Rice straw incorporation and Azolla application improves agronomic nitrogen-use-efficiency and rice grain yields in paddy fields

In paddy soils, excessive application of N fertilizer often results in substantial N losses due to low N utilization efficiency. However, this condition can be mitigated by enhancing soil organic carbon content. Two-year field experiment was carried out at Mkula Irrigation Scheme in Kilombero Valley, Tanzania with the aim of investigating the impact of Azolla, rice straw incorporation and reduced levels of nitrogen input from NPKS-containing fertilizers on N use efficiency, soil chemical properties and rice grain yield. Assuming that this technology will introduce a novel perspective to the research, shedding light on alternative and potentially more sustainable methods for nitrogen management in paddy soils, it will be particularly relevant in sub-Saharan Africa, where the annual cost of chemical fertilizers is expected to continue rising. The treatments involved absolute control, half dose N (50 kg N ha^-1), full dose N (100 kg N ha^-1), and combination of these N doses with PKS, dry Azolla (3.4 t ha^-1) and rice straw (6.9 t ha^-1) through omission approach. The soil of the experimental area was sandy clay loam in texture, very strongly acid (pH 4.8), normal electrical conductivity (0.06 dS m^-1), low amounts of recorded organic carbon (1.35%), total nitrogen (0.33%), 0.68 mg kg⁻¹ available P, exchangeable potassium (0.15 cmol₍₊₎ kg⁻¹), calcium (0.19 mg kg⁻¹) and sodium percentage (3.75%), with very low cation exchange capacity (1.6 cmol₍₊₎ kg⁻¹). The results showed that combination of Azolla, rice straw +100 kg N ha^{-1 +} 30 kg P ha^{-1 +} 30 kg K ha^{-1 +} 20 kg S ha^-1 resulted in higher rice grain yield, nitrogen uptake and agronomic efficiency of N. Azolla, being an effective biofertilizer, significantly contributes to nitrogen fixation and soil enrichment. Interestingly, this study demonstrates that co-application of Azolla, rice straw, and 50% reduced N is effective for achieving high rice yields, minimizing over-dependence on chemical N fertilizer, sustainable agricultural development, and environmental conservation.

1 Introduction

Nitrogen (N) plays a significant role in crop plants’ photosynthesis, protein synthesis, amino acids, chlorophyll, nucleic acids, ATP, and phytohormone production. Nitrogen use efficiency (NUE) the relationship between the dry matter production or economic yield of a crop and the quantity of N applied) is highly dependent on applied N fertilizer and soil (1). The NUE indices refer to key metrics used to assess the effectiveness with which plants utilize nitrogen in their growth and development (2, 3). These indices help measure the efficiency of nitrogen uptake, assimilation, and utilization by plants, which is crucial for optimizing fertilizer application and reducing environmental impacts such as nitrogen leaching and greenhouse gas emissions (4–6). According to Congreves et al. (7), the common NUE indices include nitrogen uptake efficiency (NUpE), nitrogen utilization efficiency (NUtE), and nitrogen recovery efficiency (NRE). NUpE evaluates the ability of plants to acquire nitrogen from the soil, NUtE assesses the conversion of absorbed nitrogen into biomass, and NRE quantifies the proportion of applied nitrogen that is taken up by plants. These soil-based indices provide valuable insights into nutrient dynamics and plant-soil interactions, contributing to sustainable nitrogen management in agriculture (7). The capacity of crops to absorb nitrogen (N) relies on several interconnected factors, including soil fertility, crop variety, soil moisture, temperature, seasonal timing, N uptake patterns, pest and disease prevalence, farmer knowledge, and socioeconomic conditions on the farm (6). The primary objective of this study is to explore fertilizer-based indices, specifically focusing on guiding efficient nitrogen management practices. According to Kimani et al. (8) nitrogen use efficiency for cereal crop production globally is approximately 30–50%. Similarly Liu et al. (9) reported average apparent recovery efficiency (AREN) and agronomic use efficiency of N were 39.0% and 12.7 kg kg⁻¹, respectively. Therefore, improving NUE can enhance plant performance and increase crop yields (10) especially in rice producing areas. However, the demand for rice (Oryza sativa L.) cultivation is set to soar along with a growing global population, causing nitrogen fertilizer consumption to increase by about 2-fold by 2050 (11).

Excessive application of N fertilizer in paddy soils with characteristically low N utilization efficiency leads to a large amount of N losses (12). Previous studies estimated that 10–40% of chemical N fertilizer applied in paddy is lost either through Ammonia volatilization (9, 13–16), or through conditions associated with potential environmental and ecological disturbances, such as soil acidification (17, 18), eutrophication (19), reduced soil biodiversity (20), nutrient imbalance (21, 22) and enhanced salt accumulation (9). Thus, rice cropping systems require sustainable agronomic and soil management practices to improve N use efficiency and minimize negative environmental impacts on paddy fields (1, 10, 23).

Several options have been practiced to minimize the effects of N-loss and improve nitrogen use efficiency in lowland rice production systems. These include application of urea super-granules, urease inhibitors, and slow-release urea (16, 24–26). However, these technologies result in high economic costs and become unaffordable by smallholder farmers (12, 27).

While approaches such as incorporation of organic materials with wide C/N ratios, such as rice straw can increase microbial activity and lead to increased N immobilization (28–30), their combined application with narrow C/N ratio materials such as Azolla might be a good option to mitigate methane emissions (31), improve soil organic carbon and other nutrients supply as well as minimizing N losses (32–34). Despite the widespread recognition of these materials’ potential benefits in agriculture (35, 36). Yet in Tanzania, this is the first study for Azolla and rice straw to assess N use efficiency. Hence, this study aims to address this gap by investigating the effects of azolla, rice straw, and NPK fertilizers on Tanzanian soils rather than solely focusing on traditional chemical fertilizers. This is because, Azolla application will allow resource-poor farmers to substitute chemical fertilizer N with biologically fixed N- the latter being not immediately subject to ammonia volatilization.

2 Materials and methods

2.1 Description and location of the study area

This experiment was carried out at Mkula Irrigation Scheme (7° 47’ 57.084’’ S, 36° 54’ 47.592’’ E), Kilombero district. The district is located within agroecological zone Eastern Plateaux and Mountain Blocks in Morogoro Region-Tanzania. The climate is classified as tropical savanna climate with bimodal rainfall distribution pattern; having dry spells separating short rainy season from October to December and long rainy season from March to May (37, 38). The mean annual rainfall and temperature range from 1200-1400 mm and 22-23°C, respectively (39, 40). The site receives sufficient water drained from the forest reservoir on the eastern side of Udzungwa Mountain.

2.2 Experimental design and treatments

The field experiments were carried out for two consecutive rice-growing seasons from 2022 to 2023. Randomized complete block design (RCBD) was adopted with 13 treatment levels with half and full recommended levels of N (i.e., 50 kg N ha^-1 and 100 kg N ha^-1) applied with recommended levels of P and or K and S coupled with Azolla or rice straw incorporation in three replications. Details of the treatment combination are shown in Table 1. The dimensions of the individual experimental plot were 3 m × 6 m and the space between replicate blocks was 1.5 m and between plots within a replicate was 0.5 m. The ridges protruded 30 cm above the soil to prevent any fertilizer runoff and lateral contamination.

Table 1

Table 1 Summary of the experimental treatments of chemical fertilizers, Azolla and rice straw application.

2.3 Organic amendment application and agro-techniques

2.3.1 Preparation of Azolla and rice straw

Azolla plant was collected from the Aquaculture Unit of the Sokoine University of Agriculture (6°51’9.5” S, 37°38’59.7” E) in Tanzania. Before establishing culture, Azolla was harvested and analyzed for organic C, total N, P, and C/N ratio. Subsequently, 6 kg of fresh Azolla was multiplicated in the propagation pond (6 m × 5 m) of the same aquaculture unit at the university campus.

During preparation, 7.5 kg of cow dung and 75 g P were applied as triple superphosphate (TSP, Ca₃(PO₄)₂) fertilizer in three split doses at 4-day interval for 22 days (41, 42). Nitrogen content of Azolla, surface water pH, water temperature and electrical conductivity were analyzed by taking representative samples after every 5 days until the Azolla had accumulated maximum nitrogen in biomass (Table 2). Thereafter, Azolla was harvested, drained and transferred to the field for inoculation. Rice straw was collected from farmers’ fields, cutting manually using knife and incorporated into the soil in to respective straw treatments during land preparation using hand hoe. Representative samples of rice straw were dried and transported to the laboratory for chemical analysis of N and P (43).

Table 2

Table 2 Characteristics of Azolla and rice straw used in the experiment.

2.3.2 Application of Azolla, rice straw and inorganic fertilizers

1 kg fresh Azolla was applied during nursery preparation and incorporated in the soil after 15 days. At this stage Azolla had covered the surface of water completely (See Figure 1). 36.4 kg of fresh Azolla biomass was incorporated to the soil using a hand hoe three days before transplanting of rice seedlings to allow Azolla to decompose partially and minimize competition between rice seedling and Azolla. Another 2 kg of fresh Azolla was inoculated six days after transplanting (DAT) and at a rate of 29.2 kg and incorporated into the soil at 40 DAT. By this time rice seedlings have taken roots and start to grow actively. Before incorporation, Azolla was harvested within a 1 m × 1 m wooden frame (44), dried and analyzed for total N through Kjeldahl and P by the wet digestion method (43) (See Table 3). The fertilizers containing NPKS macronutrients were applied. Fertilizers containing P, K, and S were applied uniformly in all experimental plots while N from urea (46% N) was applied at two rates of 100 kg N ha^-1 being the recommended rate and half the recommended rate (50 kg N ha^-1). Urea fertilizer for both rates of N was applied in two splits of 50% basal application at seven DAT and another 50% was top-dressed at 45 DAT, which was close to the booting stage. The triple superphosphate fertilizer (30 kg P ha^-1), muriate of potash (30 kg K ha^-1) and ammonium sulphate (21.0% N and 24.0% S) at 20 kg S ha^-1 were applied through broadcasting as basal fertilizers, except for the absolute control plots. A rice cultivar (c.v SARO-5 TXD 360) was used in this experiment, and it was obtained from the Tanzania Research Institute at Katrini-Ifakara (TARI-CATRINI). Rice seedlings (at 18 days old) were transplanted into well-puddled soils at a spacing of 20 cm × 20 cm in all treatments. Rice straw 11.3 kg 18 m^-2 was spread evenly across the designated straw treatment plots and incorporated into the soil using a hand hoe during the farm preparation stage.

Figure 1

Figure 1 Azolla cover before rice transplanting (A) and at 35 DAT (B).

Table 3

Table 3 Procedure of laboratory analysis of soil samples.

2.4 Soil sampling and analysis

Soil samples were collected for the analysis of the selected physicochemical properties before transplanting of the rice seedlings. The composite soil samples were taken from experimental site from a depth of 0–20 cm using soil auger randomly from 10 spots following a zigzag pattern. Soil samples were also taken from each experimental plot at the end of experiment. 2 kg of soil sample was taken and sent to the laboratory for analysis. The samples were air-dried, grounded, and sieved through a 2 mm wire-mesh and analyzed through standard procedures described in Table 3.

2.5 Sample analysis and calculation of nitrogen use efficiency

Rice was harvested at maturity (116 DAT), with rice ears and straw carefully separated and air-dried for two weeks. Grain yields were adjusted and reported on a basis of 14% moisture content (52). All above-ground plant samples were taken at the booting stage (75 DAT) oven-dried at 70°C to a constant weight then analyzed for total N by the Kjeldahl method. Shoot length was measured at 30 and 60 DAT. Number of tillers and effective tillers was counted at 90 DAT.

The apparent recovery efficiency for N (ARE_N), the percentage of N applied recovered in above-ground biomass was calculated using Equation 1.

$\begin{array}{ll}{\text{ARE}}_{\text{N}}(\%)=\frac{{\text{N}}_{\text{f}}-{\text{N}}_{\text{u}}}{{\text{N}}_{\text{u}}}\times 100& (1)\end{array}$

Where N_f is the N accumulation by above-ground biomass in the fertilized pots (kg), N_u is the N accumulation by above-ground biomass in the unfertilized pots (kg), and Ni is the quantity of N applied (kg) for each treatment, as shown in Table 1.

The soil N-dependent rate (SNDR; the ratio of TNU without fertilization to TNU with fertilization), was calculated using Equation 2.

$\begin{array}{ll}\text{SNDR}(\%)=\frac{{\text{N}}_{\text{u}}}{{\text{N}}_{\text{f}}}\times 100& (2)\end{array}$

The agronomic efficiency of nitrogen (AEN), an expression of unit weight increases in grain yield per N applied) was calculated using Equation 3.

$\begin{array}{ll}\text{AEN}(\text{kg\hspace{0.33em}}k{g}^{-1})=\frac{{\text{G}}_{\text{f}}-{\text{G}}_{\text{u}}}{{\text{N}}_{\text{i}}}& (3)\end{array}$

Where G_f and G_u represent the grain yield (kg) of the fertilized pots and unfertilized pots, respectively, for each replicate.

The physiological nitrogen efficiency (PEN), the unit weight increases in grain yield per unit weight increase in N uptake from N fertilizer), was calculated using Equation 4.

$\begin{array}{ll}\text{PEN}(\text{kg\hspace{0.33em}}k{g}^{-1})=\frac{{\text{Y}}_{\text{f}}-{\text{Y}}_{\text{u}}}{{\text{N}}_{\text{f}}-{\text{N}}_{\text{u}}}& (4)\end{array}$

Where Y_f and Y_u represent the total biomass (kg) of fertilized pots and total biomass of unfertilized pots (kg), respectively, for each treatment.

The internal utilization efficiency (IUEN), the amount of produced grain yield by unit weight plant nutrient accumulation in the total biomass) was calculated using Equation 5.

$\begin{array}{ll}\text{IUEN}(\text{kg\hspace{0.33em}}k{g}^{-1})=\frac{\text{Yf}-\text{Yu}}{\text{Ni}}& (5)\end{array}$

The partial factor productivity (PFPN, unit of grain yield per N applied) was calculated from Equation 6.

$\begin{array}{ll}\text{PFPN}(\text{kg\hspace{0.33em}}k{g}^{-1})=\frac{\text{Gf}}{\text{Ni}}& (6)\end{array}$

All parameters were calculated according to other researchers (10, 52).

2.6 Statistical data analysis

The data was subjected to analysis of variance (ANOVA) to examine the effect of Azolla, rice straw and synthetic fertilizers on rice performance and nitrogen use efficiency parameters. reliability of treatments for the non-significant effects observed in ANOVA was detected by in-depth analysis for normality of residuals confirmed through the Shapiro-Wilk test and the homogeneity of variances was confirmed through Bartlett’s test. The significant treatment means were compared by Turke’s test at 5% level of probability.

3 Results

3.1 The effect of Azolla, rice straw and NPKS fertilizer combinations on rice growth and yield

Results on the effect of treatments on rice plant height, number of tillers and grain yield are presented in Table 4. The fertilized treatments significantly (p< 0.05) influenced plant height compared to the control group (Figure 2). The control plots exhibited the lowest plant height (36.4 cm to 52.8 cm). No significant difference was observed between the control and the treatment involving rice straw + 30 kg P ha^-1. The significantly (p< 0.001) higher plant height (59.0 cm to 80 cm) was recorded in the combination of Azolla with full dose N and other treatments, including rice straw and NPS compared with other treatment combinations. Furthermore, the results revealed significant (p< 0.05) variations in the total number and effective tillers among different treatments (Figure 2). The co-application of NPKS (100 kg N ha^-1) resulted in significantly (p< 0.05) higher number and productive tillers among other treatment combinations. Treatment combination also resulted in the significantly (p< 0.05) higher variation in total biomass and rice grain yield (Figure 3).

Table 4

Table 4 The effect of applying Azolla, rice straw and 50% reduced N on rice growth attributes and yield of rice plants.

Figure 2

Figure 2 Effects of applying rice straw, Azolla and NPKS fertilizer combinations (T1-T13) on plant height, total number of tillers and effective tillers, small bars are standard errors at (P< 0.05). (A) Plant height 30 DAT (cm). (B) Plant height 60 DAT (cm). (C) Number of effective tillers. (D) Total number of tillers.

Figure 3

Figure 3 Effects of applying rice straw, Azolla and NPKS fertilizer combinations (T1-T13) on agronomic N use efficiency components and indices, small bars are standard errors at (P< 0.05).

3.2 Effect of rice straw, Azolla and 50% reduced N on N uptake and agronomic N use efficiency

The parameters related to N uptake and its use efficiency are presented in Table 5. All treatments demonstrated significant (p< 0.05) improvements in nitrogen uptake compared to the control. Comparable results of agronomic use efficiency of N were observed in treatment combinations with 50 and 100 kg N ha^-1. The apparent recovery efficiency of nitrogen ranged from 29.8% to 163.3% for the two seasons, with the second season lagging a bit behind in the amount of N recovered. The inclusion of Azolla in other treatment combinations with 50% N resulted in significant (p< 0.05) higher apparent recovery efficiency of nitrogen compared to other treatment combinations.

Table 5

Table 5 Effect of Azolla, rice straw and 50% reduced N along with PKS fertilizers combinations on Agronomic Nitrogen Use Efficiency.

Whereas comparable results of the calculated internal utilization efficiency of nitrogen were observed for both full dose and 50% reduced N co-application with other treatments (~76 kg kg^-1), the 50% N reduced-tailored combination significantly (p< 0.05) outperformed others with 102.22 kg kg^-1 recorded. Physiological nitrogen efficiency ranged 10.66 kg kg^-1 to 68.82 kg kg^-1 and 53.72 kg kg^-1 to 123.28 kg kg^-1 for first and second season respectively. Highest value 68.82 kg kg^-1 was recorded under application of reduced N along with NPKS in the first season and sole rice straw (23.28 kg kg^-1) in the second season. The highest value of partial factor productivity of nitrogen was recorded under sole application of Azolla with 50% N reduced-based combination 55.93 kg kg^-1 to 76.30 kg kg^-1 for first and second season respectively, that significantly (p< 0.001) outperforming other treatments. The agronomic efficiency of applied nitrogen exhibited significant (p< 0.001) variation among treatments, with the highest values being 39.26 kg grain per kilogram of applied nitrogen in the first season and 60.37 kg grain per kilogram in the second season. These remarkable results were observed under 50% N reduced-based combinations. Soil nitrogen dependent rate ranged from 7.56% to 100% during the first season and 6.31% to 100% during the second season, with the highest dependence recorded in absolute control and the lowest dependence recorded in full N dose-based combination with other treatments.

3.3 Estimation N fixation and total nitrogen enrichment by Azolla in both seasons

Characteristics of Azolla used in the experiments are shown in Table 2. In first season, fresh Azolla incorporated was 1,956 kg and 1,503.4 kg ha^-1, with nitrogen contents of 2.17% and 1.92% for the first and second incorporations, respectively. The estimated nitrogen fixed was 42.44 kg and 29.01 kg per hectare based on nitrogen fixation efficiency resulted in 71.4 kg N fixation ha^-1 in the first season. In the second season, Azolla biomass stood at 1,784 and 1,640 kg fresh Azolla ha^-1, with nitrogen contents of 1.8% and 2.2% respectively. The estimated nitrogen fixed was 32.6 kg and 36.08 kg N ha^-1 for the first and second incorporations, resulting in a total estimated nitrogen of 68.68 kg ha^-1.

3.4 Effects of Azolla rice straw and NPKS fertilizer combinations on soil chemical properties

Results of the experiment indicated that all tested soil chemical parameters were significantly affected by different treatment combinations (Table 6). Results of the first and second experiments showed that soil pH ranged from 4.87 to 5.3 and 4.2 to 4.7 at the end of first and second season respectively. While there was no significant difference in pH among treatments (p = 0.84), pH varied significantly between seasons (p< 0.05). The mean total N increased compared to pretreatment levels. In the first season, total N ranged from medium (0.18%) to high (0.46%). In the second season, it ranged from medium (0.13%) to very high (0.65%). There was a significant (p< 0.05) increase in total N between the two seasons. Organic amendments (Azolla and rice straw) impacted soil TN reserve more than sole synthetic fertilizers. SOC concentration increased significantly (p< 0.05) between seasons. At the end of the first season, the highest SOC concentration (2.9%) was under sole rice straw incorporation, statistically higher than other treatments. In the second experiment, the highest SOC value (5.79%) recorded under the Azolla treatment with 50% reduced N, along with 30 kg P ha⁻¹, 30 kg K ha⁻¹, and 20 kg S ha⁻¹. This was comparable to other organic amended treatments and superior to sole synthetic treatments. Soil C:N ratio at a depth of 0-20 cm varied between treatments, in the first season it ranges from 4.37 to 11.33 and 4.6 to 29.3 for the second season. The highest C:N ratio was observed under sole rice straw treatments in both seasons.

Table 6

Table 6 The effect of applying Azolla, rice straw and NPKS fertilizers combinations on Soil chemical properties.

4 Discussion

4.1 The effect of Azolla, rice straw and 50% reduce N on rice growth and yield attributes

Plant height serves as an indicator of overall vegetative growth in rice crops (53, 54). Results of the study indicated that application of Azolla along with rice straw incorporation with 50% reduced N statistically yields comparable results in terms of plant height compared to the full recommended dose of NPKS (Figure 4). This increase in height could be attributed to several factors, including improved soil structure, enhanced nutrient cycling, and increased microbial activity due to the balanced application of synthetic fertilizers and organic matter (8, 52, 55). Also, could be attributed to the high nitrogen supply capacity of Azolla to rice crops (36, 56). These favorable conditions promote the rice crop’s vegetative growth, leading to a larger leaf area, higher photo assimilates, greater dry matter accumulation, and increased cell division (57, 58). According to research by Feyisa et al. (59), Azolla can fix nitrogen in the range of 53-1000 kg ha-1. When Azolla is grown either as a monocrop or intercropped with rice, it can contribute 40-170 kg N ha⁻¹, which is gradually released 40-60% after 20 days and 55-90% after 40 days once incorporated into paddy soils. The reduced plant height observed in the control, as well as in treatments involving rice straw + 30 kg P ha^-1 and rice straw combined with 50% reduced N (along with 30 kg P ha⁻¹, 30 kg K ha⁻¹, and 20 kg S ha⁻¹), may be attributed to the limited supply capacity of these treatments. Additionally, the high carbon-to-nitrogen (C-to-N) ratio of rice straw could have contributed to soil nitrogen assimilation by microorganisms (58, 60). The reduced plant height observed in the sole application of nitrogen (N) may be attributed to the absence of other essential nutrients like phosphorus (P) fertilizer. Phosphorus plays a crucial role in enhancing root anatomy and promoting higher panicle formation (14, 53). The authors emphasized a significant finding related to the correlation between nitrogen application rates and rice plant height. As nitrogen doses increase, rice plant heights also tend to rise, thereby extending the overall crop cycle. To achieve an optimal balance between crop growth and maturity timing, it is essential to implement a precise and well-calibrated nitrogen application strategy (61–63). The number of tillers and productive tillers per hill significantly impacts rice yield (64). These tillers provide the necessary stalks for optimal production (65). In control plots and sole rice straw application, the low number of tillers and productive tillers could be attributed to the limited soil supply capacity when no additional inputs are provided. Research by (66) highlights that the actual tillering ability of rice is closely tied to N input and spacing. Our study corroborates this finding, showing that N supply significantly affects the number of tillers and effective tillers. Interestingly, balanced fertilizer application plays a crucial role in tiller formation. When fertilizers are judiciously applied between early and late emerging tillers, it leads to improved crop yield and a greater number of productive tillers (67). The application of Azolla + 30 kg P ha^-1 yielded comparable tillers and effective tillers to the full recommended level of NPKS and when Azolla and rice straw coupled with full or 50% reduced N + 30 kg P ha⁻¹, 30 kg K ha⁻¹, and 20 kg S ha⁻¹ outperformed sole synthetic fertilizers applications. This can be attributed to Azolla’s high supply capacity of nitrogen to rice crops (68). When Azolla and rice straw are combined, they complement each other due to their distinct carbon-to-nitrogen (C-to-N) ratios. Azolla, with its lower C-to-N ratio, provides readily available nitrogen (approximately 3–5% N) when it decomposes. Meanwhile, rice straw, with a higher C-to-N ratio, contributes organic matter and improves soil structure (69). By using Azolla alone or in combination with reduced synthetic fertilizers, plant growth parameters can be enhanced, leading to minimized nutrient loss and improved nutrient use efficiency (70–72). The consistently high total biomass and grain yield of co-treatment of Azolla, rice straw + 100 kg N ha-1 + 30 kg P ha⁻¹, 30 kg K ha⁻¹, and 20 kg S ha⁻¹, and Azolla, rice straw with 50% reduced N + 30 kg P ha⁻¹, 30 kg K ha⁻¹, and 20 kg S ha⁻¹ or Azolla + 50% reduced N + 30 kg P ha⁻¹, 30 kg K ha⁻¹, and 20 kg S ha⁻¹ treatments could be attributed to the specific combination of factors and inputs used in these treatments that favor healthy soils with good structure, high organic matter content, and a balanced pH level provide a conducive environment for root development and nutrient uptake. The observed higher total biomass and grain yield in various treatments involving Azolla, rice straw, and specific nutrient combinations can be attributed to a combination of factors. These treatments promote healthy soil conditions, including good structure, high organic matter content, and a balanced pH level, which in turn create favorable conditions for root development and efficient nutrient uptake. Specifically, the following treatments demonstrated positive effects: 1) Co-treatment of Azolla, rice straw, and specific nutrients (100 kg N ha⁻¹, 30 kg P ha⁻¹, 30 kg K ha⁻¹, and 20 kg S ha⁻¹); 2) Azolla combined with 50% reduced N, along with 30 kg P ha⁻¹, 30 kg K ha⁻¹, and 20 kg S ha⁻¹; and 3) Azolla alone with 50% reduced N, along with 30 kg P ha⁻¹, 30 kg K ha⁻¹, and 20 kg S ha⁻¹. These treatments synergistically enhance soil health and contribute to improved crop productivity. The study draws insights from previous research (35, 52, 73, 74). According to (75), the co-application of reduced chemical fertilizers and organic fertilizers effectively improves soil fertility, microbial community structure, and crop yield and limits the use of chemical fertilizers. The reduced biomass and grain yield observed in treatments involving rice straw combined with 30 kg P ha⁻¹ and rice straw with 50% reduced N + 30 kg P ha⁻¹, 30 kg K ha⁻¹, and 20 kg S ha⁻¹ may be attributed to the relatively high carbon-to-nitrogen ratio of the straw. This high ratio slows down decomposition upon incorporation into the soil. Additionally, a significant portion of the available nitrogen is consumed by microorganisms, resulting in nitrogen becoming temporarily tied up, making it less accessible to rice crops (58, 76–80).

Figure 4

Figure 4 Effects of co-application of Azolla, rice straw and NPKS fertilizer combination on some selected soil properties, small bars are standard errors at (P< 0.05).

4.2 Effect of fertilizer treatments on N uptake and agronomic N use efficiency

The key components of nitrogen use efficiency include agronomic efficiency of applied nitrogen (AE_N), apparent recovery efficiency of nitrogen, and physiological nitrogen efficiency. Additionally, partial factor productivity of nitrogen serves as a crucial index for understanding long-term productivity trends and optimizing nitrogen fertilizer use efficiency (10, 52). The apparent recovery efficiency of N is a crucial metric that quantifies how effectively plants recover and utilize nitrogen from applied fertilizers (7). It provides insights into the efficiency of N uptake by crops, which is essential for optimizing agricultural practices and sustainable nutrient management. Generally higher ARE_N values indicate more efficient nitrogen utilization by the crop. Results of the experiments indicated that the co-application of Azolla, rice straw with full and 50% reduced N + 30 kg P ha⁻¹, 30 kg K ha⁻¹, and 20 kg S ha⁻¹ resulted in higher percentage of N recovery efficiency. The observed phenomenon could be attributed to several factors. Firstly, the enhanced soil structure, increased microbial activity, and improved nutrient availability collectively contribute to better nutrient uptake by plants (9, 23, 58, 81). Additionally, the presence of Azolla cover plays a role in reducing ammonia volatilization, while simultaneously minimizing nitrogen losses through surface runoff and leaching (13, 24, 82). These combined effects create a favorable environment for efficient nutrient utilization by crops. The higher apparent recovery efficiency of nitrogen observed in balanced fertilizer applications (73.52% in the first season and 113.89% in the second season) compared to sole nitrogen treatments (30.52% in the first season and 29% in the second season) can be attributed to the fact that balanced fertilizers provide a combination of essential nutrients (such as nitrogen, phosphorus, and potassium) in optimal proportions. This balanced nutrient supply promotes better nutrient uptake by plants, ultimately leading to improved recovery efficiency (52, 53, 83). Agronomic efficiency of nitrogen (AEN) can be defined as the yield increase per unit of nitrogen (N) applied, providing a more direct measure of the production impact of applied N fertilizers, nitrogen loss, and economic return (84). Higher agronomic efficiency of applied N was observed in co-application of Azolla and 50% reducing N + 30 kg P ha⁻¹, 30 kg K ha⁻¹, and 20 kg S ha⁻¹ with values of 39.26 kgkg^-1 and 60.37 kgkg^-1 for the first and second seasons, respectively. This outcome is likely attributed to the accumulation of soil nutrient reserves and the rapid decomposition of Azolla green manure influenced by lower C: N ratios, which supply ample nutrients, particularly N (60, 85, 86). Additionally, this practice helps minimize ammonia volatilization (12, 13). For example, (87) reported that co-application of organic and chemical fertilizers is a better approach for enhancing soil fertility and crop yields compared to using either organic or chemical fertilizers alone. In the present study, the use of sole synthetic fertilizers aligns with the benchmark data of agronomic efficiency of N in lowland rice production systems, which typically falls within the range of 15–30 kg of nitrogen per kilogram of grain produced (52, 88). The reduced efficiency of sole synthetic fertilizers can be attributed to factors such as high ammonium volatilization, surface runoff, and leaching (12, 89, 90). The positive impact on nitrogen uses efficiency (NUE) resulting from the application of Azolla and rice straw, both in full and with 50% reduced nitrogen, aligns consistently with various NUE components, including internal utilization efficiency of nitrogen (IUNE), partial factor productivity of nitrogen (PFPN), and apparent recovery efficiency of nitrogen (PEN). This favorable influence of Azolla + rice straw and synthetic fertilizers on NUE is in line with findings reported by several authors (35, 73, 91, 92). The underlying premise is that this combination enhances N retention, reduces N losses, and ultimately improves crop N uptake. According to (93), Azolla biofertilizer holds significant promise as an approach to enhance nitrogen use efficiency (NUE) in paddy rice fields. Its remarkable potential for biological nitrogen fixation (BNF) makes it a valuable tool for sustainable agriculture. Soil nitrogen dependent rate (SNDR) signifies how much crop performance and nitrogen utilization rely on the availability of nitrogen in the soil. Results of the study indicated that the control plot and rice straw + 30 kg P ha^-1 have higher percentage of SNDR indicating that these treatments are entirely dependent on reserved soil nitrogen for rice crop growth. The higher SNDR in rice straw treatment might be due to a higher C/N ratio that slows decomposition and release (94). On the other hand, lower SNDR in co-application Azolla, rice straw + 30 kg P ha⁻¹, 30 kg K ha⁻¹, and 20 kg S ha⁻¹ suggested that these amendments consistently enhance N supply and contribute to rice crop performance. Here we demonstrate that SNDR is lowered under rice straw and 50% reduced N + 30 kg P ha⁻¹, 30 kg K ha⁻¹, and 20 kg S ha⁻¹ that might be due to enhances soil hydrolysable N of straw. According to (95), proper rice straw management, especially incorporating it in winter with joint N application, improves soil fertility and mitigates greenhouse gas emissions in double rice cropping systems.

4.3 Contribution of Azolla in nitrogen enrichment

The results show that Azolla is an effective biofertilizer for rice production, as it can fix significant amounts of nitrogen and enrich the soil. The results are consistent with previous studies that have demonstrated the benefits of Azolla for rice cultivation (12, 74, 96). In a study conducted by (56), it was found that Azolla, the fast-growing water fern, exhibits a remarkable ability to fix nitrogen and significantly contributes to rice growth and yield. Another study (74) highlighted that Azolla plays a crucial role in reducing reliance on synthetic nitrogen fertilizers, minimizing nitrogen loss, and optimizing nitrogen use efficiency. This approach not only promotes environmental conservation but also contributes to the long-term viability of agricultural practices.

4.4 Effects of treatment combinations on soil chemical properties

The present study demonstrated that application of Azolla and rice straw impact change in most chemical fertility (Figure 5). The stability of pH within certain ranges suggests that the treatments were effective in maintaining a suitable soil environment for rice cultivation. However, the observed seasonal disparity in pH emphasizes the dynamic nature of soil processes, influenced by both applied treatments and external factors associated with seasonal changes. Soil chemical fertility depends on several factors such as climate, topography, nature of the soil, and type of amendments (97, 98). Similar results were reported by (99) that application of chemical fertilizers alone or partially substituted with organic fertilizers increased the soil pH by 0.71 to 0.96 units over the control. This might be due to severe microbial nitrification process that led to soil acidification, which is largely attributed to ammonium fertilizers applied in the soil (98). Soil total nitrogen is the major determinant and indicator of soil fertility and quality in an agricultural ecosystem and is closely related to soil productivity (100). The significant increase in total nitrogen (TN) levels observed in the soil, particularly in the Azolla fertilized treatments might be attributed to Azolla N fixing capacity. Azolla is known for its ability to fix atmospheric nitrogen with the help of nitrogen-fixing cyanobacteria present in its symbiotic relationship (101). This process results in an increase in available nitrogen in the soil (102). The combination of Azolla and rice straw incorporation might have synergistic effects on nitrogen availability. Azolla provides nitrogen through biological nitrogen fixation, while rice straw help in accumulation of TN stocks. Together, they create a more comprehensive impact on soil TN levels. Rice straw incorporation significantly (p< 0.05) affected the soil organic carbon. This might be due to the wider C/N (59.1) ratio of straw that takes longer to decompose and thus improve soil aggregation, soil water retention and reduce bulk density of the soil, promoting crop growth and TN stocks (100, 103). The observed increase in SOC concentrations is statistically significant (P< 0.05), emphasizing the reliability of the results. This suggests that the changes in SOC are not due to random variability but are attributed to the applied treatments. This observed outcome highlights the importance of nutrient management strategies that integrate organic inputs such as Azolla and rice straw and the synergy between organic amendments and adjusted synthetic fertilizers contributes to the improvement of SOC, indicating a more sustainable and holistic approach to soil health. Soil organic carbon along with their stoichiometric characteristics, are important indicators for the quality and quantity of soil organic matter (104). The carbon-to-nitrogen (C:N) ratio in the soil is a crucial indicator of nutrient availability and microbial activity (105). A higher C:N ratio generally indicates slower decomposition of organic matter relative to nitrogen release. The consistently highest C:N ratio recorded under sole rice straw treatments in both seasons suggests that the decomposition of rice straw, which is rich in carbon, outpaced nitrogen release. This leads to a higher C:N ratio, indicating a relative abundance of carbon compared to nitrogen. This is in accordance with some results of (106). However, results demonstrated that the incorporation of synthetic fertilizers, Azolla, and rice straw each contributes differently to the carbon and nitrogen content of the soil, influencing the overall C:N ratio. The significant differences of C:N ratio between seasons, suggest that treatment continuous application of treatment combinations could enhance organic matter reserve and decomposition that subsequently impact change in nutrient release. This might be a holistic approach to nutrient management and sustainable agricultural practices. Results of the experiments indicated that application of Azolla and rice straw enhances P content in soil. The rise in soil P content can be attributed to Azolla’s high P absorption capacity, directly promoting Azolla biomass growth. The elevated Phosphorus Use Efficiency (PUE) in these treatment combinations provides clear evidence that upon the decomposition of Azolla plants, the organic nitrogen and phosphorus undergo rapid mineralization, releasing them as biofertilizers available for the thriving rice plants. The study by Chatterjee et al. (107) demonstrated that long-term organic fertilization, including the application of Azolla, consistently yielded the highest P content in soil, surpassing the levels observed in treatments solely reliant on synthetic fertilizers. These findings emphasize the effectiveness of organic matter (Azolla and rice straw) in enhancing soil phosphorus levels, suggesting its potential as a sustainable alternative to synthetic fertilizers.

Figure 5

Figure 5 Effects of co-application of Azolla, rice straw and NPKS fertilizer combination on some selected soil properties, small bars are standard errors at (P< 0.05).

5 Conclusion and recommendation

Our study demonstrated that the co-application of Azolla, rice straw and synthetic fertilizers resulted in the best performance of rice plants in terms of plant height, tiller count, effective tiller formation and yield components. This indicates that the balanced application of synthetic and organic fertilizers can improve soil quality, nutrient availability and microbial activity, which in turn enhance rice growth and productivity. The study demonstrated that Application of Azolla 50% N + 30 kg P ha⁻¹ or combined with rice straw show comparable rice grain yield to full recommended dose of NPKS, suggesting that Azolla is an effective biofertilizer that can fix significant amounts of nitrogen and enrich the soil and when applied with rice straw and reduced N provide favorable soil environment for rice growth and production. Therefore, the application of Azolla, rice straw with reduced N can improve soil quality and significantly enhance N use efficiency and sustainable rice production, especially for the local farmers.

Data availability statement

The original contributions presented in the study are included in the article/supplementary material. Further inquiries can be directed to the corresponding author.

Author contributions

SM: Conceptualization, Methodology, Writing – original draft. HT: Conceptualization, Supervision, Writing – original draft. NA: Supervision, Writing – original draft. JS: Supervision, Writing – original draft.

Funding

The author(s) declare that no financial support was received for the research, authorship, and/or publication of this article.

Conflict of interest

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

Publisher’s note

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

References

1. Cassman KG, Dobermann AR, Walters DT. Agroecosystems, Nitrogen-use Efficiency, and Nitrogen Agroecosystems, Nitrogen-use Efficiency, and Nitrogen Management Management (2002). Available at: http://www.ambio.kva.se.

Google Scholar

2. Erisman JW, Leach A, Bleeker A, Atwell B, Cattaneo L, Galloway J. An integrated approach to a nitrogen use efficiency (NUE) indicator for the food production-consumption chain. Sustain. (2018) 10:1–29. doi: 10.3390/su10040925

CrossRef Full Text | Google Scholar

3. Govindasamy P, Muthusamy SK, Bagavathiannan M, Mowrer J, Jagannadham PTK, Maity A, et al. Nitrogen use efficiency—a key to enhance crop productivity under a changing climate. Front Plant Sci. (2023) 14:1121073. doi: 10.3389/fpls.2023.1121073

PubMed Abstract | CrossRef Full Text | Google Scholar

4. Weih M, Hamnér K, Pourazari F. Analyzing plant nutrient uptake and utilization efficiencies: comparison between crops and approaches. Plant Soil. (2018) 430:7–21. doi: 10.1007/s11104-018-3738-y

CrossRef Full Text | Google Scholar

5. Elrys AS, Elnahal AS, Abdo AI, Desoky ESM, Selem E, Rady MM. Traditional, modern, and molecular strategies for improving the efficiency of nitrogen use in crops for sustainable agriculture: a fresh look at an old issue. J Soil Sci Plant Nutr. (2022) 22:3130–56. doi: 10.1007/s42729-022-00873-1

CrossRef Full Text | Google Scholar

6. Valenzuela H. Optimizing the Nitrogen Use Efficiency in Vegetable Crops. Nitrogen. (2024) 5(1):106–43. doi: 10.3390/nitrogen5010008

CrossRef Full Text | Google Scholar

7. Congreves KA, Otchere O, Ferland D, Farzadfar S, Williams S, Arcand MM. Nitrogen use efficiency definitions of today and tomorrow. Front. Plant Sci. (2021) 12:637108. doi: 10.3389/fpls.2021.637108

PubMed Abstract | CrossRef Full Text | Google Scholar

8. Kimani SM, Bimantara PO, Hattori S, Tawaraya K, Sudo S, Xu X, et al. Co-application of poultry-litter biochar with Azolla has synergistic effects on CH4 and N2O emissions from rice paddy soils. Heliyon. (2020) 6:e05042. doi: 10.1016/j.heliyon.2020.e05042

PubMed Abstract | CrossRef Full Text | Google Scholar

9. Liu H, Yang G, Ji H, Feng Y, Zhang Y, Chen L, et al. Nitrogen fertilizer reduction in combination with Azolla cover for reducing ammonia volatilization and improving nitrogen use efficiency of rice. PeerJ. (2021) 9. doi: 10.7717/peerj.11077

CrossRef Full Text | Google Scholar

10. Fageria NK, de Morais OP, dos Santos AB. Nitrogen use efficiency in upland rice genotypes. J Plant Nutr. (2010) 33:1696–711. doi: 10.1080/01904167.2010.496892

CrossRef Full Text | Google Scholar

11. Conley DJ, Paerl HW, Howarth RW, Boesch DF, Seitzinger SP, Havens KE, et al. Ecology - Controlling eutrophication: Nitrogen and phosphorus. Science. (2009) 80-.). 323:1014–5. doi: 10.1126/science.1167755

CrossRef Full Text | Google Scholar

12. Fosu-Mensah BY, Vlek PLG, Manske G, Mensah M. The influenec of Azolla pinnata on floodwater chemistry, grain yield and nitrogen uptake of rice in Dano, Southwestern Burkina Faso. J Agric Sci. (2015) 7. doi: 10.5539/jas.v7n8p118

CrossRef Full Text | Google Scholar

13. De Macale MAR, Vlek PLG. The role of Azolla cover in improving the nitrogen use efficiency of lowland rice. Plant Soil. (2004) 263:311–21. doi: 10.1023/B:PLSO.0000047742.67467.50

CrossRef Full Text | Google Scholar

14. Fageria NK, Carvalho GD, Santos AB, Ferreira EPB, Knupp AM. Chemistry of lowland rice soils and nutrient availability. Commun Soil Sci Plant Anal. (2011) 42:1913–33. doi: 10.1080/00103624.2011.591467

CrossRef Full Text | Google Scholar

15. Yao Y, Zhang M, Tian Y, Zhao M, Zhang B, Zeng K, et al. Urea deep placement in combination with Azolla for reducing nitrogen loss and improving fertilizer nitrogen recovery in rice field. F Crop Res. (2018) 218:141–9. doi: 10.1016/j.fcr.2018.01.015

CrossRef Full Text | Google Scholar

16. Yang G, Ji H, Sheng J, Zhang Y, Feng Y, Guo Z, et al. Combining Azolla and urease inhibitor to reduce ammonia volatilization and increase nitrogen use efficiency and grain yield of rice. Sci Total Environ. (2020) 743:140799. doi: 10.1016/j.scitotenv.2020.140799

PubMed Abstract | CrossRef Full Text | Google Scholar

17. Woli P, Hoogenboom G, Alva A. Simulation of potato yield, nitrate leaching, and profit margins as influenced by irrigation and nitrogen management in different soils and production regions. Agric Water Manage. (2016) 171:120–30. doi: 10.1016/j.agwat.2016.04.003

CrossRef Full Text | Google Scholar

18. Zhang Y, Ye C, Su Y, Peng W, Lu R, Liu Y, et al. Soil Acidification caused by excessive application of nitrogen fertilizer aggravates soil-borne diseases: Evidence from literature review and field trials. Agric Ecosyst Environ. (2022) 340:108176. doi: 10.1016/j.agee.2022.108176

CrossRef Full Text | Google Scholar

19. Wang JL, Liu K, Lou, Zhao XQ, Zhang HQ, Li D, et al. Balanced fertilization over four decades has sustained soil microbial communities and improved soil fertility and rice productivity in red paddy soil. Sci Total Environ. (2021) 793:148664. doi: 10.1016/j.scitotenv.2021.148664

PubMed Abstract | CrossRef Full Text | Google Scholar

20. Storkey J, Macdonald AJ, Poulton PR, Scott T, Köhler IH, Schnyder H, et al. Grassland biodiversity bounces back from long-term nitrogen addition. Nature. (2015) 528:401–4. doi: 10.1038/nature16444

PubMed Abstract | CrossRef Full Text | Google Scholar

21. Tilman D, Fargione J, Wolff B, D’Antonio C, Dobson A, Howarth R, et al. Forecasting agriculturally driven global environmental change. Science. (2001) 80-.). 292:281–4. doi: 10.1126/science.1057544

CrossRef Full Text | Google Scholar

22. Razavipour T, Moghaddam SS, Doaei S, Noorhosseini SA, Damalas CA. Azolla (Azolla filiculoides) compost improves grain yield of rice (Oryza sativa L.) under different irrigation regimes. Agric Water Manage. (2018) 209:1–10. doi: 10.1016/j.agwat.2018.05.020

CrossRef Full Text | Google Scholar

23. Sandhu PS, Walia SS, Gill RS, Dheri GS. Thirty-one years study of integrated nutrient management on physico-chemical properties of soil under rice–wheat cropping system. Commun Soil Sci Plant Anal. (2020) 00:1641–57. doi: 10.1080/00103624.2020.1791156

CrossRef Full Text | Google Scholar

24. Cabangon RJ, Tuong TP, Castillo EG, Bao, Fosu-Mensah BY, Vlek, Lumpkin A, Plueknett and DL, et al. Ammonia volatilization losses from paddy fields under controlled irrigation with different drainage treatments. Soil Sci Plant Nutr. (2015) 2:329–42. doi: 10.1155/2014/417605

CrossRef Full Text | Google Scholar

25. Meng X, Li Y, Yao H, Wang J, Dai F, Wu Y, et al. Nitrification and urease inhibitors improve rice nitrogen uptake and prevent denitrification in alkaline paddy soil. Appl Soil Ecol. (2020) 154:103665. doi: 10.1016/j.apsoil.2020.103665

CrossRef Full Text | Google Scholar

26. Haseeb-ur-Rehman AMG, Ikram RM, Hashim S, Hussain S, Irfan M, Mubeen K, et al. Sulphur coated urea improves morphological and yield characteristics of transplanted rice (Oryza sativa L.) through enhanced nitrogen uptake. J King Saud Univ Sci. (2022) 34:101664. doi: 10.1016/j.jksus.2021.101664

CrossRef Full Text | Google Scholar

27. Damodar Reddy D, Sharma KL. Effect of amending urea fertilizer with chemical additives on ammonia volatilization loss and nitrogen-use efficiency. Biol Fertil Soils. (2000) 32:24–7. doi: 10.1007/s003740000208

CrossRef Full Text | Google Scholar

28. Moritsuka N, Yanai J, Mori K, Kosaki T. Biotic and abiotic processes of nitrogen immobilization in the soil-residue interface. Soil Biol Biochem. (2004) 36:1141–8. doi: 10.1016/j.soilbio.2004.02.024

CrossRef Full Text | Google Scholar

29. Zhu J, Peng H, Ji X, Li C, Li S. Effects of reduced inorganic fertilization and rice straw recovery on soil enzyme activities and bacterial community in double-rice paddy soils. Eur J Soil Biol. (2019) 94:103116. doi: 10.1016/j.ejsobi.2019.103116

CrossRef Full Text | Google Scholar

30. Zhang S, Zhang G, Wang D, Liu Q. Long-term straw return with N addition alters reactive nitrogen runoff loss and the bacterial community during rice growth stages. J Environ Manage. (2021) 292:112772. doi: 10.1016/j.jenvman.2021.112772

PubMed Abstract | CrossRef Full Text | Google Scholar

31. Korsa G, Alemu D, Ayele A. Azolla Plant Production and Their Potential Applications. (2024). doi: 10.1155/2024/1716440

CrossRef Full Text | Google Scholar

32. Saothongnoi V, Amkha S, Inubushi K, Smakgahn K. Effect of rice straw incorporation on soil properties and rice yield. Thai J Agricultural Sci. (2014) 47(1):7–12.

Google Scholar

33. Yadav S, Kumar R, Chandra MS, Abhineet, Singh S, Yadav RB, et al. Soil organic carbon sequestration and carbon pools in rice based cropping systems in indo-gangetic plains: an overview. Int Res J Pure Appl Chem. (2020), 122–36. doi: 10.9734/irjpac/2020/v21i2430341

CrossRef Full Text | Google Scholar

34. Bhardwaj AK, Malik K, Chejara S, Rajwar D, Narjary B, Chandra P. Integration of organics in nutrient management for rice-wheat system improves nitrogen use efficiency via favorable soil biological and electrochemical responses. Front Plant Sci. (2023) 13:1075011. doi: 10.3389/fpls.2022.1075011

PubMed Abstract | CrossRef Full Text | Google Scholar

35. Ali MA, Sattar MA, Islam MN, Inubushi K. Integrated effects of organic, inorganic and biological amendments on methane emission, soil quality and rice productivity in irrigated paddy ecosystem of Bangladesh: Field study of two consecutive rice growing seasons. Plant Soil. (2014) 378:239–52. doi: 10.1007/s11104-014-2023-y

CrossRef Full Text | Google Scholar

36. Setiawati MR, Prayoga MK, Stöber S, Adinata K, Simarmata T. Performance of rice paddy varieties under various organic soil fertility strategies. Open Agric. (2020) 5:509–15. doi: 10.1515/opag-2020-0050

CrossRef Full Text | Google Scholar

37. Kwesiga J, Grotelüschen K, Senthilkumar K, Neuhoff D, Döring TF, Becker M. Rice yield gaps in smallholder systems of the kilombero floodplain in Tanzania. Agronomy. (2020) 10:1–14. doi: 10.3390/agronomy10081135

CrossRef Full Text | Google Scholar

38. Michael PS, Sanga HG, Shitindi MJ, Herzog M, Meliyo JL, Massawe BHJ. Uncovering spatiotemporal pattern of floods with Sentinel-1 synthetic aperture radar in major rice-growing river basins of Tanzania. Front Earth Sci. (2023) 11:1183834. doi: 10.3389/feart.2023.1183834

CrossRef Full Text | Google Scholar

39. Alaivasha E, Tumbo M, Senyangwa J, Mourice S. Influence of water management farming practices on soil organic carbon and nutrients : A case study of rice farming. Agronomy. (2022). doi: 10.3390/agronomy12051148

PubMed Abstract | CrossRef Full Text | Google Scholar

40. Marzouk SH, Tindwa HJ, Massawe BHJ, Amuri NA, Semoka JM. Pedological characterization and soil fertility assessment of the selected rice irrigation schemes, Tanzania. Front. Soil Sci. (2023). 3:1171849. doi: 10.3389/fsoil.2023.1171849

CrossRef Full Text | Google Scholar

41. Watanabe I, Berja NS. The growth of four species of azolla as affected by temperature. Aquat Bot. (1983). doi: 10.1016/0304-3770(83)90027-X

CrossRef Full Text | Google Scholar

42. Bagheri Novair S, Mirseyed Hosseini H, Etesami H, Razavipour T. Rice straw and composted azolla alter carbon and nitrogen mineralization and microbial activity of a paddy soil under drying–rewetting cycles. Appl Soil Ecol. (2020) 154. doi: 10.1016/j.apsoil.2020.103638

CrossRef Full Text | Google Scholar

43. Okalebo JR, Gathua KW, Paul LW. Laboratory methods of soil and plant analysis: A working manual (2nd ed.). Nairobi, Kenya: TSBF-CIAT and SACRED Africa. 1–131.

Google Scholar

44. Watanabe I, Padre B, Ramirez C, Watanabe I. Mineralization of azolla n and its availability to wetland rice: I. Nitrogen Mineralization of Different Azolla Species as Affected by Their Chemical Composition. Soil Sci Plant Nutr. (1991) 37:679–88. doi: 10.1080/00380768.1991.10416936

CrossRef Full Text | Google Scholar

45. Rochette P, Bertrand N. Soil-surface gas emissions. 2nd ed. Carter MR, editor. CANADA: Taylor and Francis group LLC (2007). doi: 10.1201/9781420005271.ch65

CrossRef Full Text | Google Scholar

46. Beretta AN, Silbermann AV, Paladino L, Torres D, Bassahun D, Musselli R, et al. Análisis de textura del suelo con hidrómetro: Modificaciones al método de Bouyoucus. Cienc e Investig Agrar. (2014) 41:263–71. doi: 10.4067/S0718-16202014000200013

CrossRef Full Text | Google Scholar

47. Nelson D, Sommers L. Chemical Methods Soil Science Society of America Book Series. Soil Science Society of America. Madison, WI 53711 USA (1996).

Google Scholar

48. Bremner M. Chapter 37: nitrogen-total. Methods Soil Anal Part 3. Chem Methods-SSSA B Ser. (1996) 5:1085–121.

Google Scholar

49. Bray RH, Kurtz LT. Determination of total, organic, and available forms of phosphorus in soils. Madison, Wisconsin, USA: Soil Science Society of America. Soil Science. (2009) 59(1):39–45.

Google Scholar

50. Mattigod SV, Zachara JM. Methods of soil analysis, Part 3 chemical methods soil. analysis, Part 3: Chemical methods. In J.B.D., S.B., Cheng, H.H., & R.L. (Eds.), Westerman methods of soil analysis (Soil Science Society of America Book Series). Madison, WI: Soil Science Society of America. doi: 10.2136/sssabookser5.3

CrossRef Full Text | Google Scholar

51. Lindsay WL, Norvell WA. Development of a DTPA soil test for zinc, iron, manganese, and copper. Soil Sci Soc America J. (1978) 42:421–8.

Google Scholar

52. Munyaka S, Putu K, Bimantara O, Kautsar V, Tawaraya K, Cheng W. Poultry litter biochar application in combination with chemical fertilizer and Azolla green manure improves rice grain yield and nitrogen use efficiency in paddy soil. Biochar. (2021). doi: 10.1007/s42773-021-00116-z

CrossRef Full Text | Google Scholar

53. Marschner H. Marschner’s mineral nutrition of higher plants. Mineral nutrition of higher plants. (3rd ed.). Elsevier (2012).

Google Scholar

54. Jimenez-Berni JA, Deery DM, Rozas-Larraondo P, Condon ATG, Rebetzke GJ, James RA, et al. High throughput determination of plant height, ground cover, and above-ground biomass in wheat with LiDAR. Front Plant Sci. (2018) 9:237. doi: 10.3389/fpls.2018.00237

PubMed Abstract | CrossRef Full Text | Google Scholar

55. Huang M, Fan L, Chen J, Jiang L, Zou Y. Continuous applications of biochar to rice: Effects on nitrogen uptake and utilization. Sci Rep. (2018) 8. doi: 10.1038/s41598-018-29877-7

CrossRef Full Text | Google Scholar

56. Marzouk SH, Tindwa HJ, Amuri NA, Semoka JM. Heliyon An overview of underutilized benefits derived from Azolla as a promising biofertilizer in lowland rice production. Heliyon. (2023) 9:e13040. doi: 10.1016/j.heliyon.2023.e13040

PubMed Abstract | CrossRef Full Text | Google Scholar

57. Rivaie AA, Isnaini S, Maryati. Changes in soil N, P, K, rice growth and yield following the application of Azolla pinnata. J Biol Agric Healthc. (2013) 3:112–7.

Google Scholar

58. Dhaliwal SS, Sharma V, Shukla AK, Verma V, Kaur M, Singh P, et al. Effect of addition of organic manures on basmati yield, nutrient content and soil fertility status in north-western India. Heliyon. (2023) 9:e14514. doi: 10.1016/j.heliyon.2023.e14514

PubMed Abstract | CrossRef Full Text | Google Scholar

59. Feyisa T, Amare T, Adgo E, Selassie YG. Symbiotic blue green algae (Azolla): A potential bio fertilizer for paddy rice production in Fogera Plain, Northwestern Ethiopia. J Sci Technol. (2013) VI:1–11.

Google Scholar

60. Zhou X, Liao YL, Lu YH, Rees RM, Cao WD, Nie J, et al. Management of rice straw with relay cropping of Chinese milk vetch improved double-rice cropping system production in southern China. J Integr Agric. (2020) 19:2103–15. doi: 10.1016/S2095-3119(20)63206-3

CrossRef Full Text | Google Scholar

61. Deng MH, Shi XJ, Tian YH, Yin B, Zhang SL, Zhu ZL, et al. Optimizing nitrogen fertilizer application for rice production in the Taihu Lake region. China: Pedosphere (2012). doi: 10.1016/S1002-0160(11)60190-2

CrossRef Full Text | Google Scholar

62. The SV, Snyder R, Tegeder M. Targeting nitrogen metabolism and transport processes to improve plant nitrogen use efficiency. Front Plant Sci. (2021) 11:628366. doi: 10.3389/fpls.2020.628366

PubMed Abstract | CrossRef Full Text | Google Scholar

63. Ye JY, Tian WH, Jin CW. Nitrogen in plants: from nutrition to the modulation of abiotic stress adaptation. Stress Biol. (2022) 2:1–14. doi: 10.1007/s44154-021-00030-1

PubMed Abstract | CrossRef Full Text | Google Scholar

64. Setiawati MR, Suryatmana P, Budiasih, Sondari N, Nurlina L, Kurnani BA, et al. (2018). Utilization Azollapinnata as substitution of manure to improve organic rice yield and paddy soil health, in: IOP Conference Series: Earth and Environmental Science, . Institute of Physics Publishing. doi: 10.1088/1755-1315/215/1/012006

CrossRef Full Text | Google Scholar

65. Mishra P, Dash D. Rejuvenation of biofertilizer for sustainable agriculture and economic development. Consilience: J Sustain Dev. (2014).

Google Scholar

66. Tian G, Gao L, Kong Y, Hu X, Xie K, Zhang R, et al. Improving rice population productivity by reducing nitrogen rate and increasing plant density. PloS One. (2017) 12:1–18. doi: 10.1371/journal.pone.0182310

CrossRef Full Text | Google Scholar

67. Zhou W, Yan F, Chen Y, Ren W. Optimized nitrogen application increases rice yield by improving the quality of tillers. Plant Prod Sci. (2022) 25:311–9. doi: 10.1080/1343943X.2022.2061538

CrossRef Full Text | Google Scholar

68. Lestari SU, Mutryarny E, Susi N. Azolla mycrophylla fertilizer for sustainable agriculture: compost and liquid fertilizer applications. Int J Sci Technol Res. (2019) 8:7.

Google Scholar

69. Bagheri S, Mirseyed H, Etesami H, Razavipour T. Rice straw and composted azolla alter carbon and nitrogen mineralization and microbial activity of a paddy soil under drying – rewetting cycles. Appl Soil Ecol. (2010) 154:103638. doi: 10.1016/j.apsoil.2020.103638

CrossRef Full Text | Google Scholar

70. Redda A, Abay F. Agronomic Performance of Integrated Use of Organic and Inorganic Fertilizers on Rice (Oryza sativa L.) in Tselemti District of North-Western Tigray, Ethiopia (2015). Available at: www.iiste.org.

Google Scholar

71. Setiawati MR, Damayani M, Herdiyantoro D, Suryatmana P, Anggraini D, Khumairah FH. (2018). The application dosage of Azolla pinnata in fresh and powder form as organic fertilizer on soil chemical properties, growth and yield of rice plant, in: AIP Conference Proceedings, . American Institute of Physics Inc. doi: 10.1063/1.5021210

CrossRef Full Text | Google Scholar

72. Vogeler I, Cichota R, Thomsen IK, Bruun S, Jensen LS, Pullens JWM. Estimating nitrogen release from Brassicacatch crop residues—Comparison of different approaches within the APSIM model. Soil Tillage Res. (2019) 195:104358. doi: 10.1016/j.still.2019.104358

CrossRef Full Text | Google Scholar

73. Zadeh AN. Effects of chemical and biological fertilizer on yield and nitrogen uptake of rice. J Bio Env Sci. (2014) 2014:37–46.

Google Scholar

74. Kimani SM, Bimantara PO, Hattori S, Tawaraya K, Sudo S, Cheng W. Azolla incorporation and dual cropping influences CH4 and N2O emissions from flooded paddy ecosystems. Soil Sci Plant Nutr. (2020) 66:152–62. doi: 10.1080/00380768.2019.1705736

CrossRef Full Text | Google Scholar

75. Jin N, Jin L, Wang S, Li J, Liu F, Liu Z, et al. Reduced chemical fertilizer combined with bio-organic fertilizer affects the soil microbial community and yield and quality of lettuce. Front Microbiol. (2022) 13:863325. doi: 10.3389/fmicb.2022.863325

PubMed Abstract | CrossRef Full Text | Google Scholar

76. Qian X, Shen Q, Xu G, Wang J, Zhou M. Nitrogen form effects on yield and nitrogen uptake of rice crop grown in aerobic soil. J Plant Nutr. (2004) 27:1061–76. doi: 10.1081/PLN-120037536

CrossRef Full Text | Google Scholar

77. Pathak H, Singh R, Bhatia A, Jain N. Recycling of rice straw to improve wheat yield and soil fertility and reduce atmospheric pollution. Paddy Water Environ. (2006) 4:111–7. doi: 10.1007/s10333-006-0038-6

CrossRef Full Text | Google Scholar

78. Mi W, Wu L, Brookes PC, Liu Y, Zhang X, Yang X. Changes in soil organic carbon fractions under integrated management systems in a low-productivity paddy soil given different organic amendments and chemical fertilizers. Soil Tillage Res. (2016) 163:64–70. doi: 10.1016/j.still.2016.05.009

CrossRef Full Text | Google Scholar

79. Gummert M, Nguyen, Hung V, Chivenge P, Douthwaite B. Sustainable Rice Straw Management. Martin Gummert BD, Van Hung N, Chivenge P, editors. lightweigh. Springer Cham (2020). doi: 10.1007/978-3-030-32373-8

CrossRef Full Text | Google Scholar

80. Li D, He H, Zhou G, He Q, Yang S. Rice yield and greenhouse gas emissions due to biochar and straw application under optimal reduced N fertilizers in a double season rice cropping system. Agronomy. (2023) 13. doi: 10.3390/agronomy13041023

CrossRef Full Text | Google Scholar

81. Yuan G, Huan W, Song H, Lu D, Chen X, Wang H, et al. Effects of straw incorporation and potassium fertilizer on crop yields, soil organic carbon, and active carbon in the rice–wheat system. Soil Tillage Res. (2021) 209:104958. doi: 10.1016/j.still.2021.104958

CrossRef Full Text | Google Scholar

82. Cissé M, Vlek PLG. Conservation of urea-N by immobilization-remobilization in a rice-Azolla intercrop Vol. 250. Springer Stable (2022) p. 95–104. Available at: https://www.jstor.org/stable/24129397. Conservation of urea-N by immobilization-remobi.

Google Scholar

83. Omara P, Aula L, Oyebiyi FB, Eickhof EM, Carpenter J, Raun WR. Biochar application in combination with inorganic nitrogen improves maize grain yield, nitrogen uptake, and use efficiency in Temperate Soils. Agronomy. (2020) 10. doi: 10.3390/agronomy10091241

PubMed Abstract | CrossRef Full Text | Google Scholar

84. Yadav RL. Assessing on-farm efficiency and economics of fertilizer N, P and K in rice wheat systems of India. F Crop Res. (2003) 81:39–51. doi: 10.1016/S0378-4290(02)00198-3

CrossRef Full Text | Google Scholar

85. Li T, Gao J, Bai L, Wang Y, Huang J, Kumar M, et al. Influence of green manure and rice straw management on soil organic carbon, enzyme activities, and rice yield in red paddy soil. Soil Tillage Res. (2019) 195:104428. doi: 10.1016/j.still.2019.104428

CrossRef Full Text | Google Scholar

86. Zhou G, Gao S, Chang D, Rees RM, Cao W. Using milk vetch (Astragalus sinicus L.) to promote rice straw decomposition by regulating enzyme activity and bacterial community. Bioresour Technol. (2021) 319:124215. doi: 10.1016/j.biortech.2020.124215

PubMed Abstract | CrossRef Full Text | Google Scholar

87. Sun R, Guo X, Wang D, Chu H. Effects of long-term application of chemical and organic fertilizers on the abundance of microbial communities involved in the nitrogen cycle. Appl Soil Ecol. (2015) 95:171–8. doi: 10.1016/j.apsoil.2015.06.010

CrossRef Full Text | Google Scholar

88. Aleminew A, Alemayehu G, Adgo E, Tadesse T. Influence of nitrogen on the growth and use efficiency of rainfed lowland rice in northwest Ethiopia. J Plant Nutr. (2020) 43:2243–58. doi: 10.1080/01904167.2020.1771574

CrossRef Full Text | Google Scholar

89. Rochette P, Angers DA, Chantigny MH, MacDonald JD, Bissonnette N, Bertrand N. Ammonia volatilization following surface application of urea to tilled and no-till soils: A laboratory comparison. Soil Tillage Res. (2009) 103:310–5. doi: 10.1016/j.still.2008.10.028

CrossRef Full Text | Google Scholar

90. Dhillon J, Torres G, Driver E, Figueiredo B, Raun, Lumpkin A, et al. World phosphorus use efficiency in cereal crops. Plant Soil. (2021) 9:1670–7. doi: 10.2134/agronj2016.08.0483

CrossRef Full Text | Google Scholar

91. Oyange WA, Chemining’wa GN, Kanya JI, Njiruh PN, Oyange WA, Agron IJ, et al. Effects of Azolla and inorganic nitrogen application on growth and yield of rice in mwea irrigation scheme International Journal of Agronomy and Agricultural Research (IJAAR). Int J Agron Agric R. (2019).

Google Scholar

92. Thapa P, Poudel K. Azolla: potential biofertilizer for increasing rice productivity, and government policy for implementation. J Wastes Biomass Manage. (2021) 3:62–8. doi: 10.26480/jwbm.02.2021.62.68

CrossRef Full Text | Google Scholar

93. Yao Y, Zhang M, Tian Y, Zhao M, Zeng K, Zhang B, et al. Azolla biofertilizer for improving low nitrogen use efficiency in an intensive rice cropping system. F Crop Res. (2018) 216:158–64. doi: 10.1016/j.fcr.2017.11.020

CrossRef Full Text | Google Scholar

94. Chen X, Liu M, Kuzyakov Y, Li W, Liu J, Jiang C, et al. Incorporation of rice straw carbon into dissolved organic matter and microbial biomass along a 100-year paddy soil chronosequence. Appl Soil Ecol. (2018) 130:84–90. doi: 10.1016/j.apsoil.2018.06.004

CrossRef Full Text | Google Scholar

95. Zhang B, Pang C, Qin J, Liu K, Xu H, Li H. Rice straw incorporation in winter with fertilizer-N application improves soil fertility and reduces global warming potential from a double rice paddy field. Biol Fertil Soils. (2013) 49:1039–52. doi: 10.1007/s00374-013-0805-7

CrossRef Full Text | Google Scholar

96. Seleiman MF, Elshayb OM, Nada AM, El-Leithy SA, Baz L, Alhammad BA, et al. Azolla compost as an approach for enhancing growth, productivity and nutrient uptake of oryza sativa L. Agronomy. (2022) 12. doi: 10.3390/agronomy12020416

PubMed Abstract | CrossRef Full Text | Google Scholar

97. Körschens M, Albert E, Armbruster M, Zorn W, et al. Effect of mineral and organic fertilization on crop yield, nitrogen uptake, carbon and nitrogen balances, as well as soil organic carbon content and dynamics: results from 20 European long-term field experiments of the twenty-first century. Arch Agron Soil Sci. (2013) 59(8). doi: 10.1080/03650340.2012.704548

CrossRef Full Text | Google Scholar

98. Tian K, Zhao Y, Xu X, Hai N, Huang B, Deng W. Effects of long-term fertilization and residue management on soil organic carbon changes in paddy soils of China: A meta-analysis. Agriculture Ecosyst Environ. (2015) . 204:40–50. doi: 10.1016/j.agee.2015.02.008

CrossRef Full Text | Google Scholar

99. Zhou J, Guan D, Zhou B, Zhao B, Ma M, Qin J, et al. Influence of 34-years of fertilization on bacterial communities in an intensively cultivated black soil in northeast China. Soil Biol Biochem. (2015) 90:42–51. doi: 10.1016/j.soilbio.2015.07.005

CrossRef Full Text | Google Scholar

100. Li M, Han X, Li LJ. Total nitrogen stock in soil profile affected by land use and soil type in three counties of mollisols. Front Environ Sci. (2022) 10:945305. doi: 10.3389/fenvs.2022.945305

CrossRef Full Text | Google Scholar

101. Akhtar M, Sarwar N, Ashraf A, Ejaz A, Ali S, Rizwan M. Beneficial role of Azolla sp. in paddy soils and their use as bioremediators in polluted aqueous environments: implications and future perspectives. Taylor and Francis Ltd (2020). doi: 10.1080/03650340.2020.1786885

CrossRef Full Text | Google Scholar

102. Dey M, Datta S. Nitrogen Fixation in Rice. Rice Improvement in the Genomics Era. Elsevier B.V (2008). doi: 10.1201/9781439822562.ch13

CrossRef Full Text | Google Scholar

103. Ekawati I, Purwanto Z. Application of immature rice straw compost, azolla, and urea for increasing rice fields production based on local wisdom. J Basic Appl Sci Res. (2014) 4:130–4.

Google Scholar

104. Tong R, Wu T, Jiang B, Wang Z, Xie B, Zhou B. Soil carbon, nitrogen, and phosphorus stoichiometry and its influencing factors in Chinese fir plantations across subtropical China. Front For Glob Change. (2023) 5:1086328. doi: 10.3389/ffgc.2022.1086328

CrossRef Full Text | Google Scholar

105. Landon JR. Booker tropical soil manual: A handbook for soil survey and agricultural land evaluation in the tropics and subtropics. Longman. (1991). doi: 10.4324/9781315846842

CrossRef Full Text | Google Scholar

106. Zhang P, Wei T, Li Y, Wang K, Jia Z, Han Q, et al. Effects of straw incorporation on the stratification of the soil organic C, total N and C:N ratio in a semiarid region of China. Soil Tillage Res. (2015) 153:28–35. doi: 10.1016/j.still.2015.04.008

CrossRef Full Text | Google Scholar

107. Chatterjee D, Nayak AK, Mishra A, Swain CK, Kumar U, Bhaduri D, et al. Effect of long-term organic fertilization in flooded rice soil on phosphorus transformation and phosphate solubilizing microorganisms. J Soil Sci Plant Nutr. (2021) 21:1368–81. doi: 10.1007/s42729-021-00446-8

CrossRef Full Text | Google Scholar