Open access peer-reviewed chapter
Legume and cereal crops and nitrogen-fixing microorganisms used for inoculation.
Abstract
This work summarizes information about organic nitrogen (N) in the agricultural system. The organic N forms in soils have been studied by identifying and quantifying the released organic compounds when soils are acid treated at high temperature, in which the following organic N fractions are obtained: hydrolyzable total N, subdivided into hydrolyzable NH4+-N, amino sugars-N, amino acids-N, and unidentified-N and acid insoluble N, a fraction that remains associated with soil minerals after acid hydrolysis. Nitrogen mineralization and immobilization are biochemical processes in nature. This chapter summarizes how these processes occur in the agricultural system. Then, soluble organic nitrogen (SON), volatilization and denitrification processes, and biological nitrogen fixation (BNF) as a key component of the nitrogen cycle and how it makes N available to plants are also discussed. Finally, we discuss the use of organic fertilizers as N source to satisfy the worldwide demand for organic foods produced without synthetic inputs.
Keywords
- biological N fixation
- immobilization
- mineralization
- organic fertilization
1. Introduction
Nitrogen (N) is the fourth most abundant element in cellular biomass and comprises most of the Earth’s atmosphere. In the surface layer of most soils, over 90% of N occurs in organic forms. Soil organic N can be divided into two categories: (1) N from organic residues and (2) N from soil organic matter or humus [1]. All these materials are important in maintaining or improving soil fertility and plant nutrition through direct and indirect effects on microbial activity and nutrient availability [2]. Analysis of organic fractions has been highlighted due to the increasing application of organic fertilizers and their direct and indirect effects on crop growth and yield and soil attributes. Thus, we will discuss about organic N forms, N mineralization and immobilization, volatilization and denitrification, soluble organic N, biological N fixation, and organic fertilization with emphasis on N.
Advertisement
2. Organic nitrogen
Nitrogen is an essential element for plants, being constituent of important biomolecules such as adenosine triphosphate (ATP), reduced nicotinamide adenine dinucleotide (NADH), nicotinamide adenine dinucleotide phosphate (NADPH), chlorophylls, amino acids and proteins (glyco- and lipoproteins), nitrogenous bases and nucleic acids, and various enzymes [3, 4]. Soil organic N consisting of proteins, chitins, amino acids, and nucleic acids represents about 90–98% of total soil N [1, 5]. Mineralized N forms are transient in the soil so that the existing amount depends on numerous processes such as mineralization, immobilization, nitrification, denitrification, leaching, and plant uptake. Therefore, the study of mineral N may not represent the N availability during the crop growing. On the other hand, the study of organic N fractions and their transformations over time can help in predicting the N availability for crops, in estimating the N supply to the soil, and in evaluating the potential release of mineral N by organic fertilizers.
Many compounds account the soil organic N, being approximately 40% protein material (proteins, peptides, and amino acids), 5–6% amino sugars, 35% heterocyclic nitrogen compounds (including purines and pyrimidines), and 19% NH3, with ¼ fixed as NH4+. Thus, protein materials and heterocyclic compounds predominate in the total soil N, and organic N fractionation may inform about the mineralization susceptibility of compounds [6]. The organic N forms in soil have been studied by identifying and quantifying the released organic compounds when soils are acid treated at high temperature. The organic N fractions obtained by acid hydrolysis are hydrolyzable total N, subdivided into hydrolyzable NH4+-N, amino sugars-N, amino acids-N, and unidentified-N and acid insoluble N, a fraction that remains associated with soil minerals after acid hydrolysis [7].
The fractionation allows separating the labile N forms from the soil, such as amide-N and amino-N (acid hydrolyzable), which can be rapidly synthesized in the mineralization process, releasing inorganic N (NH4+ and NO3−) to the soil solution. However, most of the organic N can compose more stable fractions in the soil, such as non-hydrolyzable-N and unidentified-N. Variation in the non-hydrolyzable-N may be related to soil management, because the higher the hydrolysis intensity of organic N fractions in the soil, the higher the presence of finer particles that form clay-metal-humus complexes that constitute the non-hydrolyzed N. In Brazil, studies are reported in soils from Amazônia [8], São Paulo [9, 10, 11, 12], and Espirito Santo [13].
In Latosols and Argisols from Amazônia, determination of the organic N forms indicated that the immobilization was mainly from microbial origin and the 15N immobilized in the soil was found as acid-soluble N and undistilled-N [8]. In São Paulo, in sugarcane-cultivated soil, amino acid-N fractions predominated, and, after 12 weeks incubation, the total hydrolyzable-N did not vary, but the hydrolyzable NH4+-N decreased [9]. In soil samples under different cover plants [10], the amino acid-N fraction predominated, with the following distribution: 14–38% hydrolyzable NH4+-N, 36–52% adenosine triphosphate as NH4+-N + amino sugars, 10–32% amino sugar-N, 26–46% amino acid-N, and 3–28% unidentified-N.
Moreover, in São Paulo, in a soil under maize cultivation, it was observed that topdressing N fertilization decreased the N content of the most labile fractions (hydrolyzable NH4+-N and amino sugars-N) in the surface layer of the soil, and the amino acid-N and amino sugar-N fractions were considered the organic N reservoirs that control the soil N availability [11]. In contrast, fertilization with cattle manure [12] increased the most easily mineralized (up to 100 days) organic N fractions and subsequently increased the more stable organic N fractions, mainly in clay soil. In Espirito Santo, in soil under eucalyptus, [13] observed that the amino-N was predominant (39%), followed by unidentified-N (27%), amide-N (18%), and hexosamine-N (15%).
Several theories have been developed to explain the resistance of some N compounds to microbial attack. It is mentioned that N compounds are probably protein constituents (amino acids, peptides, and proteins) that are stabilized by reactions with lignins, tannins, quinones, and reducing sugars. Moreover, N compounds would adsorb to the clay fraction of soil and thereby would be protected against the action of protease enzymes. Also, the formation of organic N complexes and polyvalent cations (iron and aluminum) is another biologically stable form of protection [14]. Accumulation and/or decrease of organic C and N is more dynamic in sandy soils than in clayey ones, probably due to the highest oxygenation capacity and lower residue input of sandy soils due to its low productive potential, which gives it less resilience.
Advertisement
3. Nitrogen mineralization and immobilization in the agricultural systems
Nitrogen mineralization and immobilization are biochemical processes widely discussed in the literature. We will focus on how these processes occur in the agricultural system. N mineralization occurs through hydrolysis and biodegradation of soil organic matter when N content in the substrate exceeds the metabolic N requirement by microbial cells. The process is mediated by heterotrophic soil microorganisms [15] that use nitrogenous organic substances as a source of C, N, and energy, releasing NH4+ ions as a residue (ammonification). In its turn, immobilization is defined as the transformation of inorganic N (NH4+, NH3, NO3−, NO2−) to microbial forms. Microbiota assimilates inorganic forms of N by incorporating them into the amino acids, which will participate in protein synthesis during soil biomass formation [14].
N mineralization and immobilization occur simultaneously and oppositely in the soil. The net balance between these processes is controlled by several factors: (a) environmental, such as soil temperature, aeration, and moisture; (b) soil physical, such as texture, structure, and size of aggregates [16]; (c) soil chemical, such as pH; (d) agricultural management system adopted [17]; and (e) quality parameters of the decomposing waste (such as C/N, C/P, and C/S ratios), content of easily decomposable and recalcitrant fractions, type of associated decomposers, size and activity of microbial biomass, and inorganic N availability [18]. Carbon/nitrogen (C/N) ratio less than 25 in organic waste favors N mineralization and fast decomposition, while greater than 30 strongly favors N immobilization and fast decomposition [19]. The crop developmental stage also influences waste C/N ratio. For instance, wastes from millet plants cut at the flowering or milky grain stages present high C/N ratio which delays mineralization. On the other hand, wastes from millet cut at the flag leaf stage, even though phytomass is lower, present less C/N ratio which favors N mineralization for the next crop [20].
In residue plant, considering 13C-CPMAS NMR spectral regions [21], observed that the carbonyl C and N-alkyl and methoxyl C regions had the most significant positive correlation with N mineralization, while the di-O-alkyl C and O-alkyl C were strongly associated with N immobilization. This study demonstrates that the biochemical quality of organic C defined by 13C-CPMAS NMR is capable of predicting N dynamic pattern better than C/N ratio. Abbasi et al. [22] observed positively correlated with the initial residue N contents and negatively correlated with lignin content C/N ratio, lignin/N ratio, polyphenol/N ratio, and (lignin + polyphenol)/N ratio indicating a significant role of residue chemical composition and quality in regulating N transformations and cycling in soil.
In the N compartments, N from the most labile fractions is released in the early mineralization process, and its mineralization estimate can be used to adjust the nitrogen fertilization recommendations. In fact, it was observed that the mineralization potential and the respective mineralization rate can be used to predict the N availability for plants in the agricultural system. Camargo et al. [23] found that the potentially mineralizable nitrogen values in 10 soils from Rio Grande do Sul ranged from 108.6 to 210.8 mg kg−1.
In respect to the management system adopted, time is essential for N mineralization, mainly in the no-tillage (NT) system. Siqueira et al. [24] found that in soil under NT system for 12 and 22 years, the averages for N mineralization were 0.19 and 0.26 g m−2 day−1, respectively. For organic compounds such as sludge, the N mineralization rate is generally below 50%, 5–38% [25], 14–43% [26], 7–16% [27], and 24–31% [28]. Among the species used in straw production, Fabaceae plants stand out for fixing atmospheric N2 and presenting low C/N ratio tissues, in addition to the high soluble compound content and low lignin and polyphenol contents. This fact favors the fast decomposition and mineralization, with significant N input to the soil–plant system, but with reduced soil cover, which is essential for NT system [29]. On the other hand, Poaceae plants present relatively high dry matter content and high C/N ratio (> 30), which increase the persistence of soil cover although increase N immobilization [30, 31].
Advertisement
4. Nitrogen volatilization and denitrification
Volatilization is the main cause of N loss where ammonia gas (NH3) is produced according to the simplified equation: NH4+ + OH− ↔ NH3(g) + H2O. NH3 loss increases with increasing soil pH. Ammonium ion (NH4+) can be adsorbed by soil colloids (clays in humus); thus the largest losses are found in sandy soils and poor in soil organic matter (SOM). Denitrification is another factor that favors N loss, which is mainly controlled by organic matter content, pH, and soil temperature. This process is performed by anaerobic bacteria such as
NH3 losses by volatilization in agriculture occur due to many factors: ambient temperature, soil moisture at fertilization time, urease enzyme activity, soil pH, cation exchange capacity, soil cover, rainfall after fertilization, and SOM content [33, 34]. Tasca et al. [34] reported 4.6-fold less NH3 volatilization when topdressing urea was performed at 18°C temperature, compared to 35° C, which demonstrates that N losses increase with increasing temperature. Low volatilization rates are also reported under higher soil moisture values, around 20%, because fertilizer hydrolysis facilitates the NH4+ diffusion, making it less susceptible to volatilization, even considering the increased soil biological activity in that moisture. In contrast, higher N losses occur under around 10% humidity values, because the NH4+ incorporation is inefficient, resulting in higher N-NH3 emissions [34]. Moreover, NH3 losses by volatilization are higher during the driest periods of the year. Soil moisture at fertilization time directly interferes with urea hydrolysis and consequently with NH3 volatilization losses. Thus, soil wetting soon after urea application is more important than the soil moisture at the application time [35]. According to Ros et al. [36], water applied after urea fertilization or the occurrence of rainfall may decrease NH3 volatilization if it is sufficient to dilute the hydroxyl (OH−) concentration around the urea granules produced during the hydrolysis, besides providing the incorporation of urea in the soil.
Plant cover also influences N-NH3 volatilization. Pinheiro [37] found the removal of sugarcane straw from the soil decreased NH3 volatilization rates. The analysis of topsoil and straw indicated higher urea and NH4+ retention in the largest amounts of straw on the soil, besides effective urea hydrolysis occurring directly in the straw. These results demonstrated a direct contribution of the straw mulches on NH3 volatilization. However, despite NH3 volatilization decreases with straw removal, the choice of straw amount to be removed cannot be based only on NH3 volatilization of N fertilizer. Analyzing fertilizer mixtures in laboratory, Vitti et al. [38] found that mixing urea (330 mg) with ammonium sulfate (300 mg) significantly reduced N-NH3 losses (97.47 mg) relative to urea (121.52 mg), without affecting the physicochemical quality attributes of the mixture for technical and agronomic efficiency purpose. In Brazil, urea is the most used mineral N fertilizer, but it has volatilization losses due to the enzymatic hydrolysis that consumes H+ and increases soil pH. For that reason, even in acidic soils, urea is subject to N losses by volatilization [39]. In agricultural systems, the largest N losses by volatilization occur 3–5 days after fertilizer application [40]. Santos [41] observed that from total N-NH3 loss by volatilization, 92.5% occurred until the fifth day after fertilization, negatively affecting the corn grain yield.
Fertilizer type may also influence N-NH3 volatilization. The application of polymer and organic compound-coated urea promoted the lowest ammonia losses by volatilization [42, 43]. In soil under pasture (
The use of liquid and solid organic biofertilizers such as poultry and swine residues are also alternative means to reduce N losses, since N is present in biofertilizers as organic form, thereby requiring more time to be mineralized by microorganisms for plant uptake. Niraula et al. [47] reported that cattle manure applied in corn had 11% lower cumulative NH3 emission than urea, without affecting grain yield, despite having higher CO2 and CH4 emissions. Thus, after comparing the ammonia volatilization levels reported in 92 studies, Bouwman et al. [48] concluded that the average NH3 emissions from the synthetic urea fertilizer and manure slurry were 21.0 and 21.2% from applied N fertilizer, respectively. Moreover, acidification has been a resource used to minimize urea volatilization with liquid waste. Park et al. [49] observed the application of acidified slurry reduced NH3 emissions by 78.1%, N2O emissions by 78.9%, and NO3− leaching by 17.81% compared to control (non-pH-controlled pig slurry), over the course of the experiment.
Quantifying ammonia volatilization from various organic N sources (castor bean cake, bokashi, legume fertilizers, cattle manure), Rocha et al. [50] observed (i) the N loss rate by NH3 volatilization varies from 3 to 25% in winter/spring and 2 to 38% in summer/autumn among the studied organic fertilizers; (ii) when incorporating organic fertilizers into the soil, volatilization was significantly lower than when they are maintained on the soil surface, with a volatilization reduction by 80% for castor cake, 78% for bokashi, and 67% for legume fertilizer, while for cattle manure there was no difference; and (iii) when on surface, potential NH3 volatilization from the total N applied in winter/spring and summer/autumn seasons, respectively, was 25.5 and 38.1% for castor cake, 16.6 and 13.7% for bokashi, 8.2 and 8.8% for legume fertilizer, and 3.4 and 2.4% for cattle manure.
In Planosol under irrigated rice, the addition of cover plants on the soil and water management by intermittent irrigation were practices that mitigated N2O emissions. Zschornack et al. [51] observed an increase in N2O emissions by more than 200% in a drained area than continuous water blade area. Thus, soil drainage during rice cultivation increases N2O emissions by stimulating nitrification and denitrification processes. In addition, N2O emissions depend on the input waste quality and increase significantly when legumes are inserted into cover plants. Moreover, analyzing biochar in rice, He et al. [52] suggested that the combination of biochar and HQ (urease inhibitor-hydroquinone) or the combined application of urease and nitrification inhibitors to soil enriched with biochar at least 1 year previously could be an effective practice for reducing NH3 emissions and increasing rice yields.
Finally, microorganism respiration may also contribute to retaining N into the soil. By dissimilatory nitrate reduction to ammonium (DNRA), a respiratory process antagonistic to denitrification, nitrate is used by microorganisms, mainly
Advertisement
5. Soluble nitrogen
Soluble organic nitrogen is a labile source of N for microorganisms and is an important soluble N reservoir in agricultural soils. Plant species (associated or not with mycorrhizae) can directly uptake simple organic N present in the SON pool [55]. The SON pool is composed of high (protein oligomers), medium (small peptides) [56], and low molecular weight compounds (monomers such as amino acids) [57]. As plants uptake organic and inorganic N, the relative proportion of these different N sources in soils is a determinant of N management.
SON is suggested as a transitional phase during N transformation between soil organic matter and inorganic N (NH4+-N) and considered an intermediate step in microbial mineralization of organic N [58]. The SON pool can regulate the N transformation rate in the soil, i.e., the ammonification and nitrification rates, affecting the substrate associated with different plant species. Thus, soil organic N fractions and SON pools are important indicators of soil fertility and plant nutrition requirements [59], inferring the potential supply of N mainly in low N mineralization soils [60].
Besides an important component of soil total soluble N, SON plays a key role in N cycling and therefore in determining soil N availability in agricultural systems [61]. The amount of SON represents a relatively high proportion of the total soluble nitrogen (TSN) pool. It has been reported that SON constitutes 17–90% and 32–50% of TSN in pasture and agricultural soils, respectively [46, 47, 62, 63]. Like in mineral N, SON dynamics are affected by mineralization, immobilization, leaching, and plant uptake, but its pool size is more constant than mineral N [64]. Although remains unclearly understood, SON is an important pool in N transformations and plant uptake.
Biotic and abiotic processes are involved in the SON generation in soil [58]. By biotic processes, SON can be produced directly from microbial turnover and indirectly through the microbial excretion of extracellular enzymes [61]. However, as plants and microorganisms can compete for soil organic N, it is also possible that SON reservoirs vary spatially due to the variation in activity and density of microbial population between different types of agricultural management. Zhang et al. [65] reported that SON fractions were significantly and positively correlated with the no-tillage system practices and that this agricultural system is beneficial and effective for increasing soil N turnover.
Proteins are the most abundant nitrogen compounds in SON. Depolymerization of these organic macromolecules in monomeric SON (amino acids) can be considered rate-limiting for the total N cycling in soils [66]. Soil amino acids can contribute, in relative and absolute terms, to the SON pool in agricultural soils, which was observed in soil under fertilized sugarcane [55]. Also, plants can use proteins as N source without the help of other organisms [67]. Although the relative contribution of amino acids to N supply for crops remains unclear, all studied plants have shown the ability to uptake and metabolize amino acids as well as soils containing amino acids [68].
Organic agriculture practices can increase the content of SON, protein, and free amino acids in the soil as a result of frequent and long-term inputs of organic matter. In addition, agricultural production quantity may also influence the SON pool abundance. However, the effect of organic cultivation on specific free amino acids and protein pools remains unclear [66].
Soil organic matter, pH, total C, total N, and C/N ratio are the main factors affecting soil SON abundance. SON dynamics can be significantly affected by mineralization and immobilization during microbial growth and decomposition of organic matter. Besides that, agricultural practices such as irrigation management, fertilization, plowing, harrowing, harvesting, and the plant growth stage can also play an important role in SON dynamics [59, 63]. Furthermore, high temperatures may increase the SON content by stimulating decomposition of organic matter [69]. Knowing the temporal dynamics of organic N pools in the soil may help to understand how these pools are affected by soil properties, climate and crop management, and whether SON can contribute to N supply of crops.
Advertisement
6. Biological nitrogen fixation
Nitrogen in the gaseous form (N2) represents 78% of the atmospheric gases but is inert and unavailable to plants. Only nitrogen-fixing microorganisms, including bacteria, cyanobacteria, and fungi, are able to break the triple bond between the atoms (N ≡ N) of the atmospheric nitrogen, thus transforming it into ammonia (NH3) through the nitrogenase enzyme (N2 + 8H+ + 6e− → 2NH3 + H2) [70]. Biological nitrogen fixation is a key component of the nitrogen cycle and responsible for most of the nitrogen available to plants.
BNF is performed by symbiotic, endophytic, or free-living microorganisms [71, 72]. Symbiotic bacteria associate with plants forming root nodules (rhizobia), where they fix nitrogen while benefiting from plant photoassimilates. It has been observed that this symbiosis occurs not only in plants from the Leguminosae family [71] but also in cereals such as rice, maize, and wheat from the Poaceae family [73]. BNF also occurs in nonsymbiotic associations. Endophytic bacteria colonize plant tissues and fix N while benefiting from plant photoassimilates, although the amount of N fixed is lower than in symbiosis [73, 74]. Also, free-living microorganisms inhabiting rhizosphere, soil region around plant roots, fix nitrogen while feeding on root exudates (amino acids, peptides, proteins, enzymes, vitamins, and hormones), which stimulate growth of diazotrophic bacteria from genera
Nitrogen-fixing microorganisms occur naturally in soil [71] and in water [72] or colonize seeds [74]. However, in the agricultural environment, conventional practices such as plowing, harrowing, chemical fertilization, and pesticide application reduce the soil microorganism populations, which make these areas depending on the application of nitrogen fertilizers [75, 76]. Chemical fertilizers require a great amount of energy to be produced, energy that is derived from fossil fuels. Moreover, they are potential soil and water contaminants and expensive and scarce for many developing country farmers [77]. Therefore, strategies have been studied to increase BNF by plants and thus reduce dependence on chemical fertilization.
Conservation practices such as minimum tillage, no tillage, and cover crops stimulate BNF as they increase the population and activity of soil microorganisms (bacteria, actinomycetes, and mycorrhizae) [78, 79]. In addition to capturing soil N, reducing N loss by leaching, and becoming an N source for succeeding crops, mixing cover crops (legumes and grasses) provide additional N through BNF [79, 80].
Another alternative for increasing BNF is to inoculate nitrogen-fixing microorganisms in crops. Inoculated into the seeds, roots, or leaves, these microorganisms may increase the formation of root nodules, stimulate root growth, improve nutrient uptake, stimulate antioxidant defense system, increase tolerance to biotic (pest and pathogen) and abiotic (drought and salinity) stresses, and thereby increase crop productivity. Inoculation of nodulating as well as endophytic fungi or bacteria stimulates growth in both legumes and grasses and represents a viable and sustainable alternative (Table 1). Among the most used microorganisms are
| Rice | [81, 82] | ||
| Sugarcane | [83] | ||
| Cowpea | [84, 85, 86, 87, 88] | ||
| Common bean | [89] | ||
| Maize | [90, 91] | ||
| Soybean | [92, 93] | ||
| Wheat | [94, 95] |
Table 1.
Studies also focus on the application of nitrogen-fixing microorganisms through irrigation water, on the genetic improvement for BNF by legume crops [96], on becoming plants able to self-fertilize by stimulating root fungal associations in grasses, and on providing cereals with the nitrogen-fixing enzyme (nitrogenase) [77]. Estimations indicate these practices can reduce fertilizer application costs by billions of dollars annually.
Advertisement
7. Nitrogen and organic fertilization
The worldwide demand for organic foods, produced without the use of synthetic inputs, has driven the use of conservation practices, especially fertilization using organic wastes. The application of organic wastes to the soil improves soil fertility by increasing the organic matter (OM) and nutrient contents, such as N and phosphorus (P), and soil microbiota population, as well as improving the cation exchange capacity (CEC) [97].
Organic fertilization improves yield and quality of vegetables such as lettuce (
| Cattle manure | 0.8–3.2 | 16.0–21.0 | [97, 106] |
| Equine manure | 1.4–3.9 | 21.9–25.0 | [97, 107] |
| Sheep manure | 1.2–1.8 | 9.0–29.0 | [108, 109] |
| Swine manure | 1.9–2.8 | 10.0–12.0 | [97, 107] |
| Poultry litter | 2.8–4.6 | 4.2–22.0 | [97, 106, 107] |
| Blood meal1 | 11.8–12.9 | — | [110, 111] |
| Bone meal | 4.1–4.2 | 4.0–7.0 | [97, 112] |
| Meat and bone meal | 5.5–6.6 | 6.0 | [106, 112, 113] |
| Castor pulp1 | 12.8 | — | |
| Castor pie | 5.2–7.5 | 6.0–9.0 | [97, 106, 112] |
| Cotton pie1 | 4.5 | — | [106] |
| Filter pie | 1.5–1.8 | 21.0–24.0 | [97, 112] |
| Sugarcane bagasse | 0.9–1.5 | 85.0 | [106, 111, 114] |
| Vinasse | 0.3–1.2 | 4.0–17.0 | [97, 112] |
| Compost | 0.7–2.6 | 11.3–64.0 | [107, 115] |
| Humus | 1.3–2.6 | 11.0–34.0 | [115, 116] |
| Millicompost | 2.0–2.2 | 15.0–19.0 | [98, 117] |
| Biochar | 0.1–5.0 | 7.0–400.0 | [118] |
| Sewage sludge | 0.8–3.5 | 9.0–50.0 | [97, 112] |
| Household waste | 0.9–2.6 | 7.0–27.0 | [97, 107, 112] |
Table 2.
Nitrogen content and carbon/nitrogen ratio (C/N) in organic fertilizers.
C/N ratio not found.
N input by organic fertilizers occurs predominantly through mineralization of organic N, although some mineral N fractions may be released [107, 119]. The organic N mineralization rate is regulated by N fractions and C/N ratio of the decomposing waste, as well as by environmental temperature and humidity [120, 121]. Under favorable conditions, high N content organic fertilizers mineralize quickly similarly to synthetic fertilizers, while those with low N content and high C/N ratio mineralize slowly [122]. Thus, knowing the mineralization rate allows choosing the best organic fertilizer to be used in agriculture (Table 2).
Manures are the main used organic fertilizers worldwide, especially as N source, though the amount and quality of N in manure may vary according to animal species, age, and feed. Forage-based diets increase the residue production, although reduce the quality that is provided by a concentrate-based diet [97, 119]. Cattle, equine, sheep, goat, and swine manures present similar N content, ranging from 0.77 to 3.90%. In its turn, poultry litter may have 2.80–4.60% N content, due to concentrate-based feed supplied to poultries, being a fast mineralizing fertilizer [106, 107]. Thus, manure fertilization has been efficient for many crops, such as sweet pepper (
Residues from the castor bean (
The product obtained from the composting of organic wastes is rich in stable organic matter. Wastes are transformed through biological decomposition, and the process is affected by environmental conditions and N content. As nitrogen compounds are food for microbiota, N deficiency in waste may retard the maturation process, and the excess may increase the N volatilization as ammonia (NH3), consequently affecting N stabilization processes in composting [130]. Also, humus from vermicomposting (usually by using
In addition to the earthworms, arthropods that constitute the edaphic macrofauna [87, 132, 133] are also of great interest. Millipedes (Myriapoda: Diplopoda) fragment and feed on organic wastes and excrete low C/N ratio feces (2.2% N) producing the millicompost [134, 135, 136]. Studies suggest that millicompost is similar to vermicompost and commercial substrates in relation to N supply and other macro- and micronutrients for seedling production, such as in lettuce (
In relation to slow-release organic fertilizers, biochar is an alternative. A by-product from carbonization (pyrolysis) of biomass under low-oxygen atmosphere, biochar is fine-grained carbonaceous material with decomposition resistance [118]. N content in biochar depends on the source material (biomass) as well as on the pyrolysis temperature. Biochars from wood have high C/N ratio and low N content (0.1%), while those from manures have low C/N ratio and high N content (5.0%). For instance, biochar from eucalyptus wood (
Urban wastes have also been used in agriculture. Sewage sludge showed to be an excellent N source (0.80 and 3.47% N) besides slowly mineralizing. N mineralization rates from 20 to 38% were found after 105 days [143], which depends on source material characteristics and treatment processes as well as on heavy metal content that accelerate or limit mineralization [107, 144]. Slaughterhouse residues, such as bone and blood meal, present high N rates, but they are not yet used in agriculture because studies on its adoption and behavior as organic fertilizer are scarce [97, 110, 112].
Advertisement
8. Concluding remarks
In the surface layer of most soils, the soil organic N can be divided into two categories: N from organic residues and N from soil organic matter or humus. N mineralization and immobilization processes occur simultaneously and oppositely in the soil. The net balance between these processes is controlled by several factors such as environmental conditions, soil physicochemical factors, agricultural management adopted, quality of the decomposing residues, and content of easily decomposable and recalcitrant fractions. As organic agriculture increases soluble organic nitrogen content, this fraction has been extensively studied. Also, being biological nitrogen fixation a key component of the nitrogen cycle and responsible for most of the nitrogen available to plants, it was also discussed in this chapter.
Finally, we discussed nitrogen and organic fertilization, since the worldwide demand for organic foods produced without the use of synthetic inputs has driven the use of conservation practices, especially fertilization using organic wastes. Most organic fertilizers used as N source is derived from agricultural and agro-industrial wastes, slaughterhouse wastes, composting and vermicomposting, biochars, household wastes, and sewage sludge composting.
References
- 1.
Kelley KR, Stevenson FJ. Forms and nature of organic N in soil. Fertilizer Research. 1995; 42 :1-11. DOI: 10.1007/BF00750495 - 2.
Nguyen TH, Shindo H. Effects of different levels of compost application on amounts and distribution of organic nitrogen forms in soil particle size fractions subjected mainly to double cropping. Agricultural Sciences. 2011; 2 :213-219. DOI: 10.4236/as.2011.23030 - 3.
Harper JE. Nitrogen metabolism. In: Boote KJ, Bennett JM, Sinclair TR, et al., editors. Physiology and Determination of Crop Yield. Madison: ASA/CSSA/SSSA. Chapt. 11A; 1994. pp. 285-302 - 4.
Bredemeier C, Mundstock CM. Regulation of nitrogen absortion and assimilation in plants. Ciência Rural. 2000; 30 :365-372 - 5.
Olk CO. Organic forms of soil nitrogen. In: Schepers JS, Raun WR, editors. Nitrogen in Agricultural Systems. Madison, USA: American Society of Agronomy; 2008. pp. 57-100 - 6.
Schulten HR, Schnitzer M. The chemistry of soil organic nitrogen: A review. Biology and Fertility of Soils. 1998; 26 :1-15 - 7.
Stevenson FJ. Nitrogen-organic forms. In: Page AL, editor. Methods of Soil Analysis: Chemical and Microbiological Properties. Part 2. Madison, USA: Soil Science Society of America; 1982. pp. 625-641 - 8.
Alfaia S. Caracterização e distribuição das formas do nitrogênio orgânico em três solos da Amazônia Central. Acta Amazonica. 2006; 36 :135-140 - 9.
Otto R, Mulvaney RL, Khan SA, Trivelin PCO. Quantifying soil nitrogen mineralization to improve fertilizer nitrogen management of sugarcane. Biology and Fertility of Soils. 2013; 1 :1-12. DOI: 10.1007/s00374-013-0787-5 - 10.
Kuhnen F. Mineralização de Nitrogênio de solos e de resíduo orgânico em laboratório e em campo [thesis]. Jaboticabal-SP: Universidade Estadual Paulista “Júlio d Mesquita Filho”; 2013. 64p - 11.
Bergamasco MAM. Formas de N-orgânico em Latossolo em função de Nitrogênio e de plantas de cobertura em pré-safra do milho [thesis]. Jaboticabal-SP: Universidade Estadual Paulista “Júlio d Mesquita Filho”; 2015. 44p - 12.
Adame CR. Formas de nitrogênio orgânico em solos tratados com esterco bovino. [thesis]. Jaboticabal-SP: Universidade Estadual Paulista “Júlio d Mesquita Filho”; 2018. 45p - 13.
Pegoraro RF, Silva IR, Novais RF, Barros NF, Cantarutti RB, Fonseca S. Abundância natural de 15N e formas de nitrogênio em Argissolo cultivado com Eucalipto e Acácia. Ciência Florestal. 2016; 26 :295-305 - 14.
Camargo FAO, Silva LS, Gianello C, Tedesco MJ. Nitrogênio orgânico do solo. In: Santos GA et al., editors. Fundamentos da matéria orgânica do solo. Porto Alegre-RS, Brazil: Metropole; 2008. pp. 87-100 - 15.
Rigby H, Clarke BO, Pritchard DL, Meehan B, Beshah F, Smith SR, et al. A critical review of nitrogen mineralization in biosolids-amended soil, the associated fertilizer value for crop production and potential for emissions to the environment. The Science of the Total Environment. 2016; 541 :1310-1338. DOI: 10.1016/j.scitotenv.2015.08.089 - 16.
Bimüller C, Kreyling O, Kölbl A, von Lützow M, Kögel-Knabner I. Carbon and nitrogen mineralization in hierarchically structured aggregates of different size. Soil and Tillage Research. 2016; 160 :23-33 - 17.
Kristensen HL, Debosz K, Mccarty GW. Short-term effects of tillage on mineralization of nitrogen and carbon in soil. Soil Biology and Biochemistry. 2003; 35 :979-986. DOI: 10.1016/S0038-0717(03)00159-7 - 18.
Moreira FMS, Siqueira JO. Microbiologia e bioquímica do solo. 2nd ed. Atual. e ampl. Editora UFLA: Lavras; 2006. 729p - 19.
Cantarella H. Nitrogênio. In: Novais RF, Alvarez VVH, Brarros NF, Fontes RLF, Cantaruti RB, Neves JCL, editors. Fertilidade do solo. 1st ed. Viçosa, MG: Sociedade Brasileira de Ciência do Solo; 2007. pp. 375-470 - 20.
Folini JSS, Catuchi TA, Barbosa AM, Calonego JC, Tititan CS. Acúmulo de nutrientes e relação C/N em diferentes estádios fenológicos do milheto submetido à adubação nitrogenada. Revista Agro@mbiente Online. 2016; 10 :1-9 - 21.
Bonanomi G, Sarker TC, Zotti M, Cesarano G, Allevato E, Mazzoleni S. Predicting nitrogen mineralization from organic amendments: Beyond C/N ratio by 13C-CPMAS NMR approach. Plant and Soil. 2019; 101 :1-18. DOI: 10.1007/s11104-019-04099-6 - 22.
Abbasi MK, Tahir MM, Sabir N, Khurshid M. Impact of the addition of different plant residues on nitrogen mineralization–immobilization turnover and carbon content of a soil incubated under laboratory conditions. Solid Earth. 2015; 6 :197-205. DOI: 10.5194/se-6-197-2015 - 23.
Camargo FAO, Gianello C, Vidor C. Potencial de mineralização do nitrogênio em solos do Rio Grande do Sul. Revista Brasileira de Ciência do Solo. 1997; 21 :575-579 - 24.
Siqueira Neto M, Piccolo MC, Venzke Filho SP, Feigl BJ, Cerri CC. Mineralização e desnitrificação do nitrogênio no solo sob sistema plantio direto. Bragantia. 2010; 69 :923-936 - 25.
Alcântara MAK, Aquino Neto V, Camargo OA, Cantarella H. Mineralização do nitrogênio em solos tratados com lodos de curtume. Pesquisa Agropecuária Brasileira. 2007; 42 :547-555. DOI: 10.1590/S0100-204X2007000400013 - 26.
Boeira RC, Maximiliano VCB. Mineralização de compostos nitrogenados de lodos de esgoto na quinta aplicação em Latossolo. Revista Brasileira de Ciência do Solo. 2009; 33 :711-722. DOI: 10.1590/S0100-06832009000100022 - 27.
Andrade CA, Silva LFM, Pires AMM, Coscione AR. Mineralização do carbono e do nitrogênio no solo após sucessivas aplicações de lodo de esgoto. Pesquisa Agropecuária Brasileira. 2013; 48 :536-544. DOI: 10.1590/ S0100-204X2013000500010 - 28.
Pires AMM, Andrade CA, Souza NAP, Carmo JB, Coscione AR, Carvalho CS. Pesquisa Agropecuária Brasileira. 2015; 50 :333-342. DOI: 10.1590/S0100-204X2015000400009 - 29.
Ferreira EPB, Stone LF, Partelli FL, Didonet AD. Produtividade do feijoeiro comum influenciada por plantas de cobertura e sistemas de manejo do solo. Revista Brasileira de Engenharia Agrícola e Ambiental. 2011; 15 :695-701 - 30.
Perin A, Santos RHS, Urquiaga S, Guerra JGM, Cecon PR. Produção de fitomassa, acúmulo de nutrientes e fixação biológica de nitrogênio por adubos verdes em cultivo isolado e consorciado. Pesquisa Agropecuária Brasileira. 2004; 39 :35-40. DOI: 10.1590/S0100-204X2004000100005 - 31.
Favarato LF, Souza JL, Galvão JCC, Souza CM, Guarconi RC, Balbino JMS. Crescimento e produtividade do milho-verde sobre diferentes coberturas de solo no sistema plantio direto orgânico. Bragantia. 2016; 75 :497-506. DOI: 10.1590/1678-4499.549 - 32.
Machado CJ. Aplicação de fertilizantes com diferentes tecnologias:volatilização de NH3 [thesis]. Uberlândia-MG: Universidade Federal de Uberlândia- MG; 2015. 62p - 33.
Rodrigues JO, Partelli FL, Pires FR, Oliosi G, Espindula MC, Monte JA. Volatilização de amônia de ureias protegidas na cultura do cafeeiro conilon. Coffee Science. 2016; 11 :530-537 - 34.
Tasca FA, Ernani PR, Rogeri DA, Gatiboni LC, Cassol PC. Volatilização de amônia do solo após a aplicação de ureia convencional ou com inibidor de urease. Revista Brasileira de Ciência do Solo. 2011; 35 :493-502 - 35.
Lima JES, Nascente AS, Silveira PM, Leandro WM. Volatilização da amônia da ureia estabilizada com NBPT na adubação em cobertura da Urochloa ruziziensis . Colloquium Agrariae. 2018;14 :92-100 - 36.
Ros COD, Aita C, Giacomini SJ. Volatilização de amônia com aplicação de uréia na superfície do solo, no sistema plantio direto. Ciência Rural. 2005; 35 :799-805. DOI: 10.1590/S0103-84782005000400008 - 37.
Pinheiro PL. Interação entre remoção de palha e adubação nitrogenada sobre a volatilização de NH3 e emissão de N2O na cultura da cana-de-açúcar[thesis]. Santa Maria-RS: Universidade Federal de Santa Maria; 2018. 82p - 38.
Vitti GC, Tavares Jr JE, Luz PHC, Favarin JL, Costa MCG. Influência da mistura de sulfato de amônio com uréia sobre a volatilização de nitrogênio amoniacal. Revista Brasileira de Ciência do Solo. 2002; 15 :663-671 - 39.
Barberena IM, Espindula MC, Araújo LFB, Marcolan AL. Use of urease inhibitors to reduce ammonia volatilization in Amazonian soils. Pesquisa Agropecuária Brasileira. 2019; 54 :1-9. DOI: 10.1590/s1678-3921.pab2019.v54.00253 - 40.
Cancellier EL, Silva DRG, Faquin V, Gonçalves B, Almeida B, Cancellier LL, et al. Ammonia volatilization from enhanced-efficiency urea on no-till maize in brazilian cerrado with improved soil fertility. Ciência e Agrotecnologia. 2016; 40 :133-144. DOI: 10.1590/1413-70542016402031115 - 41.
Santos WM. Desempenho agronômico e volatilização da amônia de fertilizantes pastilhados e convencionais na cultura de milho[thesis]. São Cristóvão-SE: Universidade Federal de Sergipe; 2017. 69p - 42.
Lorensini F, Ceretta CA, Girotto E, Cerini JB, Lourenzi CR, Trindade LCMM, et al. Lixiviação e volatilização de nitrogênio em um Argissolo cultivado com videira submetida à adubação nitrogenada. Ciência Rural. 2012; 42 :1173-1179 - 43.
Siqueira ETJ. Avaliação de fontes de nitrogênio na produção de cana-de-açúcar, aporte de matéria orgânica no solo e perdas por volatilização de amônia [thesis]. Chapadinha-MA: Universidade Federal do Maranhão; 2018. 62p - 44.
Lana RMQ , Pereira VJ, Leite CN, Teixeira GM, Gomes JS, Camargo R. NBPT (urease inhibitor) in the dynamics of ammonia volatilization. Revista Brasileira de Ciência Agrária. 2018; 13 :1-8 - 45.
Oliveira JÁ, Stafanato JB, Goulart RS, Zonta E, Lima E, Mazur N, et al. Volatilização de amônia proveniente de ureia compactada com enxofre e bentonita, em ambiente controlado. Revista Brasileira de Ciência do Solo. 2014; 38 :1558-1564. DOI: 10.1590/S0100-06832014000500021 - 46.
Gurgel GCS, Ferrari AC, Fontana A, Polidoro JC, Coelho LAM, Zonta E. Volatilização de amônia proveniente de fertilizantes minerais mistos contendo ureia. Pesquisa Agropecuária Brasileira. 2016; 51 :1686-1694 - 47.
Niraula S, Rahman S, Chatterjee A, Cortus EL, Mehata M, Spiehs MJ. Beef manure and urea applied to corn show variable effects on nitrous oxide, methane, carbon dioxide, and ammonia. Agronomy Journal. 2018; 11 :1448-1467 - 48.
Bouwman AF, Boumans LJM, Batjes NH. Estimation of global NH3 volatilization loss from synthetic fertilizers and animal manure applied to arable lands and grasslands. Global Biogeochemical Cycles. 2002; 16 :8-13 - 49.
Park SH, Lee BR, Jung KH, Kim TH. Acidification of pig slurry effects on ammonia and nitrous oxide emissions, nitrate leaching, and perennial ryegrass regrowth as estimated by 15N-urea flux. Asian-Australasian Journal of Animal Sciences. 2018; 31 :457-466 - 50.
Rocha AA, Araújo ES, Santos SS, Goulart JM, Espindola JAA, Guerra JGM, et al. Ammonia volatilization from soil-applied organic fertilizers. Revista Brasileira de Ciência do Solo. 2019; 43 :1-10. DOI: 10.1590/18069657rbcs20180151 - 51.
Zschornack T, Rosa CM, Camargo ES, Reis CES, Schoenfeld R, Bayer C. Impacto de plantas de cobertura e da drenagem do solo nas emissões de CH4 e N2 O sob cultivo de arroz irrigado. Pesquisa Agropecuária Brasileira. 2016; 51 :1163-1171. DOI: 10.1590/S0100-204X2016000900016 - 52.
He T, Deyan L, Yuan J, Ni K, Zaman M, LUO J, et al. A two years study on the combined effects of biochar and inhibitors on ammonia volatilization in an intensively managed rice field. Agriculture, Ecosystems and Environment. 2018; 264 :44-53 - 53.
Otto R, Zavaschi E, Souza Netto GJM, Machado BA, Mira AB. Ammonia volatilization from nitrogen fertilizers applied to sugarcane straw. Revista Ciência Agronômica. 2017; 48 :413-418.b. DOI: 10.5935/1806-6690.20170048 - 54.
Suleiman MF, Wagner-Riddle C, Brown SE, Warland J. Greenhouse gas mitigation potential of annual and perennial dairy food production systems. Agriculture, Ecosystems and Environment. 2017; 245 :52-62. DOI: 10.1016/j.agee.2017.05.001 - 55.
Holst J, Brackin R, Robinson N, Lakshmanan P, Schmidt S. Soluble inorganic and organic nitrogen in two Australian soils under sugarcane cultivation. Agriculture, Ecosystems and Environment. 2012; 155 :16-26. DOI: 10.1016/j.agee.2012.03.015 - 56.
Moran-Zuloaga D, Dippold M, Glaser B, Kuzyakov Y. Organic nitrogen uptake by plants: Reevaluation by position-specific labeling of amino acids. Biogeochemistry. 2015; 125 :359-374. DOI: 10.1007/s10533-015-0130-3 - 57.
Brackin R, Näsholm T, Robinson N, Guillou S, Vinall K, Lakshmanan P, et al. Nitrogen fluxes at the root-soil interface show a mismatch of nitrogen fertilizer supply and sugarcane root uptake capacity. Scientific Reports. 2015; 5 :15727. DOI: 10.1038/srep15727 - 58.
Chen CR, Xu ZH. Analysis and behavior of soluble organic nitrogen in forest soils. Journal of Soils and Sediments. 2008; 8 :363-378. DOI: 10.1007/s11368-008-0044-y - 59.
Wu H, Du S, Zhang Y, An J, Zou H, Zhang Y, et al. Effects of irrigation and nitrogen fertilization on greenhouse soil organic nitrogen fractions and soil-soluble nitrogen pools. Agricultural Water Management. 2019; 216 :415-424. DOI: 10.1016/j.agwat.2019.02.020 - 60.
Jones DL, Healey JR, Willett VB, Farrar JF, Hodge A. Dissolved organic nitrogen uptake by plants—An important N uptake pathway? Soil Biology and Biochemistry. 2005; 37 :413-423. DOI: 10.1016/j.soilbio.2004.08.008 - 61.
Yang K, Zhu J, Yan Q , Zhang J. Soil enzyme activities as potential indicators of soluble organic nitrogen pools in forest ecosystems of Northeast China. Annals of Forest Science. 2012; 69 :795-803. DOI: 10.1007/s13595-012-0198-z - 62.
Bhogal A, Murphy DV, Fortune S, Shepherd MA, Hatch DJ, Jarvis SC, et al. Distribution of nitrogen pools in the soil profile of undisturbed and reseeded grasslands. Biology and Fertility of Soils. 2000; 30 :356-362. DOI: 10.1007/s003740050016 - 63.
Zhang Y, Xu W, Duan P, Cong Y, An T, Yu N, et al. Evaluation and simulation of nitrogen mineralization of paddy soils in Mollisols area of Northeast China under waterlogged incubation. PLoS One. 2017; 12 :e0171022. DOI: 10.1371/journal.pone.0171022 - 64.
Murphy DV, Macdonald AJ, Stockdale EA, Goulding KWT, Fortune S, Gaunt JL, et al. Soluble organic nitrogen in agricultural soils. Biology and Fertility of Soils. 2000; 30 :374-387. DOI: 10.1007/s003740050018 - 65.
Zhang H, Zhang Y, Yan C, Liu E, Chen B. Soil nitrogen and its fractions between long-term conventional and no-tillage systems with straw retention in dryland farming in northern China. Geoderma. 2016; 269 :138-144. DOI: 10.1016/j.geoderma.2016.02.001 - 66.
Wang XL, Ye J, Perez PG, Tang DM, Huang DF. (2013). The impact of organic farming on the soluble organic nitrogen pool in horticultural soil under open field and greenhouse conditions: A case study. Soil Science & Plant Nutrition. 2013; 59 :237-248. DOI: 10.1080/00380768.2013.770722 - 67.
Paungfoo-Lonhienne C, Lonhienne TG, Rentsch D, Robinson N, Christie M, Webb RI, et al. Plants can use protein as a nitrogen source without assistance from other organisms. Proceedings of the National Academy of Sciences. 2008; 105 :4524-4529. DOI: 10.1073/pnas.0712078105 - 68.
Paungfoo-Lonhienne C, Visser J, Lonhienne TG, Schmidt S. Past, present and future of organic nutrients. Plant and Soil. 2012; 359 :1-18. DOI: 10.1007/s11104-012-1357-6 - 69.
Conant RT, Ryan MG, Ågren GI, Birge HE, Davidson EA, Eliasson PE, et al. Temperature and soil organic matter decomposition rates–synthesis of current knowledge and a way forward. Global Change Biology. 2011; 17 :3392-3404. DOI: 10.1111/j.1365-2486.2011.02496.x - 70.
Newton WE. 2015. Chapter 2 Recent advances in understanding nitrogenases and how they work. Available from: https://onlinelibrary.wiley.com/doi/pdf/10.1002/9781119053095.ch2 [Accessed: 03 July 2019] - 71.
Chanway CP, Anand R, Yang H. Nitrogen fixation outside and inside plant tissues. In: Advances in Biology and Ecology of Nitrogen Fixation. London: InTech. Epub ahead of print; 2014. DOI: 10.5772/57532 - 72.
Hemida AA, Ohyam T. Nitrogen fixing cyanobacteria: Future prospect. In: Advances in Biology and Ecology of Nitrogen Fixation. London: InTech. Epub ahead of print; 2014. DOI: 10.5772/56995 - 73.
Rosenblueth M, Ormeño-Orrillo E, López-López A, Rogel MA, Reyes-Hernández BJ, Martínez-Romero JC, et al. Nitrogen fixation in cereals. Frontiers in Microbiology. 2018; 9 :1794. DOI: 10.3389/fmicb.2018.01794 - 74.
Verma SK, Kingsley K, Irizarry I, Bergen M, Kharwar RN, White JF. Seed-vectored endophytic bacteria modulate development of rice seedlings. Journal of Applied Microbiology. 2017; 122 :1680-1691. DOI: 10.1111/jam.13463 - 75.
Zheng M, Zhou Z, Luo Y, Zhao P, Mo J. Global pattern and controls of biological nitrogen fixation under nutrient enrichment: A meta-analysis. In: Global Change Biology. 2019. DOI: 10.1111/gcb.14705 - 76.
Gelfand I, Philip Robertson G. A reassessment of the contribution of soybean biological nitrogen fixation to reactive N in the environment. Biogeochemistry. 2015; 123 :175-184. DOI: 10.1007/s10533-014-0061-4 - 77.
Stokstad E. The nitrogen fix. Science. 2016; 353 :1225-1227 - 78.
Mbuthia LW, Acosta-Martínez V, DeBruyn J, et al. Long term tillage, cover crop, and fertilization effects on microbial community structure, activity: Implications for soil quality. Soil Biology and Biochemistry. 2015; 89 :24-34. DOI: 10.1016/j.soilbio.2015.06.016 - 79.
Blesh J. Functional traits in cover crop mixtures: Biological nitrogen fixation and multifunctionality. Journal of Applied Ecology. 2018; 55 :38-48. DOI: 10.1111/1365-2664.13011 - 80.
Li X, Sørensen P, Li F, Li F, Petersen SO, Olesen JE. Quantifying biological nitrogen fixation of different catch crops, and residual effects of roots and tops on nitrogen uptake in barley using in-situ 15N labelling. Plant and Soil. 2015; 395 :273-287. DOI: 10.1007/s11104-015-2548-8 - 81.
Shahzad R, Khan AL, Bilal S, Waqas M, Kang SM, Lee IJ. Inoculation of abscisic acid-producing endophytic bacteria enhances salinity stress tolerance in Oryza sativa. Environmental and Experimental Botany. 2017; 136 :68-77. DOI: 10.1016/j.envexpbot.2017.01.010 - 82.
Defez R, Andreozzi A, Bianco C. The overproduction of indole-3-acetic acid (IAA) in endophytes upregulates nitrogen fixation in both bacterial cultures and inoculated rice plants. Microbial Ecology. 2017; 74 :441-452. DOI: 10.1007/s00248-017-0948-4 - 83.
Gava GJC, Scarpare FV, Cantarella H, Kölln OT, Ruiz-Corrêa ST, Arlanch AB, et al. Nitrogen source contribution in sugarcane-inoculated plants with diazotrophic bacterias under urea-N fertigation management. Sugar Tech. 2019; 21 :462-470. DOI: 10.1007/s12355-018-0614-2 - 84.
Leite J, Passos SR, Simões-Araújo JL, Rumjanek NG, Xavier GR, Zilli JÉ. Genomic identification and characterization of the elite strains Bradyrhizobium yuanmingense BR 3267 and Bradyrhizobium pachyrhizi BR 3262 recommended for cowpea inoculation in Brazil. Brazilian Journal of Microbiology. 2018; 49 :703-713. DOI: 10.1016/j.bjm.2017.01.007 - 85.
Oliveira RS, Carvalho P, Marques G, Ferreira L, Pereira S, Nunes M, et al. Improved grain yield of cowpea ( Vigna unguiculata ) under water deficit after inoculation withBradyrhizobium elkanii andRhizophagus irregularis . Crop & Pasture Science. 2017;68 :1052. DOI: 10.1071/CP17087 - 86.
Santos AA, Silveira JAG, Bonifacio A, Rodrigues AC, Figueiredo MDVB. Antioxidant response of cowpea co-inoculated with plant growth-promoting bacteria under salt stress. Brazilian Journal of Microbiology. 2018; 49 :513-521a. DOI: 10.1016/j.bjm.2017.12.003 - 87.
Santos JBD, Ramos AC, Azevedo Júnior R, Oliveira Filho LCI, Baretta D, Cardoso EJBN. Soil macrofauna in organic and conventional coffee plantations in Brazil. Biota Neotropica. 2018b; 18 :1-13. DOI: 10.1590/1676-0611-BN-2018-0515 - 88.
Souza EM, Bassani VL, Sperotto RA, Granada CE. Inoculation of new rhizobial isolates improve nutrient uptake and growth of bean ( Phaseolus vulgaris ) and arugula (Eruca sativa ). Journal of the Science of Food and Agriculture. 2016;96 :3446-3453. DOI: 10.1002/jsfa.7527 - 89.
Abou-Shanab RAI, Wongphatcharachai M, Sheaffer CC, Sadowsky MJ. Response of dry bean ( Phaseolus vulgaris L.) to inoculation with indigenous and commercial Rhizobium strains under organic farming systems in Minnesota. Symbiosis. 2019;78 :125-134. DOI: 10.1007/s13199-019-00609-3 - 90.
Curá JA, Franz DR, Filosofía JE, Balestrasse K, Burgueño L. Inoculation with Azospirillum sp. and Herbaspirillum sp. bacteria increases the tolerance of maize to drought stress. Microorganisms. 2017; 5 :41. DOI: 10.3390/microorganisms5030041 - 91.
Bertoncelli P, Martin TN, Stecca J, Deak E, Pinto MAB, Schonell A. O manejo de inverno e inoculação de sementes influenciam na produtividade e qualidade da silagem de milho sob sistema plantio direto. Revista Ceres. 2017; 64 :523-531. DOI: 10.1590/0034-737X201764050010 - 92.
Sanz-sáez Á, Heath KD, Burke PV, Ainsworth EA. Inoculation with an enhanced N2-fixing Bradyrhizobium japonicum strain (USDA110) does not alter soybean (Glycine max Merr.) response to elevated [CO2]. Plant, Cell & Environment. 2015;38 :2589-2602. DOI: 10.1111/pce.12577 - 93.
Subramanian P, Kim K, Krishnamoorthy R, Sundaram S, Sa T. Endophytic bacteria improve nodule function and plant nitrogen in soybean on co-inoculation with Bradyrhizobium japonicum MN110. Journal of Plant Growth Regulation. 2015;76 :327-332. DOI: 10.1007/s10725-014-9993-x - 94.
Silveira APD, Sala VMR, Cardoso EJBN, Labanca EG, Cipriano MAP. Nitrogen metabolism and growth of wheat plant under diazotrophic endophytic bacteria inoculation. Applied Soil Ecology. 2016; 107 :313-319. DOI: 10.1016/j.apsoil.2016.07.005 - 95.
Kumar A, Maurya BR, Raghuwanshi R, Meena VS, Islam MT. Co-inoculation with enterobacter and rhizobacteria on yield and nutrient uptake by wheat ( Triticum aestivum L.) in the alluvial soil under indo-gangetic plain of India. Journal of Plant Growth Regulation. 2017;36 :608-617. DOI: 10.1007/s00344-016-9663-5 - 96.
Alcantara RMCM, Xavier GR, Rumjanek NG, Rocha MM, Carvalho JS. Eficiência simbiótica de progenitores de cultivares brasileiras de feijão-caupi. Revista Ciência Agronômica. 2014; 45 :1-9 - 97.
Trani PE, Terra MM, Tecchio MA, Teixeira LAJ, Hanasiro J. Adubação orgânica de hortaliças e frutíferas. IAC: Campinas; 2013. 16p - 98.
Antunes LFS, Scoriza FN, França EM, Silva DG, Correia MEF, Leal MAA, et al. Desempenho agronômico da alface crespa a partir de mudas produzidas com gongocomposto. Revista Brasileira de Agropecuária Sustentável. 2018; 8 :57-65 - 99.
Arjune YP, Ansari AA, Jaikishun S, Homenauth O. Effect of vermicompost and other fertilizers on soil microbial population and growth parameters of f1 Mongal tomato ( Solanum lycopersicum mill.). Pakistan Journal of Botany. 2019;51 :1883-1889. DOI: 10.30848/PJB2019-5(1) - 100.
Rahman MA, Islam MT, Al Mamun MA, Rahman MS, Ashraf MS. Yield and quality performance of carrot under different organic and inorganic nutrient sources with mulching options. Asian Journal of Agricultural and Horticultural Research. 2018; 1 :1-8 - 101.
Mirza A, Jakhar R, Singh J. Response of organic practices, mulching and plant growth regulators on growth, yield and quality of papaya ( Carica papaya L) cv. Taiwan Red Lady. Indian Journal of Agricultural Research. 2019;96-99 (2019):53 - 102.
Escanhoela ASB, Pitombo LM, Brandani CB, Navarrete AA, Bento CB, Carmo JB. Organic management increases soil nitrogen but not carbon content in a tropical citrus orchard with pronounced N2O emissions. Journal of Environmental Management. 2019; 234 :326-335 - 103.
Stojanov D, Milošević T, Mašković P, Milošević N, Glišić I, Paunović G. Influence of organic, organo-mineral and mineral fertilisers on cane traits, productivity and berry quality of red raspberry ( Rubus idaeus L.). Scientia Horticulturae. 2019;252 :370-378. DOI: 10.1016/j.scienta.2019.04.009 - 104.
Menezes JFS, Berti MPS, Vieira Junior VD, Ribeiro RL, Berti CLF. Extração e exportação de nitrogênio, fósforo e potássio pelo milho adubado com dejetos de suínos. Revista de Agricultura Neotropical. 2018; 5 :55-59 - 105.
Magalhães ACM, Blum J, Lopes FB, Tornquist CG. Production components of the cowpea under different doses of organic fertiliser. Journal of Experimental Agriculture International. 2018; 26 :1-9 - 106.
Severino LS, Lima RDLS, Beltrão NDM. Composição química de onze materiais orgânicos utilizados em substratos para produção de mudas. Campina Grande: Embrapa Algodão; 2006. 5p - 107.
Carneiro WJDO, Silva CA, Muniz JÁ, Savian TV. Mineralização de nitrogênio em Latossolos adubados com resíduos orgânicos. Revista Brasileira de Ciência do Solo. 2013; 37 :715-725. DOI:http://dx.doi.org/10.1590/S0100-068320130003 - 108.
Figueiredo CC, Ramos MLG, Mcmanus CM, Menezes AM. Mineralização de esterco de ovinos e sua influência na produção de alface. Horticultura Brasileira. 2012; 30 :175-179. DOI: 10.1590/S0102-05362012000100029 - 109.
Peixoto Filho JU, Freire MBS, Freire FJ, Miranda MF, Pessoa LG, Kamimura KM. Produtividade de alface com doses de esterco de frango, bovino e ovino em cultivos sucessivos. Revista Brasileira de Engenharia Agrícola e Ambiental-Agriambi. 2013; 17 :419-424 - 110.
Sorrenti GB, Fachinello JC, Castilhos DD, Bianchi VJ, Marangoni B. Influência da adubação orgânica no crescimento de tangerineira cv Clemenules e nos atributos químicos e microbiológicos do solo. Revista Brasileira de Fruticultura. 2008; 30 :1129-1135. DOI: 10.1590/S0100-29452008000400047 - 111.
Zamberlam J, Froncheti A. Agroecologia-Caminho de Preservação do Agricultor e do Meio Ambiente. Editora Vozes Ltda: Petrópolis; 2012. 196p - 112.
Chacón EAV, Mendonça ES, Silva RR, Lima PC, Silva IR, Cantarutti RB. Decomposição de fontes orgânicas e mineralização de formas de nitrogênio e fósforo. Ceres. 2011; 58 :373-383. DOI: 10.1590/S0034-737X2011000300019 - 113.
Pires AA, Monnerat PH, Marciano CR, Rocha Pinho LG, Zampirolli PD, Rosa RCC, et al. Efeito da adubação alternativa do maracujazeiro-amarelo nas características químicas e físicas do solo. Revista Brasileira de Ciência do Solo. 2008; 32 :1997-2005 - 114.
Yamaguchi CS, Ramos NP, Carvalho CS, Pires AMM, Andrade CA. Decomposição da palha de cana-de-açúcar e balanço de carbono em função da massa inicialmente aportada sobre o solo e da aplicação de vinhaça. Bragantia. 2017; 76 :135-144 - 115.
Cotta JAO, Carvalho NLC, Brum TDS, Rezende MOO. Compostagem versus vermicompostagem: comparação das técnicas utilizando resíduos vegetais, esterco bovino e serragem. Engenharia Sanitária e Ambiental. 2015; 20 :65-78. DOI: 10.1590/S1413-41522015020000111864 - 116.
Lisboa CC, Lima FRD, Reis RHCL, Silva CA, Marques JJ. Taxa de mineralização do nitrogênio de resíduos orgânicos. Cultura Agronômica. 2018; 27 :341-355 - 117.
Antunes LFS, Scoriza FN, Silva DG, Fernandes MEC. Production and efficiency of organic compost generated by millipede activity. Ciência Rural. 2016; 46 :815-819. DOI: 10.1590/0103-8478cr20150714 - 118.
Lehmann J, Joseph S, editors. Biochar for Environmental Management: Science, Technology and Implementation. London: Routledge; 2015. p. 976 - 119.
Schröder JJ, De Visser W, Assinck FBT, Velthof GL. Effects of short-term nitrogen supply from livestock manures and cover crops on silage maize production and nitrate leaching. Soil Use and Management. 2013; 29 :151-160. DOI: 10.1111 / sum.12027 - 120.
Amlinger F, Götz B, Dreher P, Geszti J, Weissteiner C. Nitrogen in biowaste and yard waste compost: Dynamics of mobilisation and availability–A review. European Journal of Soil Biology. 2003; 39 :107-116. DOI: 10.1016/S1164-5563(03)00026-8 - 121.
Alves RN, Menezes RS, Salcedo IH, Pereira WE. Relação entre qualidade e liberação de N por plantas do semiárido usadas como adubo verde. Revista Brasileira de Engenharia Agrícola e Ambiental. 2011; 15 :1107-1114 - 122.
Zandvakili OR, Barker AV, Hashemi M, Etemadi F, Autio WR, Weis S. Growth and nutrient and nitrate accumulation of lettuce under different regimes of nitrogen fertilization. Journal of Plant Nutrition. 2019; 42 :1575-1593 - 123.
Rodrigues RMP, França KS, Didolanvi OD, Oliveira RL, Sousa MLL, Carvalho RS. Rendimento do pimentão em função de diferentes doses de esterco caprino. Cadernos de Agroecologia. 2018; 13 :1-7 - 124.
Lima DC, Lopes HLS, Sampaio ASO, Souto LS, Pereira ACS, Silva AM, et al. Crescimento inicial da cultura do rabanete ( Raphanus sativus L.) submetida a níveis e fontes de fertilizantes orgânicos. Revista Brasileira de Gestão Ambiental. 2019, 2019;13 :19-24. DOI: 10.18378/rbga.v13i1.6152 - 125.
Severino LS. O que sabemos sobre a torta da mamona. Campina Grande: Embrapa Algodão; 2005. 31p - 126.
Severino LS, Costa FX, Beltrão NEM, Lucena AMA, Guimarães MM. Mineralização da torta de mamona, esterco bovino e bagaço de cana estimada pela respiração microbiana. Revista de Biologia de Ciências da Terra. 2005; 5 :1-6 - 127.
Alves FQG, Soares EPS, Sobral RRS, Melo ADD, Duarte ABM, Rocha MR, et al. Diferentes doses de torta de mamona no desempenho de bulbos de rabanete consorciado com alface. Horticultura. 2012; 30 :5464-5471 - 128.
Costa FX, Severino LS, Beltrão NM, Freire RMM, Lucena AMA, Guimarães MMB. Avaliação de teores químicos na torta de mamona. Revista de Biologia e Ciências da Terra. 2004; 4 :1-7 - 129.
Lima RL, Severino LS, Sampaio LR, Sofiatti V, Gomes JA, Beltrão NE. Blends of castor meal and castor husks for optimized use as organic fertilizer. Industrial Crops and Products. 2011; 33 :364-368 - 130.
Franco GG, Silva SL, Emiliano ED, Silva MVS, Costa FS. Produção agroecológica de compostagem de folhas, frutos e madeira triturada. Cadernos de Agroecologia. 2018; 13 :1-5 - 131.
Dores-Silva PR, Landgraf MD, Rezende MOO. Processo de estabilização de resíduos orgânicos: vermicompostagem versus compostagem. Química Nova. 2013; 36 :640-645 - 132.
Souza MH, Vieira BCR, Oliveira PG, Amaral AA. Macrofauna do solo. Enciclopédia Biosfera. 2015; 11 :115-131 - 133.
Suárez LR, Pinto SPC, Salazar JCS. Soil macrofauna and edaphic properties in coffee production systems in Southern Colombia. Floresta e Ambiente. 2019; 26 :1-8. DOI: 10.1590/2179-8087.033418 - 134.
Garcia FRM, Campos JV. Biologia e controle de artrópodes de importância fitossanitária (Diplopoda, Symphyla, Isopoda), pouco conhecidos no Brasil. Biológico. 2001; 63 :7-13 - 135.
Thakur PC, Shailendra PA, Sinha K. Comparative study of characteristics of biocompost produced by millipedes and earthworms. Advances in Applied Science Research. 2011; 2 :94-98 - 136.
Ramanathan B, Alagesan P. Evaluation of millicompost versus vermicompost. Current Science. 2012; 103 :140-143 - 137.
Cruvinel FF, Antunes LFS, Vasconcellos MAS, Rangel Júnior IM, Martelleto LAP. Produção de mudas orgânicas de pitaia em diferentes substratos. Cadernos de Agroecologia. 2018; 13 :1-5 - 138.
Veiga TRLA, Lima JT, Dessimoni ALA, Pego MFF, Soares JR, Trugilho PF. Different plant biomass characterizations for biochar production. Cerne. 2017; 23 :529-536. DOI: 10.1590/01047760201723042373 - 139.
Cayuela ML, Sánchez-Monedero MA, Roig A, Hanley K, Enders A, Lehmann J. Biochar and denitrification in soils: When, how much and why does biochar reduce N2O emissions? Scientific Reports. 2013; 3-1732 :1-7. DOI: 10.1038/srep01732 - 140.
Clough T, Condron L, Kammann C, Müller C. A review of biochar and soil nitrogen dynamics. Agronomy. 2013; 3 :275-293 - 141.
El-Naggar A, Lee SS, Rinklebe J, Farooq M, Song H, Sarmah AK, et al. Biochar application to low fertility soils: A review of current status, and future prospects. Geoderma. 2019; 337 :536-554. DOI: 10.1016/j.geoderma.2018.09.034 - 142.
Fungo B, Lehmann J, Kalbitz K, Thionģo M, Tenywa M, Okeyo I, et al. Ammonia and nitrous oxide emissions from a field Ultisol amended with tithonia green manure, urea, and biochar. Biology and Fertility of Soils. 2019; 55 :135-148. DOI: 10.1007/s00374-018-01338-3 - 143.
Boeira RC, Ligo MAV, Dynia JF. Mineralização de nitrogênio em solo tropical tratado com lodos de esgoto. Pesquisa Agropecuária Brasileira. 2002; 37 :1639-1647. DOI: 10.1590/ S0100-204X2002001100016 - 144.
Cabrera ML, Kissel DE, Vigil MF. Nitrogen mineralization from organic residues: Research opportunities. Journal of Environmental Quality. 2005; 34 :75-79. DOI: 10.2134/jeq2005.0075