.C., Fry, B., Holmes, R.M., 1997. Natural abundance-level measurement of the nitrogen isotopic composition of oceanic nitrate: an adaptation of the ammonia diffusion method. Mar. Chem. 57, 227–242. Silva, M.E.F., Lopes, A.R., Cunha-Queda, A.C., Nunes, O.C., 2016. Comparison of the bacterial composition of two commercial composts with different physicochemical, stability and maturity properties. Waste Manage. 50, 20–30. Sinegani, A.A.S., Maghsoudi, J., 2011. The effects of water potential on some microbial populations and decrease kinetic of organic carbon in soil treated with cow manure under laboratory conditions. J. Appl. Sci. Environ. Manage. 15. Singh, S., Ghoshal, N., Singh, K., 2007. Synchronizing nitrogen availability through application of organic inputs of varying resource quality in a tropical dryland agroecosystem. Appl. Soil Ecol. 36, 164–175. St. Luce, M., Whalen, J.K., Ziadi, N., Zebarth, B.J., 2016. Net nitrogen mineralization enhanced with the addition of nitrogen-rich particulate organic matter. Geoderma 262, 112–118. Stieglmeier, M., Mooshammer, M., Kitzler, B., Wanek, W., Zechmeisterboltenstern, S., Richter, A., Schleper, C., 2014. Aerobic nitrous oxide production through N-nitrosating hybrid formation in ammonia-oxidizing archaea. ISME J. 8, 1135. Voroney, R., Winter, J., Gregorich, E., 1991. Microbe/Plant/Soil Interactions, Carbon Isotope Techniques. Webster, T.S., Devinny, J.S., Torres, E.M., Basrai, S.S., 1997. Microbial ecosystems in compost and granular activated carbon biofilters. Biotechnol. Bioeng. 53, 296–303. Xu, J., Jiang, Z., Li, M., Li, Q., 2019. A compost-derived thermophilic microbial consortium enhances the humification process and alters the microbial diversity during composting. J. Environ. Manage. 243, 240–249. Zafari, A., Kianmehr, M., 2014. Factors affecting mechanical properties of biomass pellet from compost. Environ. Technol. 35, 478–486.
5. Conclusions Powder and granule were the two main forms of organic fertilizer, and had different impacts on N releasing. For soil mineral N content, powdery and granular forms had the similar effect after 3–4 months incubation, but granules released more N after about 1.5 months, acted as a slow-releasing fertilizer. According to the SEM, the potential mechanism of granular organic fertilizer delaying soil N supply was that microbial action produced an interval between the granules and the soil (eg., microorganisms were activated firstly in fertilizer granules and then grown in soil). Our findings demonstrated a strong connection between microbes activity and granular organic fertilizer N transformation, and indicated that the mechanism of applying granular organic fertilizer to improve N use efficiency. Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. Acknowledgments This work was supported by the NSFC project (41171211) and the China National Supporting Plan on Science and Technology (No. 2014BAD14B03). We thank Professor Junhong Bai and anonymous reviewers for their valuable comments and critical evaluation on this manuscript. We also thank Dr. Pengpeng Duan from the Nanjing Agriculture University for his assistance with structural equation model. Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.geoderma.2019.113994. References Agrawal, P.K., Agrawal, S., Shrivastava, R., 2015. Modern molecular approaches for analyzing microbial diversity from mushroom compost ecosystem. Biotech 5, 853–866. Berglund, S.L., Ågren, G.I., 2012. When will litter mixtures decompose faster or slower than individual litters? A model for two litters. Oikos 121, 1112–1120. Bodirsky, B.L., Popp, A., Lotze-Campen, H., Dietrich, J.P., Rolinski, S., Weindl, I., Schmitz, C., Müller, C., Bonsch, M., Humpenöder, F., 2014. Reactive nitrogen requirements to feed the world in 2050 and potential to mitigate nitrogen pollution. Nat. Commun. 5, 3858. Brookes, P., Kragt, J., Powlson, D., Jenkinson, D., 1985. Chloroform fumigation and the release of soil nitrogen: the effects of fumigation time and temperature. Soil Biol. Biochem. 17, 831–835. Cabrera, M., Merka, W., Thompson, S., Chiang, S., Pancorbo, O., 1994. Pelletizing and soil water effects on gaseous emissions from surface-applied poultry litter. Soil Sci. Soc. Am. J. 58, 807–811. Cox, D., 1995. Pelletized sewage sludge as a fertilizer for containerized plants: plant growth and nitrogen leaching losses1. J. Plant Nutr. 18, 2783–2795.
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Net nitrogen mineralization delay due to microbial regulation following the addition of granular organic fertilizer
T
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Xinyi Yanga, Guitong Lia, , Xiaohong Jiab, Xiaorong Zhaoa, Qimei Lina a Department of Soil and Water Science, College of Land Science and Technology, China Agricultural University, No. 2 West Road of Yuanmingyuan, Haidian, Beijing 100193, PR China b Beijing Soil & Fertilizer Extension Service Center, No. 6 Yumin Zhong Road, Xicheng, Beijing 100029, PR China
A R T I C LE I N FO
A B S T R A C T
Handling Editor: Junhong Bai
The transformation processes and fate of nitrogen (N) in organic fertilizer are particularly important for N supply to crop in agricultural soils. However, the dynamic of the N release process of granular organic fertilizer to soil is not as clear as that of the powdery form. In this study, granular (G) and powdery (P) forms of a manure compost, which were well mixed with maize straw powders (MS) in 5% or 15%, respectively, were applied to soil and incubated for 105 days. The differences in soil N mineralization-immobilization turnover (N-MIT) between the two forms were compared. Our results showed that, 1) soil mineral N content was similar in the two soil mixtures at day 105 (the end of the incubation), while granules released more mineral N after day 45; 2) granulizing the powdery mixtures of MS and mature compost released more N from the fresh MS than those in the powdery form; and 3) structural equation model indicated that divers of the microbial N transformation in the granules amended soil were significantly different from that in the powdery form amended soil. In terms of N management in crop production, our results suggest that granular organic fertilizer could delay N release for about 1 month, which may reduce N loss risk during crop seedling stage and increase soil N supply during the rapid growth period of most crops. We therefore propose that making organic fertilizer into granules is a hopeful way to synchronize fertilizer N release to the maximal uptake of crops, which improve N use efficiency and alleviate the negative impact on environment.
Keywords: Organic fertilizer form 15 N labeling N mineralization Structural equation model
1. Introduction Nitrogen (N) is a main limiting factor for crop production in agricultural ecosystems, and one optimal organic N fertility management practice was determined by the extent of soil N supply fitting with crop demand (Reganold and Wachter, 2016). The application of organic fertilizer (OF), such as poultry manure, crop straws and their compost products, can increase crop yield, improve soil quality, and alleviate greenhouse gas emissions as well (Bodirsky et al., 2014; Gu et al., 2015). The bio-availability of N in OF is the result of the mineralizationimmobilization turnover (MIT) process of N-containing components , and application method is one of the main factors affecting the MIT process. Currently, the common way to apply OF is to incorporate with the form of small powders (smaller than 1 mm) into soil, and then mix them well to evenly distribute them among soil matrix. The advantage of this method is the evenly distributed nutrient that making roots more chance to contact. However, this powder form maybe not suitable for the adjustment of C:N ratio using two or more materials, as the different
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kinds of powders separately existed among microsites, and the un-intertouched powders could not contact with each other and the C:N ratio adjustment fail (Singh et al., 2007; Stieglmeier et al., 2014). Alternatively, applying OF in locally-concentrated forms (such as in granule, pellet, or tablet, etc.) will give another story of MIT. Generally, pelletized materials released more inorganic N than that in powder form under the same condition (Hadas et al., 1983). Meanwhile, the bigger physical forms reduce the specific contact area between OF and soil matrix, making NH4+ and NO3− a slow release to the surrounding soil (Cox, 1995; Rao et al., 2007). However, all the above effects were integrative effect of the mixture of pellets and soil. What happened in the MIT process within the pellets was not known at all. N-rich organic matter such as manure and legume crop residues and C-rich organic matter such as most crop residues are often mixed to get a suitable C:N ratio for rapid decomposition and N release (Berglund and Ågren, 2012; Harguindeguy et al., 2008; Redin et al., 2014), but the mixing effect can be synergistic (Singh et al., 2007), antagonistic, or additive (Stieglmeier et al., 2014). The main reason for this contradicts
Corresponding author. E-mail address: [email protected] (G. Li).
https://doi.org/10.1016/j.geoderma.2019.113994 Received 22 January 2019; Received in revised form 24 September 2019; Accepted 26 September 2019 0016-7061/ © 2019 Elsevier B.V. All rights reserved.
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treatment. To set up the incubation, a modified device was used (Fig. S1). For 5-G and 15-G treatments, granules were put into the middle of Box b, and surrounded by incubated soil B. According to the designed size of box b, the surrounding soil B was within 1 cm to the granule surface, and separated by the mesh (1.5 mm in diameter). When the 14 granules were put into the middle soil layer (soil B and C), the N application rate of 165 mg kg−1 was reached. To protect the incubated soil, two soil layers, 5 cm soil layer on the above and 10 cm soil layer under the bottom of the middle layer (Fig. S1), were used and separated by nylon net (to be easily moved). All soil used was the same soil with the same water content of 60% of Water holding Capacity (WHC) of the soil and filled with bulk density of 1.4 g cm−3. For 5-P and 15-P treatments, operation was same as that in 5-G and 15-G treatments, except for putting mixture of MS and OF powders in the middle layer. After all replications (21 replications for each treatment) were prepared, each replication was put into a 3000 ml plastic jar and the incubation started under 25 °C and dark condition. During the 105 days incubation, water content of the soil–OF mixture was adjusted by dropping the required amount of deionized water when the loss was greater than 0.05 g (Fig. S1). The other replications (18 for each treatment) were used for sampling soil and fertilizer granules on days 5, 15, 30, 45, 75 and 105. Three replications were destroyed for sampling at each sampling time. To do the sampling, the 5 cm protect soil layer was first removed by picking up the nylon net a. Then fertilizer granules were picked out from the soil B by tweezers in the 5-G and 15-G treatments (Fig. S1) and all soil B in each replication were thoroughly mixed to make a composted sample. Meanwhile, all fertilizer granules in each replication were mixed together to make a composted sample. In the 5-G and 15-G treatment, samples of soil B and fertilizer granules were analyzed separately. In the 5-P and 15-P treatments, the mixture of soil and fertilizer powders in the middle layer (including soil C) were sampled and measured.
result maybe lie in the fact that the single particles of different materials were dispersed among the soil matrix and actually did not interact each other. In other words, the adjustment of C:N ratio was failed. Then the final N release process was just a simple sum of various materials without any or less interaction. This spatial separation between the different types of materials is just the distribution pattern for the powdery OF application to soil. On the other hand, if two or more materials are mixed into a granular, i.e. into a tight combination of “N” and “C” materials, the real C:N ratio will be obtained and a new MIT will be created. N supply from granular OF may preferentially mineralize in the interior of the granule and then gradually release N into the surrounding soil, thus the peak of soil N supply could be delayed. Of course, smaller contact area of granular fertilizer also slows down the release of N. From this, we can expect a new MIT process of N in the granular OF applied to soil. In this study, we made granular OF by mixing powders of composted cow manure and fresh maize straw (MS) with 5% and 15%. Then we incubated these granules and those powders mixtures with soil for 105 days, respectively. The objectives of the experiment were: 1) to clarify the different patterns of N release between the powdery and granular forms of OF; 2) to explore the MIT process happened in the OF granular; and 3) to explain the difference in N transformation between the powdery and granular forms. 2. Materials and methods 2.1. Soil and organic material Soil was collected from the upper layers (0–15 cm) of a Fluvisol (FAO system), which grown winter wheat and summer maize for many years. The fresh soil was thoroughly mixed, sieved (< 2 mm) and stored at 25 °C for 1 week before used. Fresh maize straw powder (< 2 mm) used in this experiment was derived from a 15N-labeled corn leaves. Fresh cow manure and ammonium sulfate were co-composted for 90 days and the product was made into < 2 mm powders (OF). Basic properties of soil and organic materials are shown in Table 1.
2.3. Analysis method Total N and organic C concentrations of the OF and soil samples were determined by dry combustion using an Elementary CN Analyzer (elemental analyzer vario PYRO cube). To determine NH4+ and NO3− concentrations and their stable isotope ratio (δ15N), incubated soil samples and original samples were extracted with a 0.5 mol L−1 K2SO4 solution at a 1:5 (w/v) soil to extracting ratio. The samples were shaken at 250 rpm on a mechanical shaker for 1 h before being filtered through Whatman No. 42 filter papers. We used the NH3-diffusion technique (Holmes et al., 1998; Sigman et al., 1997) to determine the 15N natural abundance of NO3− and NH4+. Ammonium was diffused as NH3 after addition of MgO, while NO3− was reduced by adding Devarda’s alloy and subsequently diffused as NH3 onto a second filter. Each diffusion step was conducted at 35 °C under continuous shaking for 7 days. Pure KCl (1 M) solution was added to make standard 90 ml solutions. Standard NH4+ and NO3− solutions were analyzed using the same procedures and showed δ15N values within 0.2% of their expected values. Previous findings by Holmes et al. (1998) indicated that volumes less than 200 ml recorded accurate diffusion of N standards. For our analysis, samples were analyzed for 15N using a stable isotope ratio mass spectrometer (Isoprime 100) linked to a CN analyzer (elemental analyzer vario PYRO cube). Microbial biomass C (MBC) and N (MBN) were determined using chloroform fumigation extraction (Jenkinson et al., 2004). Fresh samples were fumigated with ethanol-free chloroform for 24 h in an evacuated desiccator. Fumigated and unfumigated samples were extracted with 0.5 mol L−1 K2SO4 solutions at a 1:10 (w/v) soil to potassium sulfate solution ratio and filtered using Whatman No. 42 filter papers. Chloroform (CHCl3) fumigation-extraction method was employed to estimate the amount of MBN and MBC by using the equation:
2.2. Experiment design and sampling The incubation experiment included 5 treatments: 1) 5% MS + 95% OF, in powdery form (5-P); 2) 15% MS + 85% OF, in powdery form (15-P); 3) 5% MS + 95% OF, in granular form (5-G); 4) 15% MS + 85% OF, in granular (15-G); and 5) a control treatment (CK). The 5% and 15% were the ratio of N in the maize straw to the total N in the mixture of MS and OF. To make granular form, moist powders (water mass content 30%) of MS and OF were thoroughly mixed, then inserted into cylinders (made with wire mesh) which diameter and height was 1 cm respectively (Fig. S1). Each cylinder (fertilizer granule) was filled with 0.964 g (calculated dry weight) of powdery mixture. According to the application rate of N, 14 granules were added to each replication in the 5-G and 15-G Table 1 The basic properties of the soil and organic material. Items
Soil
Sand (> 0.05 mm), g kg−1 Silt (0.05–0.02 mm), g kg−1 Clay (< 0.02 mm), g kg−1 Organic C, g kg−1 Total N, g kg−1 15 N, atom% NH4+-N, mg kg−1 NO3–-N, mg kg−1
280 ± 14.00
Maize straw
Organic fertilizer
44.14 ± 5.21 1.51 ± 0.03 1.25 ± 0.01 341.11 ± 21.46 172.34 ± 12.12
24.52 ± 1.41 4.80 ± 0.32 0.37 ± 0.01 584.56 ± 34.53 263.78 ± 22.08
520 ± 26.00 200 ± 10.00 4.32 ± 0.08 0.82 ± 0.02 0.37 ± 0.01 15.32 ± 0.61 16.38 ± 3.07
2
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Fig. 1. The dynamics of NH4+-N and NO3−-N contents during the 105-days incubation. (a) and (b) are the NH4+-N and NO3−-N content in the soil mixtures of the 5 treatments, respectively; (c) and (d) are the NH4+-N and NO3−-N content in the surrounding soils and OF granules in the G treatments, respectively. Error bars show the standard error of the mean of each treatment (n = 9). In some cases, error bars are smaller than the symbols.
Glucosidase activity was measured according to Ekenler and Tabatabai (2003) and protease activity was analyzed following the method of Geisseler and Horwath (2008). All measurements were undertaken in triplicate from the independent replications. N transformation was calculated as the net N mineralization rate (Nmin), where Nmin (mg N kg−1 d−1) was calculated by divided the difference in mineral N between start and end of each period with the duration in the day. Extractable NH4+-N and NO3−-N (Mineral N) was determined calorimetrically on an auto–analyzer (AA3, Bran & Luebbe, Germany).
MBN = EN/KEN and MBC = EC/KEC, where EN and EC are the N and C extracted by 0.5 M K2SO4 from fumigated soil minus that extracted from non-fumigated soil, and KEN and KEC are the conversion factors for MBN (0.68) (Brookes et al., 1985) and MBC (0.35) (Voroney et al., 1991). To measure δ15N in MBN, freeze-drying method was used to get the measuring samples from the extracts of fumigated and non-fumigated. The 15N samples were prepared using a method proposed by Shen et al. (1984), and 15N/14N ratio was measured by a stable isotoperatio mass spectrometer (Isoprime 100). The mass of maize-derived N and 15N recovery in different N pools were calculated according to the Eq. (1) and Eq. (2), and the 15N at.% excess was corrected for the corresponding background abundance.
MAB
P I = B B IA
2.4. Statistical analysis Multiple comparisons of N components and enzyme activity among different treatments were performed by LSD method, while repeated variance analysis was performed for sampling time, fertilization method and ratio, and statistical analysis was performed by SPSS 20.0. Structural equation modeling (SEM) was used to disentangle direct and indirect effects of P and G treatment, soil physicochemical properties, the ratio of substrate C and N and enzyme activities on soil mineral N by using AMOS PFtware (IBM SPSS AMOS 20.0.0). Prior to modeling, all data were normalized (ensuring all data in a standard normal distribution with a mean value of 0 and standard deviation of 1) and an a priori model was established based on the known effects and relationships among the drivers that had a significant effect on soil mineral N in previous analysis (Doncaster, 2010). SEM was employed instead of multiple regressions because directions can be assigned to several relationships, resulting in multiple explanatory as well as multiple response variables in one model (Doncaster, 2010). Furthermore, the structure of such a model can reveal whether a significant bivariate relationship occurs due to a significant relationship between two given variables and a third variable. The following criteria were used to evaluate the fit of the models: The root mean squared error of
(1)
where MAB is the maize-derived N in a given N pool (mg kg−1); IA is the 15 N at.% excess of maize, PB is the N mass of the given N pool (mg kg−1); and IB is the 15N at.% excess of the given N pool. 15N
recovery = 100 15
PB IB PA IA
(2) 15
where N recovery is the N recovered in a given N pool (%); PA is the application rate of maize-derived N (Dawson et al., 2002). Extractable C and N were determined using a vario TOC select analyzer (Elementar, Germany). Extractable C in the unfumigated samples was used to represent DOC. DON was calculated as the difference between the extractable N and the sum of NH4+-N and NO3−-N in the un-fumigated samples. Extracellular enzyme activities (β-glucosidase, protease and dehydrogenase) were determined using the following methods. Dehydrogenase activity was assayed through colorimetric determination of triphenyl formazan formed when soils were incubated with 2, 3, 5-triphenyltetrazolium chloride at 37 °C for 24 h (Moldenke, 1994). Β3
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approximation (RMSEA; the model has a good fit when RMSEA is low (< 0.05)), chi–square value (CHI/DF; the model has a good fit when CHI/DF is low), Fisher's P statistic (the model has a good fit when 0.05 < P ≤ 1.00) and the Akaike information criterion (AIC; the model has a good fit when AIC is low) (Schermelleh-Engel et al., 2003).
Although MBN and MBC of the soil mixture in G treatments were higher than that in P treatments after day 45, they were distributed differently, even in P treatments and concentrated in granules in G treatments. 3.3. Factors of soil N mineralization
3. Results SEM was used to explore the direct and indirect effects of the powdery and granular OF application forms on soil mineral N dynamics through net N mineralization (Fig. 3). Parameters in the SEM included OF parameters (C:N, enzyme activities, DON, and MBN) and soil properties (C:N, enzyme activities, MBN, DON and net N mineralization (Table S1)). In total, 32% and 29% of the soil mineral N in the P and G treatments could be explained by these parameters (Fig. 3). When OF applied in powdery form, soil mineral N dynamics was driven by a clear way which made up by a set of steps: C:N ratio of OF determined enzyme activities, then the DOC/DON ratio and the net N mineralization (Fig. 3a). Here the microbial biomass (MBN) was not a determined factor. However, the driven process of soil mineral N in the granulesamended soil was totally different (Fig. 3b). Two processes occurred under this condition, in granules first and then in the surrounding soil. In granules, both C:N ratio of OF and MBN equally important to the enzyme activities, then the enzyme activities determined the DON concentration. After the DON diffused into the surrounding soil, it positively determined the C:N ratio of the soil and the MBN. But only MBN positively determined the enzyme activities in soil, and then enzyme activities positively determined the net N mineralization. There were three aspects were difference between the powdery form and the granular form, that the MBN was important for the enzyme activities both in the granules and in the corresponding surrounded soil, but not related the enzyme activities in the powdery form; that net N mineralization was determined by the DOC/DON ratio in the powdery form, but by the enzyme activities in the granular form; and that DON was the linking pool between the granules and the surrounding soil.
3.1. Mineral N Dynamics of NH4+ and NO3− in the soil mixture showed different patterns between the powdery and granular forms of OF application (Fig. 1a and b). The NH4+ in the soil mixture rapidly increased after the powders addition at day 0 and peaked at day 15, then decreased rapidly to day 75 and un-changed to day 105. But for 5-G and 15-G, NH4+ remained the same level through the 105-day incubation. After day 45, NH4+ in G treatments were always higher than that in P treatments, and ending at ca. 40 mg kg−1 in G treatments and ca. 15 mg kg−1 in P treatments (which was also same as in CK), respectively. At day 15, NH4+ in 5-P peaked at 116 mg kg−1 whereas in 15-P it was only 86 mg kg−1. For NO3−, powdery form application increased the NO3− content quickly and peaked at day 30, then kept constant till the end of the incubation. But for G treatments, the NO3− content increased gradually till day 75, then kept constant to the end. At the end of the incubation, NO3− was ca. 160 mg kg−1 and ca. 120 mg kg−1 in P and G treatments, respectively, all significantly higher than that in the CK. For granular application, dynamics of NH4+ and NO3− in granules and the surrounding soil were shown in Fig. 1c and d. NH4+ contents in granules decreased from ca. 550 mg kg−1 just after the granules addition at day 0 to ca. 210 mg kg−1 at day 105 (Fig. 1c). Meanwhile, NO3− in granules increased correspondingly from ca. 250 mg kg−1 at day 0 to ca. 590 mg kg−1 at day 105 (Fig. 1d). Influenced by the granules, the surrounding soil got more NH4+ and NO3− (Fig. 1c and d). At the end of the incubation, the extra mineral N in the soil mixture (the sum of NH4+-N and NO3−-N in treatments minus that in CK) was ca.120 mg kg−1 and ca 110 mg kg−1 in P and G treatments, respectively, meaning no difference in the apparent net N mineralization between the two OF application forms. But the N distribution pattern was different, evenly distributed in P treatments and concentrated distributed in granules in G treatments.
3.4. Transformation of N in maize straw The N in the 15N-labeled maize straw transformed into NH4+, NO3−, DON and MBN during the incubation (Fig. S2), and the total recovery ratios into these 4 pools could be found in Table 2. The total N recovered in the 4 pools was 80.3% and 27.5% after 105 days incubation in 5-G and 15-G treatments, respectively, about 2 times higher than the 44.7% and 14.5% in 5-P and 15-P treatments (Table 2), indicating that applied OF in granular form increased its N transformation. Meanwhile, the more maize straw added, the less proportion of transformed N during the incubation. For granular form, although more the transformed N located in the granules, a small proportion of the transformed N moved into the surrounding soil.
3.2. Microbial biomass C and N There were significant differences of MBN and MBC dynamics in the soil mixture between the powdery and granular forms of OF application (Fig. 2a and b). For MBN, firstly it rapidly increased after the powders addition at day 0 and peaked at day 15, then decreased rapidly to day 45 and slowly to day 105. But for 5-G and 15-G, MBN kept constant till day 30, then increased till day 75, and kept stable to the end of the incubation (Fig. 2a). Secondly, after day 45, MBN in G treatments were always higher than that in P treatments, and ending at ca. 65 mg kg−1 in G treatments and ca. 25 mg kg−1 in P treatments (which was also higher than that in CK), respectively. Thirdly, at day 15, MBN in 5-P and 15-P peaked at the same value, ca 110 mg kg−1. In general, dynamics of MBC were nearly as same as that of MBN (Fig. 2a and b). At the end of the incubation, MBC was ca. 90 mg kg−1 and ca. 35 mg kg−1 in G and P treatments, respectively, all significantly higher than that in the CK. For granular application, dynamics of MBN and MBC in granules and the surrounding soil were shown in Fig. 2c and d. MBN contents in granules kept constant till day 45, then increased rapidly till day 75, and kept constant again (Fig. 2c). On the other hand, MBC in granules increased rapidly till day 45, and then slowly to the end of the incubation (Fig. 2d). In the surrounding soil, MBN and MBC kept constant till day 45, then increased rapidly till day 75. After day 75, MBN kept constant while MBC decreased (Fig. 2c and d).
4. Discussion 4.1. Difference in N transformation between the two application methods After 105-days incubation, no difference in mineral N of soil mixture (120 vs 110 mg kg−1) between the powdery and the granular forms (Fig. 1a and b), indicating that these two OF application forms provided similar amount of soil mineral N during the experimental period. This was similar with some of the previous studies (Hadas et al., 1983; Cabrera et al., 1994), but different to the study which fresh (but not well composted) poultry litter used (Reiter et al., 2014). Meanwhile, more NH4+-N, ca 25 mg kg−1, presented in the soil mixtures amended with granular OF, consisted with the previous studies (Hadas et al., 1983; Reiter et al., 2014). This more NH4+ would be favorable to plants which prefer to use NH4+ form of the mineral N as plant uptake. The C:N ratios in powders-amended soil mixture and in granules were 6.1–6.9:1 and 6.5–7.6:1, respectively. They were similar and less 4
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Fig. 2. The dynamics of MBN and MBC contents during the 105-days incubation. (a) and (b) are the MBN and MBC contents in the soil mixtures of the 5 treatments, respectively; (c) and (d) are the MBN and MBC contents in the surrounding soils and OF granules of the G treatments. Error bars show the standard error of the mean of each treatment (n = 9). In some cases, error bars are smaller than the symbols.
Fig. 3. Possible effects of changes in soil mineral N driven by properties of soil and OF and N components. (a) Powdery treatments (5-P and 15-P) and (b) Granular treatments (5-G and 15-G). The “Fer” in (b) represents the OF, and the “soil” in (b) represents the “surrounding soil”. The width of the arrows is proportional to the strength of the path coefficients adjacent with numbers. Solid and dashed lines represent positive and negative paths, respectively. The R2 denotes the proportion of variance that could be explained by the corresponding variable in the structural equation model. Significance levels are as follows: *p < 0.05, **p < 0.01 and ***p < 0.001. Goodness-of-fit statistics are shown underneath the modeling frames. Nmin: net N mineralization.
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Table 2 The total N recovery (%) of the Day (d)
Soil mixtures 5-P
5 15 30 45 75 105
N-labeled maize straw in the pools of NH4+, NO3−, MBN and DON.
15
51.1 74.8 63.8 49.1 44.8 44.7
Surrounding soils 15-P
± ± ± ± ± ±
2.6 3.7 3.2 2.5 2.2 2.2
17.7 23.3 18.9 16.5 15.2 14.5
5-G ± ± ± ± ± ±
0.9 1.2 1.0 0.8 0.8 0.7
68.8 68.7 71.1 71.4 86.4 80.3
15-G ± ± ± ± ± ±
4.1 4.1 4.3 4.3 5.2 4.8
22.1 26.0 25.8 26.5 30.7 27.5
5-G ± ± ± ± ± ±
1.1 1.3 1.3 1.3 1.5 1.4
19.0 21.9 21.2 20.4 19.7 17.7
± ± ± ± ± ±
1.0 1.1 1.1 1.0 1.0 0.9
OF granules 15-G
5-G
3.1 ± 0.2 4.1 ± 0.2 4.7 ± 0.2 6.1 ± 0.3 11.0 ± 0.6 9.8 ± 0.5
60.4 55.9 54.2 51.3 52.2 48.6
15-G ± ± ± ± ± ±
3.0 2.8 2.7 2.6 2.6 2.4
8.4 ± 0.4 12.8 ± 0.6 17.0 ± 0.9 20.1 ± 1.0 34.2 ± 1.7 31.7 ± 1.6
4.2. Potential mechanism for the difference between different OM form
than the typical C:N ratio of 25:1, meaning net N mineralization occurred (Norton and Schimel, 2011), especially during the early period of incubation. In fact, these similar C:N ratios in the powders-amended soil mixtures and the granules gave out nearly the same amount of net N mineralization during the first 15 days (Fig. 1). But in the granules, ca 200 mg kg−1 DON lost during the first 15 days, whereas only ca 20 mg kg−1 DON lost in the powders-amended soil mixture (Fig. S3a and c). The minor loss of DON in the powders-amended soil mixture meant that more un-dissolved organic N (other than the original DON) mineralized during the first 15 days, which showed the powdery OF caused more stable organic N to be mineralized in the soil mixture than that in the granules. In granules-amended soil mixture, the NH4+-N, NO3−-N, DON, and MBN distributed un-evenly. Concentrations of these N forms was about 36, 21, 7, and 22 times higher in the granules than those in the surrounding soil during the first 15 days (Figs. 1c, d, 2c and Fig. S3c). Surprisingly, although MBN in granules was higher than that in the powders-amended soil mixtures (5-P and 15-P), they did not increase rapidly during the first 15 days as expected. This may be due to the relatively lack of r-type microorganisms in the granules than that in the soil, as k-type microorganisms was more dominant in the mature compost (Meng et al., 2019; Silva et al., 2016) and also could be due to the low relative water content (30%) in the OF granules, because the water potential of this water content for the composted material and fresh maize straw was too low for an active microbial growth (Da Silva et al., 2016; Miller, 1989; Sinegani and Maghsoudi, 2011). Additionally, in powders-amended soil mixtures (5-P and 15-P), although the water content of the OF powders was also 30%, the small powders and the big surface area made the powders quickly contact to the soil matrix and then water moved into the powders, because the water potential of the soil matrix, 60% of WHC, was much higher than the water potential of the powders (Miller, 1989). This made an increase of MBN in powders-amended soil mixtures before day 15 (Fig. 2a). But for the later period of the incubation (day 45 to day 105), MBN in granules increased rapidly while decreased slowly in the powders-amended soil mixtures. The enzyme activities in granules were similar with that in the powders-amended soil mixtures during the first 15 days of incubation, but much higher afterwards (Fig. S4), becoming hotspot of the microbial activity in the soil mixture (Kuzyakov and Blagodatskaya, 2015). These higher enzyme activities after day 30, especially the protease (Fig. S4c), directly co-related to the decrease of DON and DOC (Fig. S3c and d) and the increase of MBN and MBC (Fig. 2c and d) in the granules. Meanwhile, with more DON and DOC mineralized into the surrounding soil (Fig. S3c and d), MBN and MBC increased (Fig. 2c and d), resulting in an increase in enzyme activities (Fig. S4), and then an increase in mineral N in the surrounding soil (Fig. 1c and d). Therefore, in the granular OF application way, the N transformation started first within the granules and then transmitted to the surrounding soil via DON (Fig. 3).
Powdery OF rapidly increased the NH4+ and NO3− contents in the soil mixture than granular OF did (Fig. 1a and b), which was similar with the previous researches (Cabrera et al., 1994; Hadas et al., 1983). The common reason for this difference was attributed to the large surface area of powdery OF and the slow diffusion of organic N out of the OF pellets (Cabrera et al., 1994; Hadas et al., 1983), hinting that organic N must be contacted to soil microorganism to be mineralized. However, this conclusion was just based on the experiment in which NH4+, NO3− and DON contents in the pellets were not measured (Hadas et al., 1983). In the current study, we measured them in the pellets. Results showed that high concentration of NH4+ and NO3− existed in the pellets during the first 15 days (Fig. 1c and d). Most importantly, net N mineralization occurred (the sum of NH4+-N and NO3−-N increased in Fig. 1c and d) in the pellets. In fact, if we take the soil mixture as the whole calculation base of soil mineral N content, the pellet surface was not the reason for the difference in mineral N content between the soil mixtures amended with powdery or granular OF, because NH4+-N and NO3−-N both in pellets and their surrounding soil are included in the calculation. For organic N, we measured the DON in the pellets and the surrounding soil (Fig. S3c). There was high DON in the pellets, and more importantly, this DON decreased rapidly during the first 15 days, indicating a net N mineralization occurred (Fig. S3c). Therefore, DON in the pellets cannot be diffused to the surrounding soil to be mineralized, and it could be mineralized within the pellets. As a result, the difference in surface area between the powdery and granular OF and the less diffusion of organic N out of the pellets seemed not directly related to the difference in mineral N between the soil mixtures amended with powdery or granular OF during the first 15 days of the incubation. Based on the above analysis, we attributed the reason for this difference to the difference in microbial transformation of N between the soil mixtures amended with powdery or granular OF. In powdersamended soil mixture, soil mineral N increased ca 120–210 mg kg−1 (Fig. 1a and b) and soil MBN increased ca 60 mg kg−1 (Fig. 2a) before day 15, but in the granules amended soil mixture only soil mineral N increased ca 60 mg kg−1 (Fig. 1c and d). This meant that the net N mineralization processes in the two soil mixtures were nearly the same, but microbial N immobilization (MNI) occurred in the powdersamended soil mixture and no MNI in the granules-amended soil mixture. The comparative net N mineralization in the two soil mixtures could also be proofed by the similar proteinase activity on day 15 (Fig. Scc). Based on the MIT theory (Norton and Schimel, 2011), the similar net N mineralization and the difference in microbial immobilization meant that difference in gross N mineralization existed between the two mixtures. Conditions for N transformation in granules were totally different with that in the powders-amended soil mixture. Firstly, the microbial community was mostly from the mature compost, which was significantly different with those from soil (Gattinger et al., 2004; Xu et al., 2019); Secondly, available C and N sources were relatively rich and contacted each other in space, more easy for microorganism to get 6
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(Agrawal et al., 2015; Webster et al., 1997); and thirdly, concentrations of substrate (DON) and products (NH4+ and NO3−) of organic N mineralization process were very high, which had strong feedback effects (positive or negative) on the MIT process. With the high concentrations of DON (Fig. S3cFig. S3c) and microbial biomass (Fig. 2c and d) in the granules, organic N mineralization was just determined by the enzyme activities as the substrate and microbial driver were not the limited factors for the mineralization in the granules (Fig. 3b). General speaking, making OF into granules would increase OF producing cost (Zafari and Kianmehr, 2014; Ikenganyia et al., 2015). But if we want to improve OF’s fertilizer value (especially for N), or to synchronize the N supply and crop absorb under only OF applied condition (Singh et al., 2007; Loecke et al., 2012; St. Luce et al., 2016), granulizing or pelleting the original compost product could be a good choice.
Da Silva, A.M.F., Boukhdoud, N., Gros, R., 2016. Distance from the sea as a driving force of microbial communities under water potential stresses in litters of two typical Mediterranean plant species. Geoderma 269, 1–9. Dawson, T.E., Mambelli, S., Plamboeck, A.H., Templer, P.H., Tu, K.P., 2002. Stable isotopes in plant ecology. Annu. Rev. Ecol. Syst. 33, 507–559. Doncaster, C.P., 2010. Structural equation modeling and natural systems. Fish Fish. 8, 368–369. Ekenler, M., Tabatabai, M.A., 2003. Effects of liming and tillage systems on microbial biomass and glycosidases in soils. Biol. Fert. Soils 39, 51–61. Gattinger, A., Bausenwein, U., Bruns, C., 2004. Microbial biomass and activity in composts of different composition and age. J. Plant Nutr. Soil Sci. 167, 556–561. Geisseler, D., Horwath, W.R., 2008. Regulation of extracellular protease activity in soil in response to different sources and concentrations of nitrogen and carbon. Soil Biol. Biochem. 40, 3040–3048. Gu, B., Ju, X., Chang, J., Ge, Y., Vitousek, P.M., 2015. Integrated reactive nitrogen budgets and future trends in China. Proc. Natl. Acad. Sci. U.S.A. 112, 8792. Hadas, A., Bar-Yosef, B., Davidov, S., Sofer, M., 1983. Effect of pelleting, temperature, and soil type on mineral nitrogen release from poultry and dairy manures. Soil Sci. Soc. Am. J. 47, 1129–1133. Harguindeguy, N.P., Blundo, C.M., Gurvich, D.E., Díaz, S., Cuevas, E., 2008. More than the sum of its parts? Assessing litter heterogeneity effects on the decomposition of litter mixtures through leaf chemistry. Plant Soil 303, 151–159. Holmes, R.M., Mcclelland, J.W., Sigman, D.M., Fry, B., Peterson, B.J., 1998. Measuring ja:math –NH4+ in marine, estuarine and fresh waters: An adaptation of the ammonia diffusion method for samples with low ammonium concentrations. Mar. Chem. 60, 235–243. Ikenganyia, E., Ndubuaku, U., Onyeonagu, C., Ukonze, U., 2015. 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Organic agriculture in the twenty-first century. Nat. Plants 2, 15221. Reiter, M.S., Daniel, T.C., Slaton, N.A., Norman, R.J., 2014. Nitrogen availability from granulated fortified poultry litter fertilizers. Soil Sci. Soc. Am. J. 78, 861. Schermelleh-Engel, K., Moosbrugger, H., Müller, H., 2003. Evaluating the fit of structural equation models: tests of significance and descriptive goodness-of-fit measures. Methods Psychol. Res. Online 8, 23–74. Shen, S., Pruden, G., Jenkinson, D., 1984. Mineralization and immobilization of nitrogen in fumigated soil and the measurement of microbial biomass nitrogen. Soil Biol. Biochem. 16, 437–444. Sigman, D.M., Altabet, M.A., Michener, R., Mccorkle, D.C., Fry, B., Holmes, R.M., 1997. Natural abundance-level measurement of the nitrogen isotopic composition of oceanic nitrate: an adaptation of the ammonia diffusion method. Mar. Chem. 57, 227–242. Silva, M.E.F., Lopes, A.R., Cunha-Queda, A.C., Nunes, O.C., 2016. 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5. Conclusions Powder and granule were the two main forms of organic fertilizer, and had different impacts on N releasing. For soil mineral N content, powdery and granular forms had the similar effect after 3–4 months incubation, but granules released more N after about 1.5 months, acted as a slow-releasing fertilizer. According to the SEM, the potential mechanism of granular organic fertilizer delaying soil N supply was that microbial action produced an interval between the granules and the soil (eg., microorganisms were activated firstly in fertilizer granules and then grown in soil). Our findings demonstrated a strong connection between microbes activity and granular organic fertilizer N transformation, and indicated that the mechanism of applying granular organic fertilizer to improve N use efficiency. Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. Acknowledgments This work was supported by the NSFC project (41171211) and the China National Supporting Plan on Science and Technology (No. 2014BAD14B03). We thank Professor Junhong Bai and anonymous reviewers for their valuable comments and critical evaluation on this manuscript. We also thank Dr. Pengpeng Duan from the Nanjing Agriculture University for his assistance with structural equation model. Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.geoderma.2019.113994. References Agrawal, P.K., Agrawal, S., Shrivastava, R., 2015. Modern molecular approaches for analyzing microbial diversity from mushroom compost ecosystem. Biotech 5, 853–866. Berglund, S.L., Ågren, G.I., 2012. When will litter mixtures decompose faster or slower than individual litters? A model for two litters. Oikos 121, 1112–1120. Bodirsky, B.L., Popp, A., Lotze-Campen, H., Dietrich, J.P., Rolinski, S., Weindl, I., Schmitz, C., Müller, C., Bonsch, M., Humpenöder, F., 2014. Reactive nitrogen requirements to feed the world in 2050 and potential to mitigate nitrogen pollution. Nat. Commun. 5, 3858. Brookes, P., Kragt, J., Powlson, D., Jenkinson, D., 1985. Chloroform fumigation and the release of soil nitrogen: the effects of fumigation time and temperature. Soil Biol. Biochem. 17, 831–835. Cabrera, M., Merka, W., Thompson, S., Chiang, S., Pancorbo, O., 1994. Pelletizing and soil water effects on gaseous emissions from surface-applied poultry litter. Soil Sci. Soc. Am. J. 58, 807–811. Cox, D., 1995. Pelletized sewage sludge as a fertilizer for containerized plants: plant growth and nitrogen leaching losses1. J. Plant Nutr. 18, 2783–2795.
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