research study about fertilizer

ORIGINAL RESEARCH article

Effects of organic fertilizer incorporation practices on crops yield, soil quality, and soil fauna feeding activity in the wheat-maize rotation system.

• 1 Agro-Environmental Protection Institute (CAAS), Ministry of Agriculture and Rural Affairs, Tianjin, China
• 2 Key Laboratory for Protected Agricultural Engineering in the Middle and Lower Reaches of Yangtze River, Ministry of Agriculture and Rural Affairs, Institute of Facilities and Equipment in Agriculture, Jiangsu Academy of Agricultural Sciences, Nanjing, China

The decline in soil quality is becoming a significant process of soil degradation. Optimizing organic fertilizer incorporation practices in cropland is essential to enhancing crop productivity and soil health. However, that requires a comprehensive understanding of crop yield and soil quality reaction across an application gradient of organic fertilizer. We investigated the effect of organic fertilizer incorporation practices on crop yield, soil quality, and fauna feeding activity from fluvo-aquic soils on wheat ( Triticum aestivum )-maize ( Zea mays ) rotation field. The six treatments included were unfertilized N control (UC), traditional chemical fertilizer application (TF, 600 N kg ha −1  year −1 ), and recommended chemical fertilization (RF, 400 N kg ha −1  year −1 ) with no organic fertilizer application rate, low-level 15.0 (RFLO), medium-level 30.0 (RFMO), and high-level 45.0 t ha −1  year −1 (RFHO) application, respectively. The research findings show that the yield with organic fertilizer incorporation treatments increased 26.4%–44.6% for wheat and 12.5%–40.8% for maize compared to RF plots. The long-term organic fertilizer incorporation rate increased organic carbon from 54.7% to 110.6% versus UC plots and 27.9%–74.0% versus chemical fertilizer (TF and RF) treatments, and the total nitrogen content of soil increased from 41.8% to 59.2%, and 24.6%–39.2%. The long-term inorganic fertilizer combined with organic fertilizer incorporation practices significantly enhanced soil sucrose (30.1%–51.9%), urease (28.4%–38.3%), and β-1,4-glucosidase (34.6%–122.4%) activity. Still, nitrite reductase, polyphenol oxidase, and catalase significantly lower 27.3%–49.9%, 8.5%–26.3% and 23.3%–34.3% than single applications of inorganic N fertilizer groups. Meanwhile, the results showed that organic fertilizer incorporation practices improved soil fauna feeding activity by 35.2%–42.5%, and the excessive application of inorganic N fertilizer reduced the activity level of soil fauna.

Introduction

Organic fertilizers are materials with defined chemical composition and high nutritional value that can provide adequate nutrients for plant growth ( Moller and Schultheiss, 2015 ; Rajan and Anandhan, 2015 ). Organic fertilizers were mainly made by composting animal manure, human excrement, or plant matter (such as straw and garden waste) under microorganisms fermenting at high temperatures ( Chew et al., 2019 ). Organic fertilizers improve the soil structure, provide a wide range of plant nutrients, and add beneficial microorganisms to the soil. Because of the benefits of organic fertilizers on soil structure and crop yield were widely used in the agricultural system ( Brar et al., 2015 ; Maltas et al., 2018 ).

Organic fertilization practices can improve crop yields and soil quality, and combining organic and inorganic fertilizers was considered an effective solution to maintain the sustainability of crop ecosystems ( Gentile et al., 2008 ). The application of organic fertilizers can not only improve soil structure and fertility, and increase soil organic carbon and other nutrients ( Diacono and Montemurro, 2010 ; Liu et al., 2010 ). Many studies have shown that applying organic fertilizers to the soil surface can provide a rich food source for microorganisms and significantly increase microbial community composition and diversity compared to no application ( Chang et al., 2007 ; Diacono and Montemurro, 2010 ). In addition, applying organic fertilizers significantly changes cation exchange capacity (CEC) and increases soil moisture content, causing changes in soil fauna community structure and composition in acidic soils ( Zelles et al., 1992 ; Abbott and Murphy, 2007 ). Adding organic fertilizers benefits the formation and stability of earthworm communities due to the more stable nutrients in organic manure after aerobic fermentation ( Bertrand et al., 2015 ). In contrast, others have found that long-term use of chemical fertilizers may reduce soil OM content and change the activity of soil biota, resulting in changes in soil microbial composition, and resulting in decreased soil invertebrates abundance and diversity due to environmental constraints and reductions in soil pH ( Fauci and Dick, 1994 ; Davies et al., 2022 ). Wahyuningsih et al. (2019) show that the short-term applications of inorganic fertilizers (urea) significantly increased the soil fauna feeding activity after 2 days, compared to before the application. Tao et al. (2016) also show that soil organic matter (empty fruit bunch) plays an important role in soil ecosystem functioning by enhancing soil fauna feeding activity. Therefore, many studies have announced the effects of fertilization practice on soil nutritions, but the effects of inorganic combined with organic fertilizers on soil biota remain unclear.

In the wheat-maize rotation system, long-term fertilization is an essential factor affecting soil physicochemical properties and biota functions ( Welbaum et al., 2004 ; Kaiser et al., 2007 ; Thomas et al., 2007 ; Miao et al., 2011 ; Chen et al., 2015b ; Miller et al., 2020 ; Miner et al., 2020 ), and its response mechanism is mainly related to local climatic conditions, soil types, and fertilizer types ( Lupwayi et al., 2011 ; Yu et al., 2015 ). Qaswar et al. (2020) and Gao et al. (2015) studies show that combining organic and inorganic fertilizers is one of the essential techniques to replace part of the inorganic chemical fertilizers and stabilize wheat and maize yield. Many studies have shown that replacing 20%–30% of chemical fertilizers with organic fertilizers can increase wheat-maize yields and improve soil availability and organic matter ( Zhang et al., 2016b ). Then, the applications of organic fertilizers were a relatively large range of variation, and the fresh weight of compost was generally from 10.0 to 35.0 t ha −1 ( Hannet et al., 2021 ), and the application rate of dry matter of compost between 8.8 and 14.0 t ha −1 , but liquid manure up to 68.3 t ha −1 ( Feng et al., 2013 ). This suggests the need for a better balance of the impact of fertilization with different organic fertilizer incorporation rates on the wheat-maize rotation system. Moreover, few have conducted long-term investigations of inorganic chemical fertilizers combined application of organic fertilizers with different incorporation rates for soil quality and health, including total soil carbon, organic carbon, nutrients, enzyme activities, and soil fauna activities.

The study aimed to determine the influence of inorganic combined with organic fertilizer incorporation practices (high, medium, and low levels) on crop yields, soil quality, and the fauna feeding activity on fluvo-aquic soil in north China.

Methods and materials

Site description.

The research treatments were set up starting in 2015 at Tianjin Experimental Farm (TEF), which is located in the suburbs of Tianjin, North China (39°28′N, 117°42′E, Supplementary Figure S1 ). The region belongs to a temperate monsoon climate, with an annual mean air temperature of 12.9°C and rainfall 586 mm, respectively (2015–2020) ( Zhou et al., 2021 ). Rainfall is concentrated between July and September, with a tremendous annual variation. This soil was classified as fluvo-aquic soil, and the values of TN, OM, TP, and pH in soil (0–20 cm) were 0.82, 12.6, 0.80 and 8.1 g kg −1 , respectively.

Experimental design

The research treatments were conducted on a wheat-maize rotation system with the same cultivation and management practice from October 2019 to October 2020. In previous years, all wheat-maize straw was returned to the field following management practices. The six trial treatments of each area being 288 m 2 with three replicates, were established in 2015. The treatments included were unfertilized N control (UC), traditional chemical fertilizer application (TF, 600 N kg·ha −1  year −1 ), and recommended chemical fertilization (RF, 400 N kg·ha −1  year −1 ) with zero organic fertilizer (O) application rate, low-level 15.0 (RFLO), medium-level 30.0 (RFMO), and high-level 45.0 t ha −1  year −1 (RFHO) application, respectively. The recommended fertilization was based on the local soil characteristics and the crop target yield, combined with precision irrigation conditions ( Cai and Qin., 2006 ; Yang et al., 2015 ). The recommended inorganic NPK fertilizers were urea (46.4% N), diammonium phosphate (18% N and 20.09% P), and potassium chloride (49.6% K), respectively ( Zhou et al., 2021 ). In this study, inorganic nitrogen fertilizer was the limiting factor; when applying inorganic N fertilizer, simultaneously apply 200 kg ha −1  year −1 P and K fertilizer as base fertilizer. The organic fertilizer was produced through high-temperature fermentation of garden wastes and agricultural straw, by Xixing Fertilizer Technology Co., Ltd. (Shijiazhuang, China). The values of OM, TN, and TP in organic fertilizer were 86.6 ± 4.9, 6.18 ± 0.10, and 3.39 ± 0.07 g kg −1 , respectively ( Zhou et al., 2021 ). The inorganic NPK rate in each wheat and maize season was half the annual application amount in six trial treatments, respectively. The application rates of fertilizers under different fertilization treatments was shown in Table 1 . Two-thirds of the inorganic nitrogen fertilizer and the entire quantity diammonium phosphate and muriate potash fertilizer was applied when sowing as basal fertilizer, and one-third of nitrogen fertilizer is mainly used for top-dressing applications of wheat and maize, respectively. The organic fertilizer was applied to the soil surface by scattering before wheat sowing and incorporated into the topsoil by rotary tillage.

TABLE 1 . Application rates of fertilizers under different fertilization treatments.

Field sampling and processing

The quadrat method determined the winter wheat yield by harvesting three 1 m 2 sampling areas per treatment ( Lu et al., 2018 ). At the summer maize maturity stage, 20 plants were randomly selected from the middle row of each plot and harvested manually to determine the yield ( Lu et al., 2018 ). The remaining crop was harvested mechanically.

Less than 1 week after harvest, three soil samples (each was a composite of five cores that formed one sample, 5.0 cm in diameter) were collected from each treatment at 20 cm depth on 24 October 2019 and 22 October 2020 to determine the chemical properties ( Zhou et al., 2021 ). The chemical properties of soil were determined, including TC, TOC, TN, AN, TP, AP, TK, exchangeable Ca, Mg, K, Na concentrations, and CEC, EC, and soil pH values. The pH value and electric conductivity (EC) of the soil were measured with a glass electrode and extracted in a 1:2.5 soil/water (H 2 O) suspension after being allowed to stand for 30 min ( Zhang et al., 2016b ). The Dumas dry-combustion method analyzed all dry soil samples collected for total soil nitrogen (TC) and soil nitrogen (TN) contents using a PerkinElmer 2400 Series Ⅱ CHNS/O Analyzer (PerkinElmer Inc., Shelton, CT, United States). Soil total organic carbon (TOC) was determined using K 2 Cr 2 O 7 –H 2 SO 4 digestion. The alkaline hydrolysis diffusion method determined the available soil nitrogen (AN). The molybdenum blue colorimetrically determined the soil’s total phosphorus (TP) content after extraction with a mixed acid solution of H 2 SO 4 and HClO 4 . Available phosphorus (AP) was determined colorimetrically after sodium bicarbonate extraction at pH 8.5. The content of total potassium (TK) in soil was determined by flame photometer detection using H 2 SO 4 –H 2 O 2 digestion ( Bao, 2008 ; Sunnemann et al., 2021 ). The concentrations of exchangeable Na, Mg, K, and Ca in soil were measured by ICP-OES (Agilent, 710 Series) after extraction with 1.0 mol L −1 ammonium acetate ( Setia et al., 2013 ). The cation exchange capacity (CEC) was calculated with colorimetrically after using a hexamminecobalt (III) chloride extraction ( ISO, 2018 ). Air-dried soil samples were sifted through a 2 mm sieve for soil enzyme activity determination. The six soil enzymes activity involved in C and N cycling were studied, including soil catalase, soil nitrite reductase, soil sucrase, soil urease, soil polyphenol oxidase, and soil β-1,4-glucosidase, and was determined spectrophotometrically with the soil enzyme kits provided by Suzhou Comin Biotechnology Company Limited (Suzhou, China) ( Liu et al., 2018 ; Gao et al., 2019 ).

Soil fauna feeding activity

Törne (1990) set up the bait lamina test for soil fauna feeding activity for soil environmental quality assessment. The bait lamina is made of polyvinyl chloride board (PVC board, gray), and the size by 120 mm × 6.0 mm × 1.0 mm (length × width × thickness) with a set of 16 double tapered holes (inner diameter 1.5 mm, outer diameter 2.0 mm) at the lower 85 mm, with the aperture spacing of 5 mm ( Römbke et al., 2006 ). The standard feed for bait lamina filling usually consists of 70% cellulose (microparticles), 27% bran flakes (<500 mm), and 3% activated carbon ( Eisenhauer et al., 2014 ). After filling double tapered holes with standard feed, insert the bait strip vertically into the soil, and the top hole was just below the soil surface ( Supplementary Figure S2 ). In this study, soil fauna activities were measured from September 15 to 30 in 2019 and September 9 to 24 in 2020, respectively. Five test areas were set up for each treatment, and 5 strips per area were placed about 15–20 cm apart to monitor the feeding activities of soil fauna with 150 bait lamina in total. After 2 weeks of monitoring, the bait strips were taken from the soil and evaluated with filled (0), partly empty (0.5), and empty (1) ( Vorobeichik and Bergman, 2021 ), to calculate the number of perforated bait strips at each study site and evaluate the percentage of perforated bait strips to the number of test holes in the field. In this study, soil temperature was measured using a HOBO U23-003 sensor (Onset Computer Corporation, Pocasset, MA, United States).

Statistical analysis

Statistical analysis used the Statistical Analysis System (SAS 9.2) software package and Origin Pro 2022 software. Analysis of variance and comparisons of means between treatments was determined using Duncan’s multiple range test, and correlations between soil chemical properties were determined using Spearman’s correlation coefficient analysis. Treatment impacts were reported to be significant at the 5% probability level.

Crop production

The grain yields of wheat and maize according to fertilization management practices are shown in Figure 1 . Different fertilization management practices significantly affect wheat and maize yields, and there was no significant difference in the yield of wheat and maize between different years ( Table 2 ). The grain yields ranged from 0.68 to 6.35 t ha −1 for wheat and 5.40 to 9.77 t ha −1 for maize in 2018–2020. There was no difference in the wheat yields between different organic fertilizer (RFLO, RFMO, RFHO) incorporation and traditional fertilization (TF) treatments in 2018–2019, while the RFHO and TF significantly ( p < 0.05) increased the maize yield by 34.7%, 36.6% as compared with RF, respectively. In 2019–2020, the medium and high organic fertilizer (RFMO, RFHO) incorporation and TF treatments increased the wheat yield by 36.4%, 50.6%, and 41.5% compared to RF, respectively ( p < 0.05). There was no difference in wheat yields between RFMO, RFHO, and TF treatments. Similar to the 2018–2019 year, the RFHO and TF plots increased the maize yield by 47.2%, and 42.8% compared to RF, respectively ( p < 0.05).

FIGURE 1 . Wheat and maize yield (2018–2019, 2019–2020) is according to fertilization management practices. UC, unfertilized control; RF, recommended mineral fertilizer application of 400 kg ha −1 N; RFLO, RF plus 15 t ha −1 of organic fertilizer; RFMO, RF plus 30 t ha −1 of organic fertilizer; RFHO, RF plus 45 t ha −1 of organic fertilizer; TF, traditional mineral fertilizer application of 600 kg ha −1 N, whole wheat-maize growing season. The same letters are not significantly different at 5% level by Duncan’s Multiple Range Test.

TABLE 2 . Effects of fertilizer management practices and years on crop yield.

Soil physicochemical properties

Table 3 shows the soil chemical variables under each soil fertilizer management practice at 0–20 cm soil depth. Eleven variables were significantly affected by long-term inorganic combined with organic fertilizer incorporation practices compared with inorganic fertilizer plots ( Table 3 ). The soil chemical parameters were significant correlations ( Table 4 ). Organic fertilizer incorporation led to significant changes in total organic carbon (TOC) and total carbon (TC), levels of soil nutrients (Total N and P, Available N and P), and soil chemical properties of RFHO, RFMO, and RFLO plots, as compared to the RF and TF. The long-term organic fertilizer incorporation rate increased total organic carbon (TOC) from 54.7% to 110.6% versus unfertilized soil and 27.9%–74.0% versus chemical fertilizer treatments. TC content showed the same trend as TOC, increasing 19.5%–49.1% compared with UC and 17.2%–46.3% compared with RF. Soil total organic carbon (TC) and total organic carbon (TOC) increased positively under organic fertilizer plots with higher 2.2–6.0 g kg −1 for TC, and 2.4–6.4 g kg −1 for TOC than RF.

TABLE 3 . Soil chemical variables under each soil fertilizer management practice at 0–20 cm soil depth.

TABLE 4 . Spearman’s correlation coefficients between soil chemical variables.

The contents of total soil nitrogen (TN) and available nitrogen (AN) in the organic fertilizer incorporation plots increased significantly by 41.8%–59.2%, 56.1%–82.7% versus unfertilized soil (UC), and 24.6%–39.2%, 25.6%–46.9% compared with the application of recommended mineral fertilizer (RF), with the increase of the amount of organic fertilizer. Still, RFLO, RFMO, and RFHO treatments did not reach a significant level ( p > 0.05). Compared with the RF treatment, the contents of total phosphorus (TP) and available phosphorus (AP) in the RFHO plots increased by 33.3% and 95.4%, respectively, and RFMO plots increased by 37.0% and 115.8%, and RFLO plots increased by 18.2% and 43.2%, respectively. However, there was no significant difference between RFHO and RFMO treatments ( p > 0.05). Soil TK concentration remained at the same levels across all plots.

Compared with the UC, the fertilization treatment plots pH decreased by 0.49%–5.68%, while the organic fertilizer (RFLO, RFMO, RFHO) incorporation significantly reduced the pH by 3.40%, 5.44%, and 5.68% ( p < 0.05), respectively. The content of exchangeable Ca in the organic fertilizer incorporation was significantly lower 10.05%, 7.64%, and 9.82%, than in the TF plots ( p < 0.05). While no difference in the exchangeable Mg and CEC between different organic fertilizer (RFLO, RFMO, RFHO) incorporation and chemical fertilizer plots. The contents of exchangeable K and Na in the organic fertilizer incorporation plots significantly increased 49.4%–122.2%, and 21.4%–107.4%, compared with inorganic fertilizer. Figure 2 shows PCA for soil characteristics according to fertilization management practices. The PCA results show that the cumulative contribution of the first three principal components reached 84.7% (PC1: 62.9%; PC2: 13.8%; PC3: 8.0%; Supplementary Table S1 ).

FIGURE 2 . Principal component analysis (PCA) for soil chemical characteristics (2019, 2020) is formed by the first principal component (PC1) and the second principal component (PC2) according to fertilization management practices. * Ca, exchangeable Ca concentration (mg·kg −1 ); Mg, exchangeable Mg concentration (mg·kg −1 ); TK, total K concentration (g·kg −1 ); CEC, cation exchange capacity (cmol·kg −1 ); AN, available nitrogen (mg·kg −1 ); TP, total P concentration (g·kg −1 ); K, exchangeable K concentration (mg·kg −1 ); TN, total N concentration (g·kg −1 ); TOC, organic C concentration (g·kg −1 ); TC, total C concentration (g·kg −1 ); Na, exchangeable Na concentration (mg·kg −1 ); AP, available P concentration (mg·kg −1 ); EC, electrical conductivity (μs·cm −1 ).

Soil enzyme activity

Organic fertilizer incorporation led to significant changes in the nitrite reductase, catalase, sucrase, urease, β-1,4-glucosidase, and polyphenol oxidase at different plots ( Table 5 ). Compared to RF plots, organic fertilizer incorporation plots significantly increased by 28.4%–38.3%, 34.6%–122.4%, and 30.1%–51.9% of soil urease, β-1,4-glucosidase, and sucrase activity ( p < 0.05). The nitrite reductase and catalase activity in the organic fertilizer plots was 3.17–4.59 μmol d −1  g −1 and 14.9–17.2 μmol d −1  g −1 , significantly lower 27.3%–49.9%, and 23.3%–34.3% than in the RF plots, respectively ( p < 0.05). In the TF plots, the activity of nitrite reductase increased 98.7% and 27.6% more than in all organic fertilizer treatments and RF plots ( p < 0.05). Compared with organic fertilizer treatments and RF plots, the polyphenol oxidase activity of TF plots increased by 65.5% and 35.3%, respectively. However, the activity of polyphenol oxidase was not significantly different between TF and UC plots ( p < 0.05).

TABLE 5 . Soil enzyme variables under each soil fertilizer management practice at 0–20 cm soil depth.

This study significantly reduced soil fauna feeding activity in inorganic fertilizer plots. The feeding activities of soil fauna in the traditional fertilization (TF) and recommended fertilization (RF) site were lower than in all the other plots, about 24.6% in the RF site and 21.6% in the TF site ( Figure 3 ). We measured the highest average feeding activities in RFLO (35.2%), RFMO (46.8%), and RFHO (42.5%) compared with the other three investigation sites between 2019 and 2020. In RFLO, RFMO, and RFHO, adjoint with increased organic fertilizer incorporation, soil fauna feeding activities were significantly increased compared with RF and TF plots; however, the differences were not statistically significant in RFMO and RFHO plots. Furthermore, RFLO (31.9%) and RFMO (38.8%) in 2019, which had been treated additionally with organic fertilizer, showed higher feeding activities than UC (26.3%), but not significant. Throughout the 0–8 cm soil depth, the UC, RF, and TF treatments showed identical distributions, while RFLO, RFMO, and RFHO had consistent distribution trends ( Figure 4 ). Compared with the organic fertilizer sites, feeding activities in RF and TF treatments showed that they rapidly decreased with increasing soil depth, compared with RFLO, RFMO, and RFHO, and reached a plateau after 4 cm. In the 0–6 cm layer soil depth, the soil fauna feeding activity in organic fertilizer plots was significantly higher compared with the UC and inorganic fertilizer plots ( Figure 4 ).

FIGURE 3 . Feeding activities (%) in the six fertilization management practices were determined by the bait-lamina test ( n = 150 bait laminae) after 15 days of exposure in September 2019, and 2020. The data are median values, and the vertical bars represent SDs. Columns marked by different letters indicate significant differences at p < 0.05.

FIGURE 4 . Depth profiles of the feeding activities (%) in the six fertilization management practices were determined by the bait-lamina test ( n = 150 bait laminae) after 15 days of exposure in September 2019 (A) , and 2020 (B) .

Effect of organic fertilizer incorporation on crop yields

The results showed that compared with the recommended fertilization, the application of organic fertilizer significantly increased the yield of wheat ( p < 0.05). Compared with the recommended fertilization (RF), the treatment of medium (RFMO) and low organic fertilizer (RFLO) had no significant influence on maize yield ( p > 0.05), and the RFMO and RFLO plots were significantly lower than the high amount of organic fertilizer (RFHO) and the traditional fertilization treatment (TF). Similarly, Yang et al. (2014) reported that combinations of organic and inorganic nitrogen are likely to increase achievable yields and improve soil fertility with the wheat-maize system. This might be due to all organic fertilizers being used as base fertilizers in the wheat season, all chemical fertilizers being used in maize planting, and organic fertilizer incorporation into the soil, which increased soil OM contents, soil water availability, and aeration ( Choudhary et al., 2018 ; Li et al., 2020 ). Welbaum et al. (2004) and Li et al. (2012) reported that when organic fertilizers incorporation can delay the senescence rate of crop roots and leaves, prolong the photosynthetic time of crops, increase the grain quality of ears by prolonging the grain filling time, and finally increase the yield. Studies have shown that the recommended fertilization amount requires good water and fertilizer management to maximize crop yield ( Zhang et al., 2021 ). The lower wheat yield in the recommended fertilization amount in this study may be caused by flood irrigation resulting in reduced plant availability of nitrogen ( Li and Rao, 2003 ; Shang et al., 2015 ). The traditional fertilization (TF) could increase crop yields, indicating that inorganic N fertilizer input significantly affects crop yields; the soil organic fertilizers incorporation significantly affects TOC content and yields ( Table 2 ). This result suggests that long-term studies were required to identify the effect of the inorganic combined with organic fertilizers on wheat-maize yield constraints and soil fertility.

Effect of organic fertilizer incorporation on soil chemical properties

The combined application of organic-inorganic fertilizers can provide quick-acting nutrients for crop growth, and effectively increase fertilizer efficiency and ensure the continuous supply of soil nutrients ( Diacono and Montemurro, 2010 ). This study found that organic fertilizer incorporation benefited TC and TOC content, and medium and high levels (>30 t ha −1  year −1 ) significantly increased TC, and TOC contents compared to RF and TF treatment. The content of nitrogen (TN, AN) and phosphorus (TP, AP) in the organic-inorganic fertilizers treatment was higher than in the no fertilizer treatment and chemical fertilizer treatment, the same trend as TC and TOC. Liu et al. (2015) and Cai and Qin (2006) research shows that organic fertilizer incorporation can increase TOC capacity by improving agricultural root biomass and exudates. Chen et al. (2015a) studies indicate that soil nutrient content increases after organic fertilizer incorporation and the increase rate is mainly affected by the type and amount of organic fertilizer. Organic fertilizer incorporation increased crop yields, and soil organic matter and nutrient content were improved, consistent with the research of Gao et al. (2015) and Choudhary et al. (2018) . The traditional mineral fertilizer (TF) significantly increased wheat and maize yields. Still, it did not have a significant influence on TC and TOC ( p > 0.05), similar to the findings of Chen et al. (2015a) considered that the balanced application of inorganic fertilizers could keep farmers high, but it has a limited impact on soil carbon sequestration. Moreover, additional C, N, and P releases in the high-rate organic fertilizers could partly explain our findings. In addition, combined application of organic-inorganic fertilizers treatments increased exchangeable K, while the same treatments did not significantly increase the content of soil TK, relative to the UC and RF, consistent with the research of Hannet et al. (2021) , indicating that potassium in the soil is not a limiting factor in alkaline soils. In this study, organic fertilizer incorporation significantly decreased soil pH and exchangeable Ca concentration, while exchangeable Na concentration and electrical conductivity increased in these plots compared with inorganic fertilizer. The pH of alkaline soil tends to decrease with the increase of commercial organic fertilizer application years, and the soil pH tends to be neutral, which is beneficial to the better growth of crops ( Oyetunji et al., 2022 ). Demelash et al. (2014) reported increased Ca and Mg content with applying organic-inorganic fertilizers treatments, but it was not observed to increase the levels of other alkaline elements (K, Na). In this study, although the exchangeable Ca decreased, the exchangeable Na and K concentrations increased significantly. Organic fertilizer and soil type may be the main reasons for these differences ( Abu Bakar et al., 2011 ; Manolikaki and Diamadopoulos, 2019 ; Jain and Kalamdhad, 2020 ). In this study, the cation exchange capacity (CEC) of soil increased by 4.9%–5.6% due to organic fertilizer incorporation; the same finding by Ouédraogo et al. (2001) and Cooper et al. (2020) studies that the increase in CEC with organic fertilizer application could be attributed to an increase in TOC. Still, it did not significantly affect (CEC) relative to the inorganic fertilizer plots in this study. It shows that based on stabilizing the wheat-maize yield, the soil quality of the wheat-maize planting area can be improved by combining organic and inorganic methods.

Effect of organic fertilizer incorporation on soil enzyme activity

Studies have shown that fertilization management and incorporation of organic matter can affect soil enzyme activity ( Zhao et al., 2016 ; Li et al., 2017 ). Urease is closely related to soil nitrogen supply, and improving urease activity in the soil can convert organic nitrogen with high stability to available nitrogen ( Zhang et al., 2016a ). Therefore, the improvement of urease activity indicated that adding organic fertilizer incorporation improved soil nitrogen conversion. Li et al. (2010) and Wang et al. (2021) study found that soil catalase activity increased with more organic nitrogen, while Yang et al. (2018) showed no significant effect with the incorporation of cattle manure and biochar. The fertilization management practices decreased soil catalase, and nitrite reductase activity in this study may be caused by different soil types, organic fertilizer types and sampling time ( Li et al., 2017 ). Soil sucrose and β-1,4-glucosidase reflects soil organic carbon accumulation and are an essential indicator of soil fertility ( Zhang et al., 2016b ; Ullah et al., 2019 ). The response of invertase and β-1,4-glucosidase to different fertilization practices was consistent with that of urease. The long-term addition of organic fertilizers significantly increased the activity of soil sucrose and β-1,4-glucosidase, mainly due to the soil organic carbon increase ( Table 3 ). Polyphenol oxidase may suppress the synthesis of humic substances from phenolic intermediates produced during the mineralization of organic C, resulting in the accumulation of phenolic compounds ( Wang et al., 2022 ). Applying organic fertilizers significant reduces the accumulation of phenolic substances and possible poisoning. In the long-term organic fertilizer incorporation plots, the decomposed organic matter provides sufficient energy and carbon source for soil microbial activities, accelerates the reproduction and growth of microorganisms, and improves soil physicochemical properties ( Tiemann and Billings, 2011 ; Ai et al., 2012 ; Bowles et al., 2014 ). At the same time, organic fertilizer also contains many enzymes, which are beneficial to improve soil enzyme activity ( Li et al., 2017 ). Therefore, the inorganic fertilizer combined with organic fertilizer incorporation practices can significantly increase the activities of urease (S-UE), sucrose (S-SC), and β-1,4-glucosidase (S-B-GC) in the soil compared with the chemical fertilizer.

Effect of organic fertilizer incorporation on soil fauna feeding activity

This study found that soil fertilizer management influenced the feeding activities of soil fauna, and these responses were closely related to soil nutrition. Organic fertilizer application greatly enhanced soil fauna feeding activity, and then inorganic nitrogen fertilizer reduced the soil fauna feeding activity. The highest feeding activity rates were found in plots RFMO and RFHO with a larger amount of organic fertilizer incorporation practices, and traditional fertilization treatment (TF) had the lowest feeding activities ( Figure 3 ). However, the feeding activity of soil fauna showed no significant differences between the control UC and inorganic fertilizer (RF and TF) plots. Studies have shown that the experimental time of using the Bait Lamina test is short, usually 3–15 days, and microorganisms cannot decompose and perforate organic matter in a short time, and nematodes, microarthropods such as earthworms, mites, enchytraeids, and collembolans was the main soil fauna causing bait perforation ( Gongalsky et al., 2008 ; Birkhofer et al., 2011 ). Although some microorganisms are involved in feeding activities, the feeding activities is negligibly small compared to soil fauna ( Gestel et al., 2003 ; Ashford et al., 2013 ). Applying organic fertilizers increased soil fauna feeding activities, which may be related to the changed soil fauna community’s abundance and composition, leading to higher soil fauna feeding activity ( Tao et al., 2016 ). This may explain why the highest feeding activity rates were found in plots RFMO and RFHO with a larger amount of organic fertilizer incorporation practices. The feeding activity of soil fauna in the inorganic fertilizer combined with organic fertilizer polts was high in the 0–6 cm depth range. Many studies show that feeding activities of soil fauna were strongly reduced from 4 to 8 cm soil layer in grassland and forest sites ( Larade et al., 2012 ; Filzek et al., 2004 ; Gongalsky et al., 2008 ; Rożen et al., 2010 ). Other studies showed that soil fauna feeding activities were higher in the bottom of 5–8 cm soil layer than in topsoil layers at ryegrass and soybean fields ( Marx et al., 2016 ; Mousavi et al., 2022 ). The long-term inorganic fertilizer combined with organic fertilizer incorporation practices significantly increased the soil fauna feeding activity, while the application of RFHO and RFMO did not significantly increase. Soil fertilizer management may affect soil fauna feeding activities by the soil chemical properties; meanwhile, the feeding activities of soil fauna affect the soil physicochemical properties by regulating the decomposition process of soil organic matter ( Römbke et al., 2006 ; Briones and Schmidt, 2017 ). Geissen and Brummer (1999) research show a strong correlation between soil fauna feeding activities and chemical parameters, and fauna feeding activity increased with higher pH values in acid soil.

In contrast, we found that the soils under organic fertilizer had the higher exchangeable K, Na, EC, nutrients (AN, AP), and TOC of all the management practices; however, the lowest pH and exchangeable Ca in alkaline soil ( Table 3 ). The feeding activity of soil fauna was in organic fertilizer plots significantly higher than inorganic fertilized (RF and TF) plots and unfertilized (UC) plots. Soil water content and soil temperature are the main environmental factors affecting fauna feeding activities. The feeding activity of fauna measured with the bait-laminae showed that the feeding activities increased with temperature ( Gongalsky et al., 2008 ). Drought seriously affects the activities of invertebrates, especially earthworms that like moist soil ( Eggleton et al., 2009 ). Törne (1990) research showed that in cracked clay with low moisture content in Germany, the percentage of bait bar perforation was between 4% and 16%. Precipitation explained the variation in feeding rates observed between 2019 and 2020 ( Supplementary Figure S3 ).

We examined the effects of inorganic fertilizer combined with organic fertilizer incorporation practices on crop yields, soil quality, and fauna feeding activity. We showed that long-term inorganic fertilizer combined with organic fertilizer incorporation practices enhanced soil organic carbon, nutrition, and fauna feeding activity and significantly enhanced soil sucrose, urease, and β-1,4-glucosidase activity. Soil organic carbon, total nitrogen, and fauna activity showed a linear increase of 27.9%–74.0%, 24.6%–39.2%, and 35.2%%-42.5%, respectively, but the enzyme activity did not increase with the increase of organic fertilizer incorporation. In our studied area, the treatment of medium levels (30 t ha −1  year −1 ) may be recommended from crop yields and soil carbon sequestration. Our study findings have important significance for the application of organic fertilizer to the wheat-maize rotation systems.

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 authors.

Author contributions

ZZ: data curation, formal analysis, writing—original draft, and writing—review and editing. SZ: data curation, formal analysis, and writing—review and editing. NJ: formal analysis, investigation. WX: investigation, validation, and writing—review and editing. JZ: conceptualization, funding acquisition, and writing—review and editing. DY: funding acquisition, methodology, writing review and editing, supervision.

This work was supported by the Central Public-Interest Scientific Institution Basal Research Fund (Agro-Environmental Protection Institute, Ministry of Agriculture and Rural Affairs) and the Cooperative Innovation Project of Agricultural Science and Technology Innovation Program of CAAS (CAAS-XTCX2016015).

Acknowledgments

We sincerely appreciate the cooperation and assistance of the Tianjin Experimental Farm in the implementation of this field study.

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.

Supplementary material

The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fenvs.2022.1058071/full#supplementary-material

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Zhou, Z., Yang, D., Zhao, J., Zhang, H., and Wang, L. (2021). Emissions of greenhouse gas and ammonia from an intensive wheat site affected by different fertilization practices. AvaliableAt: https://elibrary.asabe.org/abstract.asp?aid=52457&t=5 .

Keywords: soil organic carbon, soil nutrients, organic fertilizer incorporation, soil enzymes, soil fauna feeding activity, feeding activity

Citation: Zhou Z, Zhang S, Jiang N, Xiu W, Zhao J and Yang D (2022) Effects of organic fertilizer incorporation practices on crops yield, soil quality, and soil fauna feeding activity in the wheat-maize rotation system. Front. Environ. Sci. 10:1058071. doi: 10.3389/fenvs.2022.1058071

Received: 04 October 2022; Accepted: 01 November 2022; Published: 17 November 2022.

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Copyright © 2022 Zhou, Zhang, Jiang, Xiu, Zhao and Yang. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: Jianning Zhao, [email protected] ; Dianlin Yang, [email protected]

Disclaimer: 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.

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• Published: 13 January 2020

Bio-organic fertilizer with reduced rates of chemical fertilization improves soil fertility and enhances tomato yield and quality

• Lin Ye 1 , 2 ,
• Xia Zhao 1 , 2 ,
• Encai Bao 3 ,
• Jianshe Li 2 ,
• Zhirong Zou 1 &
• Kai Cao 3  

Scientific Reports volume  10 , Article number:  177 ( 2020 ) Cite this article

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• Plant physiology

The extensive use of chemical fertilizers poses serious collateral problems such as environmental pollution, pest resistance development and food safety decline. Researches focused on applying plant-beneficial microorganisms to partially replace chemical fertilizer use is increasing due to the requirement of sustainable agriculture development. Thus to investigate the possibility of a plant-beneficial Trichoderma strain and its bio-organic fertilizer product in saving chemical fertilizer application and in improving crop quality, a field trial and continuous pot experiments were carried out with tomato. Four treatments were set up: a reduced application of chemical fertilizer (75% of the conventional application) plus Trichoderma -enriched bio-organic fertilizer (BF), organic fertilizer (OF) or Trichoderma spore suspension (SS), with using the 100% rate of the conventional chemical fertilizer as the control (CF). The results showed that the total soluble sugar, Vitamin C and nitrate accumulations were, respectively, +up to 24%, +up to 57% and –up to 62% in the tomatoes of the BF treatment compared to those of the control (CF). And both of the pot and field trials revealed that reduced rates of chemical fertilizer plus bio-organic fertilizer produced tomato yields equivalent to those obtained using the 100% of the chemical fertilizer. However, application with the inoculant alone (SS) or combined with the organic fertilizer alone (OF) would lead to a yield decreases of 6–38% and 9–35% over the control. Since the increased abundance of soil microflora and the enhanced soil fertility frequently showed positive linear correlations especially in the BF-treated soils, we conclude that the efficacy of this bio-organic fertilizer for maintaining a stable tomato yield and improving tomato quality may be due to the improved soil microbial activity. Thus, the results suggest that the Trichoderma bio-organic fertilizer could be employed in combination with the appropriate rates of chemical fertilizers to get maximum benefits regarding yield, quality and fertilizer savings.

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Introduction.

Application of chemical fertilizers is one of the most adopted regimes in developing intensive agriculture nowdays 1 , 2 . However, the continuous long-term use of chemical fertilizer has led to many unexpected effects. For example, the productivity-cost does not scale linearly and results in a huge waste of mineral resources. In addition, millions of tons of synthetic nutrients that are loaded to soil yearly are not absorbed by plants. About up to 50% of N and 90% of P have been reported to run off from crop fields and escape into the atmosphere or water sources, thereby causing the generation of greenhouse gas, eutrophication in aquatic system and salinization in soil 2 , 3 . Besides, the excessive application of chemical fertilizer leads to food safety and quality decline problems, such as nitrate accumulation in vegetal products. Indeed, several studies have demonstrated that organic farming, which strictly prohibits synthetic fertilizers, provides an alternative that has the potential to minimize the negative influence from by using chemical fertilization, and the products from the organic farming systems are generally endowed with improved nutritional properties 4 , 5 , 6 , 7 . For example, the work of Caris-Veyrat et al . 4 reported that organic tomatoes had higher contents of carotenoids, polyphenols and Vitamin C than the ones from the conventional farming agriculture. However, organic farming is always associated with lower yield of crops and thus a higher cost. Therefore, the use of chemical fertilizers is not able to be eliminated once a considerable food production is expected 1 , 8 . Another current proposition for solving the agro-environmental problem is the integrated nutrient management that does not aim to entirely remove synthetic fertilizers in the near future instead suggests using microbial inoculations to reduce the amount of fertilizers applied 1 . Previous studies have shown that the inefficiency of synthetic fertilizers can be alleviated by applying plant growth-promoting microbes (PGPM), which are capable of increasing nutrient use efficiency and plant growth while reducing fertilizer inputs by up to 50% without causing any yield loss relative to the fully fertilized controls 2 , 9 , 10 .

PGPM exert considerable beneficial effects on the growth and development of plants. Many microbial genera have been commercially applied in agriculture 11 , 12 . For example, the plant-beneficial effect of Trichoderma harzianum has been widely studied and some of the strains are commercially applied to fields in China 12 , 13 . They have been previously shown with significant effects on plant growth, root development, biocontrol of soil-borne diseases and inducing plant systemic resistance 12 , 13 , 14 . To effectively apply such PGPM, it was suggested to enrich the strain in some organic substrate (e.g., as the form of bio-organic fertilizer) and then apply, since T . harzianum was reported to survive better in the rhizosphere after enriched in organic substrates 13 , 15 , 16 . For nearly all commercial uses of Trichoderma for biocontrol and plant growth and yield enhancement, a better understanding of the interactions among the Trichoderma , the fertilizer, the soil and the plant is essential. Although the number of research papers focused on reducing the inputs of fertilizer through different PGPM inoculations has increased in recent years, there are few reports concerning the combination of Trichoderma -enriched bio-organic fertilizer and reduced chemical fertilizer, especially in a long-term follow-up study, or concerning its potential effect on food quality 16 , 17 , 18 . Until recently, the focus has primarily been on the yield rather than the gustative or micro nutritional quality of fresh vegetal products. It could be acceptable for staple foods, but, as far as vegetables and fruits have been concerned, it can be argued the food quality matters more than the energy supply 4 . Tomato ( Solanum lycopersicum ), one of the most popular vegetables worldwide, is cultivated in over 140 countries 19 . It has many metabolites responsible for health and nutritional values, thus making it as an excellent model for studying fruit development and food safety 20 . However, in spite of the importance of vegetable quality to human health, there has been little improvement in the tomato fruit quality since producers preferentially select cultivars with traits of resistance to biotic and abiotic stress, extended shelf-life and appearance 19 . And the understanding of how fertilization regimes influence tomato quality stay poor.

Therefore, the aims of the present research were to investigate 1) if PGPM inoculants ( Trichoderma or Trichoderma bio-organic fertilizer) combined with reduced rates of chemical fertilizer would produce tomato yield and fruit quality equivalent to those obtained using full rates of chemical fertilizer, and 2) how the soil fertility responses to these fertilization regimes in a continuous cropping system. We therefore investigated the effectiveness of a Trichoderma bio-organic fertilizer on tomato yield and quality in an open field and evaluated the effect of Trichoderma inoculation on some chemical and biological properties of the soil related to plant growth via continuous 4-season pot experiments. Due to the importance of soluble sugars to a tomato’s organoleptic quality as well as that of Vitamin C (Vc) to nutrition and nitrate accumulation to safety, it is acceptable to use these three indexes to indicate the quality of a tomato fruit 7 , 19 , 21 , 22 . The introduction of a PGPM agent and fertilization could influence the soil’s microbial diversity and nutrient status and could subsequently change the soil quality; thus, the soil microbial population and the soil total and available nutrients were measured at the end of each growing season. In addition, strains with the potential of promoting plant growth and providing other benefits must be able to colonize roots 23 ; therefore, the number of Trichoderma in the rhizosphere soil was determined in this study.

Tomato yield

The results (Table  1 ) of both field trials and pot experiments indicated that the tomato yields from treatments with 75% chemical fertilizer plus bio-organic fertilizer (BF) were statistically equivalent to the yields obtained using full rate of chemical fertilizer (CF) without inoculants, while the yields obtained using 75% chemical fertilizer with Trichoderma spore suspension (SS) or organic fertilizer (OF) were less than those of the CF treatment in most cases significantly ( P  < 0.05) (Table  1 ). In contrast to the control (CF), the OF and SS treatments led to a decrease of 6–38% and 9–35%, respectively, in tomato yield in the pot experiments. The results were slightly different among the 4 pot experiments as the yields of the 4 treatments in the 1st season did not differ from each other. Because the data of the 1st field trial were more persuasive than those from the 2nd trial, here and similarly hereafter, only the data of the 1st field trial are shown.

Tomato quality parameters

The results in Fig.  1 showed that, in field trials, the fertilization treatments had significant ( P  < 0.05) effect on the total soluble sugars (TSS) content and NO 3 - accumulation in tomato fruit while had little effect on Vc content. Specifically, TSS content was approximately 40% higher in fruit from the BF or OF treatments than it was in fruit from the control (CF), whereas the NO 3 - content in fruit from the CF treatment was approximately 70% higher than that in fruit from the reduced chemical fertilization treatments (BF and OF). The results in Fig.  2 showed that different fertilization significantly affected the quality of the tomato fruit in the pot experiments. The variance in the Vc content observed in the tomato fruit in the 4 treatments was not obvious in the 1st and 3rd seasons, but it was evident in the 4th season: specifically, the Vc contents in the organic material added treatments (BF and OF) were 23–30% higher than the Vc contents in the synthetic fertilizer treatments (CF and SS) (Fig.  2a ). The chromatograms of Vc and NO 3 - analysis are illustrated with Figs.  S1 and S2 . The TSS contents in the four treatments gradually increased with continuous cropping, and the NO 3 - contents generally increased first and subsequently decreased; the TSS content in the 3 reduced chemical fertilizer treatments (BF, OF and SS) were much higher than with the full rate chemical fertilizer treatment (CF), while the trend was opposite in NO 3 - accumulation throughout the 4 cropping seasons (Fig.  2b,c ).

Effects of different treatments on tomato fruit quality in the open field. CF: 100% chemical fertilizer; BF: 75% chemical fertilizer + bio-organic fertilizer; OF: 75% chemical fertilizer + organic fertilizer. Error bars represent the standard deviation calculated from 5 replicates. Bars followed by the same letter are not significantly different at P  < 0.05.

Effects of different treatments on tomato fruit quality with cropping seasons in the greenhouse. CF: 100% chemical fertilizer; BF: 75% chemical fertilizer + bio-organic fertilizer; OF: 75% chemical fertilizer + organic fertilizer; SS: 75% chemical fertilizer + spore suspension. Error bars represent the standard deviation calculated from 5 replicates.

Soil nutrients content and organic matter

In general, the soil available nutrient contents at the end of the growing season reflect the soil nutrient supply. In the field trial, the available P and available K in the BF treatment were significantly higher than the contents in CF and OF treatments ( P  < 0.05) (Fig.  3 ). Conversely, no significant differences were observed in soil nitrate-N among the 3 treatments, and the ammonium-N in the CF treatment was markedly higher than the contents in the BF and OF treatments.

Effects of different treatments on soil available nutrients in the open field. CF: 100% chemical fertilizer; BF: 75% chemical fertilizer + bio-organic fertilizer; OF: 75% chemical fertilizer + organic fertilizer. Error bars represent the standard deviation calculated from 5 replicates. Bars followed by the same letter are not significantly different at P  < 0.05.

Figure  4 showed the fluctuations in available nutrients over time in the pot experiments. A similar trend of available P and available K was found in both the pot experiments and the field trials. The available P and available K in the organic material added treatments (BF and OF) were significantly higher than the contents in the synthetic fertilizer treatments (CF and SS), while the ammonium-N in the CF treatment was the highest among the 4 treatments throughout the 4 copping seasons (Fig.  4a,c,d ). The soil nitrate-N gradually grew with time, and its content in the BF and OF treatments remained at a higher level compared with that of the CF (Fig.  4b ). Higher levels of nitrate-N, available P and available K were more frequently observed in the BF treatment, whereas the lowest contents of available nutrients, including all of the above indexes, were mostly found in the SS treatment.

Effects of different treatments on soil available nutrients with cropping seasons in the greenhouse. ( a ) Soil ammonium-N; ( b ) Soil nitrate-N; ( c ) Soil available P; ( d ) Soil available K. CF: 100% chemical fertilizer; BF: 75% chemical fertilizer + bio-organic fertilizer; OF: 75% chemical fertilizer + organic fertilizer; SS: 75% chemical fertilizer + spore suspension. Error bars represent the standard deviation calculated from 3 replicates.

The data in Fig.  5 showed that bio-organic or organic fertilization (BF and OF) significantly enriched soil fertility, as the soil organic matter increased by 55–75%, total N by 25–36%, total P by 116–123% and total K by 99%–100% after the 4-season fertilization. Total P and total K also improved following the CF and SS treatments (Fig.  5c,d ), while the soil organic matter maintained a stable level, and the total N decreased with time in these 2 treatments (Fig.  5a,b ). Higher levels of total nutrients were always found in the OF treatment.

Effects of different treatments on soil total nutrients with cropping seasons in the greenhouse. ( a ) Soil organic matter; ( b ) Soil total N; ( c ) Soil total P; ( d ) Soil total K. CF: 100% chemical fertilizer; BF: 75% chemical fertilizer + bio-organic fertilizer; OF: 75% chemical fertilizer + organic fertilizer; SS: 75% chemical fertilizer + spore suspension. The standard deviation (n = 3) was analyzed using a one-way ANOVA.

Soil bacteria, fungi, actinomycetes and Trichoderma population

The colony forming unites (cfu) of culturable soil microbes including bacteria, fungi and actinomycetes and Trichoderma , were transformed into their logarithms, as shown in Fig.  6 . The total bacteria population of the pot soils in the BF, OF and SS treatments increased (to Log8.6, Log8.5 and Log8.2, respectively), while the number in the CF treatment decreased (to Log7.9) slightly (Fig.  6a ). The total fungi population generally first decreased, then increased and divided into 2 groups (one group including the BF and OF treatments decreased, and the other including the CF and SS treatments kept increasing) (Fig.  6b ). The total actinomycetes population for all of the treatments first showed a decrease and then an increase (Fig.  6c ). The Trichoderma population in the soil generally first increased and then decreased in the BF and SS treatments, whereas it remained at a low level in the CF and OF treatments, which were non-inoculated (Fig.  6d ). Additionally, the microbial population in the BF treatment always maintained the highest level among the 4 treatments, while the CF treatment was more frequently found to have the lowest microbial population.

Effects of different treatments on microbial abundance with cropping seasons in the greenhouse. ( a ) Total population of cultivable bacteria in pot soil; ( b ) Total population of cultivable fungi in pot soil; ( c ) Total population of cultivable actinomycetes in pot soil; ( d ) Total population of cultivable Trichoderma in pot soil. CF: 100% chemical fertilizer; BF: 75% chemical fertilizer + bio-organic fertilizer; OF: 75% chemical fertilizer + organic fertilizer; SS: 75% chemical fertilizer + spore suspension. Quantification of the total cultivable microorganisms in the soils was performed using the standard 10-fold dilution plating method via colony forming units (cfu) and expressed as its logarithm. The data fulfilled the prerequisites of one-way ANOVA.

Pearson correlations of soil nutrients and microbial abundance with tomato yield and quality

In total, 120 correlations among the soil nutrients, microflora, tomato yield and fruit quality properties were detected (Table  2 ). Of these correlations, 19 and 28 correlations had a significance level of 0.05 and 0.01, respectively. In particular, there was no correlation between the tomato fruit yield and the other parameters detected. The Vc content in the tomato fruit was found to have a positive correlation with soil organic matter but a negative correlation with NO 3 - accumulation in fruit. The TSS content in the fruit was positively correlated with all of the soil parameters detected in this work, with the exception of a negative correlation with the soil ammonium-N. The NO 3 - content in the fruit was negatively correlated with several soil parameters, including total N, organic matter and the bacteria population, and positively correlated with ammonium-N. The Trichoderma population in soil showed positive internal links with the soil fungi and actinomycetes populations, as well as a negative link with the soil ammonium-N. Furthermore, 2 major correlation groups with numerous internal links were observed. The first group consisted of strong positive links among the soil nutrient parameters themselves, especially the strong positive links between the organic matter and the other nutrient parameters. The second group included connections (some positive and some negative) among the soil nutrient parameters and the soil microflora.

The reduced load of fertilizers into crop fields without causing productivity lost is a feasible but difficult challenge 2 . The results of the field trials confirmed our hypothesis that the combination of Trichoderma -enriched bio-organic fertilizer with reduced (75%) chemical fertilizers (BF) could produce tomato yield equivalent to or higher than those obtained using full rates of the fertilizer (CF) (Table  1 ). This result was consistent with repeated observations in pot experiments. However, inoculation with the Trichoderma alone (SS, without organic substrate supply) or supplement with organic fertilizer alone (OF, without Trichoderma ) would cause 6–38% and 9–35% decreases in yield over the control (CF) in the presence of 100% chemical fertilizer doses. Hence, only bio-organic fertilizer could be a viable supplementary strategy to maintain or increase tomato yields. Similar results regarding PGPM application was also reported by Adesemoye et al . 11 that the growth and yield of tomato grown in a greenhouse with 75% fertilizer plus PGPM were statistically equivalent to those obtained using full fertilizer rates without PGPM. Moreover, some reports showed that bio-organic fertilizers could replace 23–52% of N fertilizer without any loss of yield 24 , which also indicating the potential role of bio-organic fertilizer in reducing the amount of chemical fertilizer load to soil. Whereas, few previously reported evidences regarding the influence of PGPM or its bio-fertilizer application on crop quality could be found 8 , 11 . The effects of the same treatment on the measured yield differed greatly throughout the four growing seasons may due to the variations of climatic conditions.

In this study, at reduced fertilizer rates (75%), inoculants consistently enhanced tomato fruit quality (Figs.  1 and 2 ). In particular, NO 3 - accumulation in fruit, which is associated with risks of several human health problems such as methemoglobinemia and gastric cancer 22 , from the reduced chemical fertilization (BF, OF and SS) was coupled with a lower (down to 62%) content compared with the full-rate fertilized control (CF) in the greenhouse. Actually, NO 3 - is relatively non-toxic, but its metabolite products, especially NO 2 -, raised concern in human health 25 . As 85–90% of an adult dietary intake of NO 3 - is from vegetables, while the vegetables tend to concentrate NO 3 - when grown in a N highly applied field 22 , 26 . Therefore, a proper control of the application rate of chemical fertilizers to soil would directly reduce our risks to some nitrate-related health problems. Moreover, the Vc and TSS contents in the tomato fruit in the treatments with added organic material (BF and OF) were significantly higher (up to 24% and 57%, respectively) than that of the control (CF). As suggested by Oliveira1 et al . 7 , organic farming creates stressing conditions for tomatoes and thus resulted in the higher accumulation of soluble solids in fruits such as sugars and other compounds that contribute to the nutritional quality of fruit, including Vc and phenolic compounds. The differences observed in tomato yield and quality for different treatments may originate from the differences in nitrogen availability because the organic fertilizers (including bio-organic fertilizer and organic fertilizer) release N (more obviously as ammonium-N in this study; Figs.  3 and 4 ) much more slowly than do chemical fertilizers, thus forcing the plants to struggle more for growth and resulting in a more complex diversion of protein synthesis and secondary metabolisms 4 , 27 .

Concerning the other elements, more available P and available K were found in the BF- and OF-treated soils at the end of each growing season. T . harzianum has been reported to be able to solubilize several plant nutrients 28 , and T . asperellum has been shown to enhance the P and Fe availability for cucumber once colonized on roots 29 . However, the enhancement of available K in the BF treatment in this study did not occur via K dissolution because T7 has shown no direct K dissolution ability in vitro under laboratory conditions (data not shown). Hence, the resulted enhancement of K availability must be due to alternative microbial effects. As shown in Fig.  6 , the treatment with reduced chemical fertilization plus Trichoderma bio-organic fertilizer (BF) resulted in a greater increase of the population of bacteria, fungi and actinomycetes relative to the other treatments. Thus, the BF treatment was a more efficient tool to enhance the abundance of soil microflora, which had a potential effect on soil nutrient cycling. Based on the explanations by Adesemoye et al . 11 and Huang et al . 30 , T . harzianum promotes plant root growth via the secretion of an auxin-like phytohormone. Better root growth impacts soil microbiome via secreting more exudates, like sugars and organic acids, and soil microbes, in turn, response with higher microbial abundance and frequent interactions leading to more available nutrients that affect plant growth and health. Gradually, better plant growth caused by more bio-available nutrients again stimulates more microbes moving towards the rhizosphere resulting in higher nutrient uptake by the inoculated plants. This process can be illustrated using Pearson correlations, which showed a sharp correlation of these two traits (soil nutrients and soil microflora), as in Table  2 .

In addition, strong positive links between soil organic matter and the other soil nutrient parameters (e.g., total N, P and K contents) were observed in this continuous cropping system. The changes in soil organic matter based on the application of mature compost are important. It was suggested that the application of composts to soils in agriculture could provide long-term fertility and less off-site impacts 31 . However, the nutrient supply capability of the OF treatment was efficient as compared to that of the BF. Therefore, the combination of functional PGPM (i.e., T7) and organic fertilizer as the form of bio-organic fertilizer was the better choice to reduce the use of chemical fertilizers and promote tomato yield and quality. After fermentation in compost, T7 utilized the nutrients provided by the organic material and established themselves in it, which increased the viability of the added T7 and made these strains more competitive in the microbial community in rhizosphere 5 . This may also be the reason why the BF treatment was more effective in maintaining tomato yield compared with T7 alone (SS).

In conclusion, the results of the present work imply that the application of this Trichoderma -enriched bio-organic fertilizer rather than applying the PGPM inoculant alone could help to avoid the overuse of expensive chemical fertilizers to a significant extent without compromising the yield (at least in tomatoes). More importantly, the use of Trichoderma -enriched bio-organic fertilizer with lower fertilizer application leads to the enhancement of fruit quality and the improvement of soil fertility and microbial environment. There, bio-organic fertilizers like this could be employed to supplement to the reduced rate of chemical fertilizers, and should be further evaluated as an important component of the integrated nutrient management regime.

Materials and Methods

Microbial strain.

T . harzianum strain T7 was maintained in our lab which was originally isolated from soil. It was cultured on potato dextrose agar (PDA) at 28 °C and stored at 4 °C on slants. The strain purity was confirmed by PCR and sequencing to exclude the contamination from bacteria and other fungi before use.

Bio-organic fertilizer preparation

Spore suspensions of T7 were prepared by flooding PDA cultures of 7-day-old T7 with sterile water; the suspensions were then filtered through a double layer of sterile cheesecloth and adjusted to 10 6 conidiospores per mL based on the hemocytometer counts. The bio-organic fertilizer used in this study was obtained by aerobically fermenting a mixed organic fertilizer with T7 spore suspension (100:1, w/v) for 7 days at < 50 °C. The mixed organic fertilizer was prepared from mature compost of pig manure, which contained 42.5% organic matter, 3.5% N, 2.1% P 2 O 5 , 1.2% K 2 O and 28.4% H 2 O. The final bio-organic fertilizer was stored at 4 °C and was used in the experiments only if the population of the T7 remained at the level of 10 6 cfu per gram of dry matter.

Field trials design

Field trials were conducted twice at a vegetable testing site in army horse ranch 6 team (located at longitude 106°27’ E and latitude 38°47’ N), Yinchuan, Ningxia Province, China. No specific permits were required for the described field studies. The location is not privately owned or protected, and the field studies did not involve endangered or protected species. The soil characteristics were pH 6.1, organic matter 27.6 g kg −1 , ammonium-N 21.9 mg kg −1 , nitrate-N 22.7 mg kg −1 , available P 131.3 mg kg −1 and available K 218.7 mg kg −1 . The above data were collected by measuring five soil samples from the field site before planting. The first crop season extended from August to November; the second crop season lasted from March to June. The field treatments were designed as (1) CF: 100% chemical fertilizer; (2) BF: 75% chemical fertilizer + bio-organic fertilizer; and (3) OF: 75% chemical fertilizer + organic fertilizer. The 100% chemical fertilizer contained 600 kg ha −1 YaraMila compound fertilizer (N: P: K = 15: 15: 15) and 300 kg ha −1 YaraLiva-Ca(NO 3 ) 2 fertilizer (N ≥ 15%, split into 3 × 100 kg, YARA international ASA, Oslo, Norway) and was applied in plots consistent with the local farmers’ fertilization practice. The 75% chemical fertilizer used in this study was based on the 100% fertilizer because a 75% rate was reported to be a threshold below which the PGPM-fertilizer interaction could not produce consistent nutrient uptake comparable to the non-inoculated full fertilizer rates 1 , 11 . The application rate of bio-organic fertilizer or organic fertilizer was 1800 kg ha −1 . Each treatment with 5 plots was randomly arranged in the selected fields, and each plot (6.0 m × 1.6 m) contained 60 tomato seedlings. Conventional practices like watering (every ten days), scarifying and disinsection were equally given when needed.

Pot experiments design

To investigate the effect of T. harzianum T7 inoculation alone (without organic substance) on tomato growth, yield and fruit quality and on the soil environment, another treatment (SS: 75% chemical fertilizer + spore suspension) was added to the pot experiments, and further experiments were conducted using the same treatments applied in the field trials. At planting, seedlings with CF treatment (100% chemical fertilizer) received 5.33 g plant −1 YaraMila compound fertilizer. They were then fertigated with 2.67 g plant −1 YaraLiva-Ca(NO 3 ) 2 between four and five weeks after planting. The reduced fertilization treatments (BF, OF and SS) received 75% of the chemical fertilizer and 50 g plant −1 bio-organic fertilizer, 50 g plant −1 organic fertilizer or 5 mL plant −1 Trichoderma spore suspension (10 6 cfu mL −1 ). Each pot (30 × 30 × 35 cm 3 ) contained 10 kg soil and 2 seedlings. The soil used in this work was a loam (pH 7.3) with an organic matter content of 19.2 g kg −1 . The available P and K, ammonium-N and nitrate-N contents were 99.2, 150.5, 29.3 and 0.8 mg kg −1 , respectively. Six pots were used for each treatment, and they were arranged randomly in the greenhouse, with a maintained temperature of 20–30 °C. The pot experiments were continuously carried out for four times with repeated fertilization and planting.

Estimation of tomato yield and fruit quality parameters

Destructive harvest was conducted on the 100th day after planting in both field trials and pot experiments, and data regarding the tomato yields were collected. Ripe fruits were harvested 3 times manually from 60 plants for each plot in the field trials (10 plants for pot experiments), and 3 of the fruits were selected to form a replicate for each treatment.

The contents of Vc and nitrate (expressed in NO 3 -) in the tomato fruit were analyzed with an Agilent 1200 semi-preparative HPLC (Agilent Technologies, Santa Clara, Cal., USA). For the Vc content, 5 g of fruit samples were homogenized in 50 mL of ice-cold extraction buffer (5 g L −1 oxalic acid) for 15 min and then transferred to a 100 mL volumetric flask diluted with the extraction buffer. The homogenate was filtered through a 0.45 μm filter membrane. All of the procedures were performed at 4 °C. The mobile phase was composed of 0.05 M KH 2 PO 4 solution and methanol at a ratio of 95:5 (v/v) and used at a flow rate of 1.0 mL min −1 ; the eluate was detected at 265 nm at room temperature. The standard curve of Vc was developed with ascorbic acid (Sigma, USA) from 5 mg L −1 to 100 mg L −1 . To evaluate the nitrate content in the tomato fruit, 50 g of fresh fruit was homogenized in 50 mL of deionized water. Five grams of the homogenate was added to 50 mL of hot water (70–80 °C) and used for ultrasonication for 20 min. After cooling, 5 mL of the above extract was diluted to 25 mL with deionized water and filtered through a 0.45 μm filter membrane. The eluent was 0.03 M KH 2 PO 4 -H 3 PO 4 buffer (pH = 3.3) at a 1 mL min −1 flow at room temperature at 210 nm. Standard control was set up from 0.1 mg L −1 to 10 mg L −1 with KNO 3 . The TSS content was measured using an anthrone colorimetric method at 620 nm as described by Allen 32 .

Soil sampling and nutrient content analysis

A composite soil sample (with three replicates) was collected from the pot soil which was mixed thoroughly manually before splitting into pots and was referred to as the 0th soil sample. At every harvest, soil samples were collected from the harvested plant roots of each treatment as described by Hervás et al . 33 and referred to as the 1st, 2nd, 3rd and 4th soil samples. The tomato plants were carefully removed from the pots and gently shaken to detach the soil. Soils still adhering to the roots were defined as the rhizosphere soil samples. The soil samples for the field trials were prepared at harvest as described above for the pot experiment sampling.

The total N content and organic matter of soil samples were analyzed using a Vario EL elemental analyzer (Elementar Analysensysteme GmbH, Hanau, Germany). The total P and total K were analyzed using inductively coupled plasma-atomic emission spectrometer (Agilent 710 ICP-OES, Agilent Technologies, Santa Clara, Cal., USA). The soil available nutrients, including soil available P and available K, were determined following Shen et al . 34 , and the soil available N (ammonium-N and nitrate-N) was analyzed using a continuous-flow analyzer (AutoAnalyzer 3, Bran + Luebbe GmbH, Germany).

Soil cultivable microbial count

The populations of soil cultivable bacteria, fungi, actinomycetes and Trichoderma were detected using the standard 10-fold dilution plating method. Specifically, Beef extract medium was used for the characterization of total bacteria population, Martin medium for fungi, Gause NO.1 medium for actinomycetes 35 and a modified Trichoderma selective medium [1 L contained water, 800 mL; agar, 20 g; glucose, 3 g; NH 4 NO 3 , 1 g; KH 2 PO 4 , 0.9 g; MgSO 4 ·7H 2 O 0.2 g; KCl, 0.15 g; rose Bengal, 0.15 g; chloramphenicol, 0.25 g; streptomycin, 0.05 g; quintozene (PCNB), 0.15 g; Captan, 0.1 g; propamocarb (772 g of active ingredient per liter), 1.2 mL; and Triton X-100, 1 mL] based on TSM medium 36 for Trichoderma population. The data were expressed as the number of cfu per gram dry soil.

Statistical analysis

The results were expressed as the means ± standard deviations and were calculated and statistically examined using an analysis of variance and a Duncan’s multiple range test. Statistical significance was considered at P  < 0.05, unless otherwise stated. Most tests were conducted using SPSS version 13.0 (SPSS, Inc., Chicago, IL, USA). The Pearson correlation coefficient of pairwise correlation analysis was performed using SPSS to relate the tomato yield, quality and soil chemical and biological properties.

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Acknowledgements

This research was funded by the key research and development projects of Ningxia Hui Autonomous Region (Grant No. 2018BBF02009 and 2018BBF03001), Ningxia University first-class discipline construction project (Grant No. NXYLXK2017B03), and the Natural Science Foundation of China (Grant No. 31801903). We are grateful to the Institutes of Ningxia protected horticulture engineering technology research center and Ningxia protected horticulture (Ningxia University) technology innovation center for supporting.

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L.Y. and J.L. conceived the study. L.Y. designed the experiments. L.Y. and X.Z. conducted the experiments and the data analysis. K.C., E.B. and Z.Z. wrote and revised the manuscript. All authors read and approved the final manuscript.

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Ye, L., Zhao, X., Bao, E. et al. Bio-organic fertilizer with reduced rates of chemical fertilization improves soil fertility and enhances tomato yield and quality. Sci Rep 10 , 177 (2020). https://doi.org/10.1038/s41598-019-56954-2

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Definition of the Subject

Fertilizers are compounds or mixtures delivered as solids, liquids or gases, that supply essential nutrients to crops in soluble forms that are convenient and safe to handle. Fertilizers may be applied to the soil or directly to foliage. All nutrients except N are manufactured by concentrating and refining ores extracted from mines. N fertilizers are manufactured from ammonia, which is synthesized from N 2 and H 2 . Science contributes to fertilizer use with improved products and methods to increase fertilizer efficiency, profitability of nutrient used, and reducing adverse environmental effects. Technology contributes to fertilizer use by improving the efficiency of manufacture and the complex logistics of delivering hundreds of million tons of products to farms safely, economically, and on time. Fertilizers can be both inorganic and organic, but this contribution refers mostly to inorganic or manufactured...

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Abbreviations

There are 16 mineral elements that are essential for plant growth. They are referred to here by their symbols: nitrogen, N; phosphorus, P; potassium, K; calcium, Ca; magnesium, Mg; sulfur, S; boron, B; iron, Fe; manganese, Mn; copper, Cu; zinc, Zn; molybdenum, Mo; sodium, Na; chlorine, Cl; silicon, Si; nickel, Ni.

This refers to the additional grain or other agricultural product produced per unit of additional nutrient applied in fertilizer. A related concept is Fertilizer Recovery, which is the additional mass of a nutrient in the aboveground parts of a crop expressed as a proportion of the additional nutrient applied in fertilizer.

N, P, and K.

Cl, Fe, Mn, B, Zn, Cu, Mo, and Ni.

These include mineralization, which is oxidation of organic matter and the release of mineral nutrients; immobilization, which is the reverse process of incorporating mineral nutrients into organic matter; and nitrification, which is conversion of ammonium to nitrate.

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Marschner H (1995) Mineral nutrition of higher plants. Academic, London

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Acknowledgments

Tony Good provided insights into fertilizer technology and John Passioura and Mark Peoples made helpful suggestions about the article.

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Dr. J. F. Angus

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Angus, J.F. (2012). Fertilizer Science and Technology . In: Meyers, R.A. (eds) Encyclopedia of Sustainability Science and Technology. Springer, New York, NY. https://doi.org/10.1007/978-1-4419-0851-3_193

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The effects of bio-fertilizer by arbuscular mycorrhizal fungi and phosphate solubilizing bacteria on the growth and productivity of barley under deficit of water irrigation conditions.

1. Introduction

2. materials and methods, 2.1. experimental design, 2.2. studied traits and recorded data, 2.3. statistical analysis, 3.1. the effects of bio-fertilizers, drought, and phosphorus fertilizers on yield, yield components.

3.2. The Effects of Bio-Fertilizers, Drought, and Phosphorus Fertilizers on Nutrients Uptake in Grain and Straw of Barley

3.3. The Interactions Effects between the Bio-Fertilizers, and Phosphorus Fertilizers Rates on Yield, Yield Components of Barley

Click here to enlarge figure

3.4. The Interactions Effects between the Bio-Fertilizers, and Phosphorus Fertilizers Rates on Nutrients Uptake in Grain and Straw of Barley

3.5. the interactions effects between the bio-fertilizers, and irrigation intervals on yield, yield components of barley, 3.6. the interactions effects between the bio-fertilizers, irrigation and drought conditions on nutrients uptake in grain and straw of barley, 3.7. the interactions effects between irrigation intervals and the ratios of the recommended dose of phosphorus fertilizers (rdp) on yield, yield components and nutrients uptake in grain and straw of barley, 4. discussion, 5. conclusions, supplementary materials, author contributions, data availability statement, acknowledgments, conflicts of interest.

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Share and Cite

Alotaibi, M.M.; Aljuaid, A.; Alharbi, M.M.; Qumsani, A.T.; Alzuaibr, F.M.; Alsubeie, M.S.; Ismail, K.A.; Gharib, H.S.; Awad-Allah, M.M.A. The Effects of Bio-Fertilizer by Arbuscular Mycorrhizal Fungi and Phosphate Solubilizing Bacteria on the Growth and Productivity of Barley under Deficit of Water Irrigation Conditions. Agronomy 2024 , 14 , 1973. https://doi.org/10.3390/agronomy14091973

Alotaibi MM, Aljuaid A, Alharbi MM, Qumsani AT, Alzuaibr FM, Alsubeie MS, Ismail KA, Gharib HS, Awad-Allah MMA. The Effects of Bio-Fertilizer by Arbuscular Mycorrhizal Fungi and Phosphate Solubilizing Bacteria on the Growth and Productivity of Barley under Deficit of Water Irrigation Conditions. Agronomy . 2024; 14(9):1973. https://doi.org/10.3390/agronomy14091973

Alotaibi, Mashael M., Alya Aljuaid, Maha Mohammed Alharbi, Alaa T. Qumsani, Fahad Mohammed Alzuaibr, Moodi S. Alsubeie, Khadiga Ahmed Ismail, Hany S. Gharib, and Mamdouh M. A. Awad-Allah. 2024. "The Effects of Bio-Fertilizer by Arbuscular Mycorrhizal Fungi and Phosphate Solubilizing Bacteria on the Growth and Productivity of Barley under Deficit of Water Irrigation Conditions" Agronomy 14, no. 9: 1973. https://doi.org/10.3390/agronomy14091973

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• v.8(12); 2022 Dec

Liquid biofertilizers as a sustainable solution for agriculture

Mintallah mousa a. allouzi.

a Department of Chemical and Environmental Engineering, Faculty of Science and Engineering, University of Nottingham, Broga Road, 43500 Selangor, Malaysia

Safa Mousa A. Allouzi

b Department of Medicine, Faculty of Medicine, Bioscience, and Nursing, MAHSA University, Jalan SP 2, Bandar Saujana Putra, 42610 Jenjarom, Selangor, Malaysia

Zi Xiang Keng

Christina vimala supramaniam.

c School of Biosciences, Faculty of Science and Engineering, University of Nottingham, Broga Road, 43500 Selangor, Malaysia

Siewhui Chong

Associated data.

Data will be made available on request.

This paper provides a mini review of liquid biofertilizers, which have been proven to perform better than the other forms in lasting for longer periods of time, improving crop quality, and requiring less amounts for application. The production of liquid biofertilizers, types of liquid inoculants, and their effect on plant growth are covered in this review. Liquid biofertilizers can be made from wastes and by-products of several industries, making zero or near-zero discharge possible and thus gearing towards circular economy. Despite their usefulness in enhancing crop quality and eco-friendliness, in order to compete with chemical fertilizers, there are a number of challenges to overcome, such as extending the shelf life, making them more susceptible to seasonal climate conditions and soil types, and development of suitable machineries for production and application. More field trials, cost-benefit analysis and long-term studies should also be evaluated for commercialization purposes.

• • This paper presents state-of-the-art review of liquid biofertilizers.
• • Liquid biofertilizers were compared and their production processes were outlined.
• • Sources of liquid inoculants were reviewed with plant growth analysis compared.
• • Shelf life, machinery and susceptibility to climate and soil hinder its widespread.
• • More field trials, cost analysis, and multistakeholder partnerships are essential.

Biofertilizer; Green fertilizer; Liquid fertilizer; Plant growth; Soil enhancement.

1. Introduction

The current increase in the world population to 7.8 billion has placed an increasing demand on agricultural crops, thus posing great challenges in terms of how to feed such a large population ( Worldometers, 2021 ). According to the United Nations Food and Agriculture Organization’s estimates, the demand on agricultural crops will increase to 60% by the year 2030 ( Bruinsma, 2002 ). To reach self-sufficiency, chemical fertilizers have been widely used by countries to increase crop yield. However, these chemical fertilizers are causing serious environmental pollution by reducing water-holding capacity in the soil and thus its fertility, increasing soil acidity, and reducing the number of microorganisms, resulting in nutritional imbalances in the soil ( Nosheen et al., 2021 ). In addition, these hazardous substances are not taken up by plants, but accumulate in ground water affecting the soil negatively. Therefore, it is vital to shift the focus to the production of safe and environmentally friendly methods for sustainable crop production.

Beneficial microorganisms present in the soil are often utilized for sustainable crop production as they have long lasting effects on the soil fertility ( Mitter et al., 2021 ; Umesha et al., 2018 ). Knowledge of the use of microorganisms to increase soil fertility began as early as 1901, when the American chemist, Harvey W. Wiley, delivered a speech to the Franklin Institute in which he spoke about the possibility of using microorganisms ( Rhizobium sp.) to enhance soil fertility. Discovering that organisms capture nitrogen laid the groundwork for further developments in scientific research related to agriculture. He described “Alinite and Nitragin”, a commercial product for fixing nitrogen in the soil, but these products needed more development by multiplication of the organisms in favorable environments ( Knight, 1878 ).

Biofertilizers consist of single or multiple strains of microbes like algae, bacteria, and fungi that enhance the plant growth through colonization of the rhizosphere and the interior of the plant, and through enhanced nutrient availability that can be added to the seeds, plant surface, or the soil ( Nosheen et al., 2021 ; Riaz et al., 2020 ). Biofertilizers are not only responsible for enhancing soil physiochemical properties, but also affecting the structure and function of microorganisms via changes in the microbial carbon, microbial diversity, and the community level physiological profiling ( Aponte et al., 2022 ; Javoreková et al., 2015 ). Even so, not all native soil microbes interact the same with biofertilizers, since the addition of plant growth promoting rhizobacteria (PGPR) in the rhizosphere may enhance certain microbial groups or inhibit them, and in some cases PGPR does not affect the native microbial population at all ( Mącik et al., 2020 ).

Consumer awareness about the hazards of chemical fertilizers, soil deterioration, and nitrate emissions, as well as government measures, are increasing with years. Hence, the market for biofertilizers is expected to increase from 2.3 billion USD in 2020 to 3.9 billion in 2025 ( Mehra, 2020 ). Biofertilizers are known for their ability to provide plants with nutrients such as nitrogen, phosphate, zinc, phosphorus and also help in promoting plant growth ( Szilagyi-Zecchin et al., 2016 ). Since carrier based biofertilizers have a short shelf life, low cell count, and difficulties in storage and handling, liquid biofertilizers which a have a high cell count of more than 10 9 were developed to overcome these problems ( Nagarajan, 2021 ).

Production of low cost, effective biofertilizers involves multiple phases, starting from choosing the suitable carrier, isolation and screening of microbes to find the most potent one, to undergoing several tests, before scaling it up from flask-stage to commercial stage ( Stamenković et al., 2018 ; Vassileva et al., 2021 ). It is also important to find cheaper raw materials that are high in nutrients, carbon, and nitrogen source and use it as a substrate or possible liquid media to culture microorganisms. Some industries are required to pay to get rid of their waste or have a difficult time in treating their wastes. Thus, these wastes and byproducts can be used as possible substrates to develop a sustainable, eco-friendly biofertilizer ( He et al., 2020 ; Namfon et al., 2017 ). Moreover, biofertilizers can be tailored to provide plants with nitrogen, phosphate, zinc, or other nutrients in different soil types using certain types of bacteria compared to using none or chemical fertilizers ( He et al., 2019 ).

In the light of these features, this review first compares biofertilizers with chemical and organic fertilizers, then evaluates the production processes and compares the liquid inoculants and their impacts on plant growth. The development of liquid biofertilizers is discussed based on how it is developed from different substrates, or by-products and wastes of some industries. Finally, the challenges and recommendations for future studies are discussed to improve the production and development of liquid biofertilizer, benefiting its expansion and commercialization for the agricultural industries.

2. Biofertilizers

2.1. biofertilizers in general.

Biofertilizers are one of the most promising ways to increase crop production while staying environmentally friendly ( Kour et al., 2020 ). Unlike organic fertilizers which consist of animal manure, compost, slurry waste, peat, bones, and blood meal ( Hazra, 2016 ; Raimi et al., 2017 ), biofertilizers contain one or more living microorganisms (i.e., bacteria, fungi, algae) alone or in combination that settle down in the rhizosphere and enhance soil productivity by fixing down atmospheric nitrogen and solubilizing different nutrients, thereby exerting direct or indirect beneficial effects on crop growth and yield through different mechanisms ( El-Ramady et al., 2018 ; Mącik et al., 2020 ). In organic fertilizers, some organisms like earthworms need to convert the fertilizer into useful material which plants can absorb easily. Plant-growth promoting rhizobacteria is the most used bacteria in producing biofertilizers since it enhances plant growth by releasing potassium (K), fixing nitrogen (N), solving phosphorus (P), and producing hormones ( Lu et al., 2020 ). Biofertilizers come in solid, liquid, polymer entrapped formulations, and fluidized bed dry formulations ( Mącik et al., 2020 ). Table 1 shows the differences between biofertilizers, chemical, and organic fertilizers with the pros and cons analyzed.

Table 1

Comparison between biofertilizers, chemical and organic fertilizers.

Plants need 14 essential mineral elements to grow and develop, which are macronutrients – N, P, K, Ca, Mg and S, and micronutrients – Fe, B, Cl, Mn, Zn, Cu, Mo, and Ni ( de Bang et al., 2021 ; Romera et al., 2021 ). Although most of the elements are found in soil, they cannot be taken up by the plants because they are in forms that plants cannot assimilate. Some of these elements are absorbed by plants only in certain forms like nitrogen that is absorbed as either nitrate or ammonia. As shown in Figure 1 , using microorganisms will promote plant growth and provide plants with nutrients ( Stamenković et al., 2018 ). Biofertilizers are classified based on the groups of microorganisms they contain and the functional features they have developed during the interactions with plants in the rhizosphere ( Mącik et al., 2020 ; Raimi et al., 2017 ). Table 2 shows the general classification of biofertilizers – N-fixing, P-solubilizing, P-mobilizing, micronutrient solubilizer and plant-growth promoting rhizobacteria.

Key microbially-mediated nutrient transformation/acquisition pathways associated with biofertilizers. Full arrows represent microbial transformations whereas dashed arrows represent mobilization/movement of nutrients ( Mitter et al., 2021 ).

Table 2

Grouping of biofertilizers with functions ( Umesha et al., 2018 ).

2.2. Liquid biofertilizers

Liquid biofertilizers are used as an alternative to carrier-based formulations ( Mącik et al., 2020 ; Nagarajan, 2021 ). They are also called flowable or aqueous suspension. They are based on broth culture, mineral and organic oil, oil in water, and polymer based suspension ( Bharti et al., 2017 ). Liquid biofertilizers typically consist of 10–40% microbes, 1–3% suspender ingredient, 1–5% dispersant, 3–8% surfactant, and 35–65% carrier liquid (water or oil) ( Mishra and Arora, 2016 ). Liquid biofertilizers should contain special cell protectants that contribute to the development of cysts and dormant spores ( Raimi et al., 2021 ).

Liquid biofertilizers are more attractive than solid inoculants because they have a long shelf life of 1.5–2 years, have no contamination, do not need sticky materials, can be used with modern machinery, can withstand high temperatures up to 45 °C, are easy to handle and use, are easy for adding ingredients that enhance the growth of microbial strains, and are easy to apply on both seeds and soil ( Mahanty et al., 2017 ). Also, liquid inoculants have higher microbial densities that allow for lower dosages compared to solid-inoculants yet obtain the same effect ( El-Ramady et al., 2018 ; Mącik et al., 2020 ).

The carrier material for liquid biofertilizers should be cheap, abundantly available, non-toxic, and easy to use. The carrier also must have a suitable pH, high water holding capacity, and physical and chemical homogeneity to enhance microbial growth ( Raimi et al., 2021 ). Although liquid biofertilizers can be stored for a long time, microorganisms may face nutrient depletion, hypoxia, and environmental stresses which cause the microbial population to dramatically decrease. Therefore, special storing conditions are needed such as cool temperatures ( Lee et al., 2016 ; Mącik et al., 2020 ).

Microbes in broth culture do not survive for a long time and lose their effectiveness on seeds ( Mahanty et al., 2017 ). Hence, to let microbes survive for a longer time in liquid formulations, some additives are added such as sucrose, Arabic gum, glycerol, and polyvinylpyrrolidone, due to their ability to inactivate toxic compounds, improve adhesion to seeds, and improve microbial strains survival under different environmental conditions ( Mącik et al., 2020 ). Liquid biofertilizers can reduce the use of chemical fertilizers by 15–40%. In addition, their dosages are less than solid biofertilizer by 10%, thus less amount is needed, allowing for smaller storage spaces ( Riaz et al., 2020 ).

There are four types of liquid biofertilizers: suspension concentrates, ultralow volume suspension, oil-miscible flowable concentrate, and oil dispersion. Suspension concentrates are favored by farmers more than wettable powders because they are not dusty, easier to measure, and can be poured in spray tanks. Suspension concentrates are made by combining solid active ingredients with low water solubility and acceptable hydrolysis stability. Before using, suspension concentrates must be diluted in water. Using surfactants and other chemicals can increase their storage and solubility. Ultralow volume suspension is a ready-to-use formulation that can be dispersed by ultralow volume aerial or ground spray machinery in a very fine spray. Oil miscible flow concentrate is a dispersion of active ingredients in an organic liquid. It must be diluted before use ( Mishra and Arora, 2016 ). Oil dispersion contains active ingredients in oil or in water immiscible solvent ( Mącik et al., 2020 ). Oil is known to evaporate much less than water, so it stays in contact with plants for a longer time. It can be applied as an emulsion or an inverted emulsion (water in oil) ( Mishra and Arora, 2016 ). Table 3 shows some of the companies that produce liquid biofertilizers in Jordan, India, Sri Lanka, and the United States.

Table 3

Companies providing liquid biofertilizers in Jordan, India, Sri Lanka and the United States.

2.3. Mechanism of biofertilizers

Plant growth-promoting rhizobacteria stimulate plant growth through a variety of methods. They are frequently divided into direct and indirect methods. The bacteria may either directly increase plant growth by altering hormone levels or resource acquisition, or indirectly increase plant growth by reducing the impact of numerous pathogenic agents on plant growth and development ( Daniel et al., 2022 ).

2.3.1. Direct mechanism

Nitrogen becomes available to plants by the energy intensive process of biological nitrogen fixation (BNF) due to the fact that most of it is available in the atmosphere. Diazotrophs which consist of bacteria and archaea use the large stock of N 2 from the soil to biologically fix nitrogen. Atmospheric N 2 is catalyzed and reduced into ammonium (NH 4 + ) by the nifH gene that encodes the highly conserved iron-protein subunit of the nitrogenase enzyme which consists of dinitrogenase reductase that has Fe as its co factor and dinitrogenase with Fe and Mo as its co factor as well as it being controlled by diazotrophs ( Carpanez et al., 2022 ).

These microorganisms are divided into two groups symbiotic, and non-symbiotic. The symbiotic family consist of Rhizobiaceae and Cyanobacterium anabaena with azolla fern water where it has been used for more than 1000 years as a biofertilizer (Azolla- Anabaena symbiosis). The non-symbiotic family consists of Azospirillum sp. and Cyanobacteria sp. ( Daniel et al., 2022 ; Mahmud et al., 2021 ). Phosphate is the second most important element for plant growth and development after nitrogen, except that it is not available to plants since it is in an insoluble form and only 0.1% is available to plants. Microorganisms help solubilize insoluble P like dicalcium phosphate, tricalcium phosphate, hydroxyapatite, and rock phosphate by acids and other mechanisms that reduce the soil’s pH into soluble forms of monobasic and dibasic which increase plants yield. Sometimes these bacteria mobilize the phosphorus ( Mahanty et al., 2017 ; Riaz et al., 2020 ). Phosphate solubilizing bacteria efficiency depends on soil buffering capacity and its carbon and nitrogen sources ( Raimi et al., 2017 ).

Potassium is also important for plant growth. Organic acids such as citric acid, formic acid, malic acid, and oxalic acid are produced by the dissolution of organic matter in soil. By providing protons and complexing Ca + ions, these organic acids aid in the breakdown of K compounds. There are two main mechanisms in which Zn becomes available in soil. Those two mechanisms are dependent on pH. The first way is in acidic soils where Zn becomes available by cation exchange. The second mechanism is by forming zinc calcium carbonate by chemisorption ( Mącik et al., 2020 ). With each unit increase in pH, Zn availability decreases by 100 times ( Zeb et al., 2018 ). In an aerobic setting, iron is present as Fe 3+ . Because of this, microbes and plants are unable to absorb the majority of the iron. Typically, bacteria secrete siderophores, which are low-molecular-weight iron chelators with a strong affinity for complex iron, to get iron. Siderophores act as solubilizing agents for iron from minerals and organic molecules when there is a deficiency of iron. Several methods, such as chelation and release, direct uptake of siderophore Fe complexes, and ligand exchange events, are used by plants to absorb iron from bacterial siderophores ( Daniel et al., 2022 ). Finally the last direct method is plant hormone production. Hormones like gibberellins, and acids such as acetic acid that enhances roots growth and uptake of nutrients by inhibiting some harmful and disease-causing microorganisms ( Kumar et al., 2019 ) and indole-3-acetic acid (IAA) primarily controls plant cell differentiation, cell division, and root length ( Mahmud et al., 2021 ).

2.3.2. Indirect mechanism

Indirect plant growth stimulants include the production of hydrogen cynide (HCN) and ammonia. The generation of ammonia can help the host plant fulfill its needs for nitrogen while simultaneously lessening pathogen invasion. Because of its great toxicity against phytopathogens, HCN is extensively used as a biocontrol agent in agricultural settings. However, HCN is also used to chelate metal ions, and therefore indirectly contributes to phosphate availability. Another method for controlling plant infections has been thought to involve microbial production of chitinase. Chitinase causes the disintegration of the cell wall, which impairs the stability of the structure and prevents the growth of pathogens. An integral part of the fungal cell wall known as chitin (1,4-N-acetylglucosamine) is attacked by the enzyme chitinase. A defense mechanism employed by the host plant against a variety of plant diseases, induced systemic resistance (ISR) is brought on by jasmonate and ethylene signaling. ISR is recognized to lessen the severity of disease in a variety of plant species. Through the interaction of specific rhizobacteria with plant roots, it is possible to establish plant resistance against pathogenic bacteria, fungi, and viruses ( Daniel et al., 2022 ; Mahmud et al., 2021 ).

2.4. Biofertilizer production

Biofertilizer was registered in the United Kingdom in 1896 and first produced by Nobbe and Hiltner as a product named “Nitragin” ( Arora et al., 2020 ). It was also produced on a commercial scale in the United States, Malaysia and India in the 1930’s, 1940’s and 1960’s, respectively ( Riaz et al., 2020 ). Biofertilizer production consists of six steps – screening for inoculant strains, deciding on biofertilizer functional traits, product formulation, strain cultivation, testing product type and efficiency, and commercial production ( Raimi et al., 2021 ). Each of these steps is crucial to achieving a high-quality biofertilizer and must be carried out under strict conditions ( Mącik et al., 2020 ).

As shown in Figure 2 , in the first step, the microbial strains are isolated from soil, rhizosphere, and plant tissues such as stems, leaves, seeds, and roots. These strains must withstand the different cultivation methods. Then the microbes that can help enhance the plant growth are identified, isolated, and the functional traits are decided. Culturing improvements broaden the range of recovered microorganisms, increase the chances of discovering useful characteristics ( El-Ramady et al., 2018 ; Kaminsky et al., 2019 ; Raimi et al., 2021 ).

Standardization process for commercial biofertilizer production (Reprinted from Raimi et al. (2021) , with permission from Elsevier).

In the second step, a pure culture is selected based on the desired functional traits like nitrogen fixation, nutrient mobilization and solubilization, and phytohormone production. The suitability and applicability of the selected strains are tested using different lab testing methods, for example, growth on selective media and quantitative testing to determine efficacy degree ( Raimi et al., 2021 ). Also, before producing biofertilizers on a commercial scale, biofertilizer must undergo greenhouse tests to determine their efficiency before application on fields to make sure that it does not have any eco-toxicological effects and has beneficial impacts in promoting plant growth ( Mącik et al., 2020 ). Moreover, the strains are analyzed to see how they promote plant growth. This knowledge can help in formulating the best formula for biofertilizer that can work in different ecosystems, since it is not profitable to produce a biofertilizer for each soil type.

In the third step, the carrier material, which is an inert material that transform microorganisms from the biofertilizer to the soil, is selected, either carrier-based or liquid (broth, broth + polyvinylpyrrolidone). Choosing the suitable carrier is very important to keep the microbes alive and in the right amount must be non-toxic, biodegradable, environmentally friendly, stable at room temperature, and cheap. Compared to solid carriers, liquid inoculants do not need sticky materials, need a fewer number of cells, and can be put in a bottle in larger amounts ( El-Ramady et al., 2018 ; Raimi et al., 2021 ).

In the fourth step, the microbial strains are cultivated and multiplied using fermenters in laboratories under optimal conditions, as well as the appropriate reproduction method. Solid state and liquid fermentation methods are used for producing biofertilizers. In the fifth step, different types of the product (microbial type, product type, and product properties) are tested to select the one with the best performance. In the sixth step, large-scale field testing of biofertilizers is done to determine their efficiency and shortcomings in a variety of ecological regions and environments before finalizing a standardized method for production and processing ( Raimi et al., 2021 ). Finally, the produced biofertilizers must be packed and the package must contain the following information: product name, date of production in addition to expiry date, the microbial strains in it, target crops, name and address of manufacturer, and instructions and recommendations for application ( Mącik et al., 2020 ).

3. Liquid inoculants

For liquid biofertilizers, peat is the most used carrier for biofertilizers due to its properties in supporting the microorganism’s growth and survival. Still, due to its high sterilization cost, difficulty of application in large fields, and difficulty in processing, liquid inoculants were invented to be used as an alternative to solid inoculants. Liquid inoculants can be made from single mixed cultures that improve the cell survival in application and storage conditions ( Buntić et al., 2019 ). The selected carrier should provide the microorganisms with a protective and suitable medium to survive, as well as staying effective over a long period of release. They also must be at neutral or near neutral pH in addition to being environmentally friendly ( Buntić et al., 2019 ; Zommere and Nikolajeva, 2017 ).

Kumar et al. (2019) tested the survivability, nitrogenase activity, indole acetic acid production, ammonia, and siderophore production of 43 isolates obtained on Jensen’s medium of Triticum aestivum (wheat), Zea mays (Maize), Solanum tuberosum (potato), Aloe baradensis ( Aloe vera ), and Bacopa monnieri (Brahmi) soil samples . Four different liquid carriers of compost tea, biogas slurry, vermiwash, and minimal growth medium (peptone water) were used to develop the liquid biofertilizer. The viable cell count was counted over six months with samples drawn at monthly intervals. All the 43 bacterial strains were compared to a reference strain of A. chroococcum . It was found that only 18 isolates produced more than 150 nmol C 2 H 4 h −1 mg −1 of protein nitrogenase activity. In addition, out of these 18 isolates, only six showed higher nitrogenase activity compared to the reference bacterial strain of A. chroococcum , 13 produced IAA, nine produces siderophores, and 11 produced ammonia. Out of these isolates, the isolate from wheat rhizosphere was the most efficient. Based on the 16S rRNA gene sequencing, it was identified as S. rhizophila (WT-A2). As for the survivability test, only the most efficient isolate of WT-A2 was tested. The compost tea carrier showed a mean value of cell count higher than that of the reference strain. After compost tea, biogas slurry was the second-best carrier followed by vermiwash and minimal growth medium. Glycerol can also be added to liquid carriers to increase biofertilizer’s shelf life.

Gopi et al. (2019) developed an optimized liquid formulation of PGPR mix-I containing component cultures – Azotobacter chroococcum , Azospirillum lipoferum , Bacillus megaterium , and Bacillus sporothermodurans . This study was done using totally randomized design of liquid media. The liquid media used were 2% glycerol, 2% polyvinylpyrrolidone (PVP), 15 mM trehalose, 1% glycerol +1% PVP, 2% glycerol, 1% trehalose, 1% yeast extract, 1% PVP, and 1% proline, with a talc based formulation as the standard. All of the inoculated flasks were kept for 18 months at room temperature in a rotary shaker with a constant speed of 100 rpm and were grown on a medium of 1:1:1:1 of Jensen’s broth, nutrient agar, Pikovaskaya’s broth, and nitrogen-free bromothymol blue (NFB). Samples were drawn at bimonthly regular interval. After the first two months 2% glycerol medium showed the highest number of bacterial cells in all of the strains, while at the end of the study 15mM trehalose had the highest viable count due to the protective capability of trehalose in enhancing cell tolerance to desiccation, osmotic pressure, and temperature stress.

Elsakhawy et al. (2021) tested the survivability of Rhizobium sp. SARS 81 maintained on a yeast extract mannitol agar medium (YEMA) and used several additives over 12 months. The bacterial strain was tested on several compositions of YEMA with different compositions of acetone, glycerol, Gum Arabic, and PVP. The cell was counted on a monthly basis. It reached its maximum after the first two months. As for some additives like PVP and PVP + glycerol, they showed a sharp decline after the first six months and reached lower count at the end of the six-month period. Yet, the compositions that contained acetone survived for a longer time. The treatment with PVP + acetone reached a count of 9.93 log CFU mL −1 at the end of the storage period.

Lee et al. (2016) tested the surviavability of Rhodopseudomonas palustris strain PS3 on six additives of alginate, polyethylene glycol, polyvinylpyrrolidone-40, glycerol, glucose, and horticultural oil under low (4 °C ± 2), medium (25 °C ± 2), and high (40 °C ± 3) temperatues. The PS3 strain was grown on purple non-sulfur bacteria (PNSB) broth, incubated for 22 h at 37 °C with 200 rpm until the cell count reached 2 × 10 9 CFU mL −1 . The cell count was adjusted at 9 log CFU mL −1 for all of the six additives. All additives were tested at different concentrations (% w/v ). under the low temperature conditions, 0.5–5% of horticultural oil, 3% glucose, 3% glycerol, and 5% PVP had the highest viable cell count of PS3 > 8 log CFU mL −1 . At medium temperatures, 1% glucose, 0.5% alginate, 2% PVP, and 0.5 and 1% horticultural oil supported the growth of 5.9–6.5 log CFU mL −1 of PS3. Meanwhile, at high temperatures, 1% glycerol, 0.5 and 2% horticultural oil, 3% glucose, and 0.5% PEG supported the growth of 4.7–5.3 log CFU mL −1 of PS3. As seen from the study, only 0.5% horticultural oil supported the growth of PS3 under low, medium and high temperature conditions compared to the control treatment.

Karadbhajne and Jambhekar (2018) tested five different bacterial strains survival over one and a half years to see their viable cell count. This study was done on a pilot scale using a cheap liquid media and showed great results of the effectiveness of liquid inoculant with high viable cell count. All samples were grown on nutrient agar media for 48 h at 30 °C. Samples were drawn at regular interval of 30 days over one and a half year. Acetobacter (nitrogen fixing), Azotobacter (nitrogen fixing), Frateuria sp . (potassium mobilizing), and Pseudomonas sp . (phosphate mobilizing) had 10 14 –10 15 CFU mL −1 viable microorganisms at 28 °C, whilst Trichoderma (plant growth promoting bacteria) had less than 10 8 CFU mL −1 . Another experiment was done using Rhizobium leguminosarum bacteria on nutrient agar broth with additives of polyvinylpyrrolidone at varying concentrations of 2%, 2.5%, and 5%. The concentration at 2.5 % showed the longest survival time of over 720 days with 9.903 CFUmL −1 ( Trivedi et al., 2016 ). Also, bacteria grown on acetone additives (10 mg L -1 ) had a shelf life up to 12 months at room temperature. These experiments showed that a shelf life up to two years is achievable with liquid biofertilizers.

Liquid biofertilizers can be made from the by-products and wastes from several industries. Table 4 shows the possible liquid media sources derived from wastes – the by-product of monosodium glutamate (MSG), fruit and vegetable, glycerin pitch from oleochemical industries, cane molasses, corn steep liquor, and wastewaters.

Table 4

Summary of studies using wastes as growth media for bacteria.

MSG by-products are difficult to treat but they are rich in nutrients and available at low cost. Hence, they can be used as a substrate for liquid biofertilizers. In Namfon et al. (2017) , MSG by-product was used as the main carbon and nitrogen source for the cultivation of bacteria. The study concluded that the best conditions for producing liquid biofertilizer from MSG by-products at economical scale were at a reducing sugar of 20 g L −1 and an inoculum level of 10% for higher viable cell count. The spore count was however low which is an aspect for improvement to achieve longer shelf lives.

Glycerin pitch is a waste product produced from oleochemical industries and possesses risk to the environment when disposed. Glycerin pitch consists mainly of glycerol >55% that can be used as a carbon and energy source for fermentation processes. In Nasarudin et al. (2020) , three samples were prepared with ratios of 1:1, 1; 2, 2:1 of glycerin pitch to Lactobacillus . After mixing them, they were left for 14 days before using it on cucumber seeds. The number of L actobacillus bacteria was determined based on the increment of the turbidity (in nephelometric turbidity units, NTU) in addition to the increase in dry mass concentration in the prepared samples while its size was determined in the order of wavelengths of the visible light. Turbidity increased from 300 NTU to about 380 NTU in 200 h at the glycerin pitch to a Lactobacillus ratio of 2:1, indicating a consistency in the growth of Lactobacillus . The pH in the three samples was reduced. Fumaric acid, lactate and acetate were formed by Lactobacillus that exhibited nutrient-solubilizing characteristics, which helped to tackle hard-to-dissolve nutrients and made them available to plants. Carbon content was also reduced by Lactobacillus bacteria. The reduction in carbon indicates that it was converted into simple and useful forms to the plant. Another parameter was an increase in the liquid viscosity from 2.35 to 3.75 MPS. This viscosity is related to the increase in microbial density which enables longer shelf lives.

In Pastor-Bueis et al. (2017) , the anaerobic digestate from the vegetable and fruit industry was used as the main ingredient of the growth medium for PGPR Bacillus siamensis , which was isolated from the rhizosphere of a sweet pepper crop. The field tests showed that treatments inoculated with the biofertilizer made of anaerobic digestate at 50% dilution and 2.3% sugar beet molasses and fertilized with decreased mineral N at 80% produced much better results than the ones with merely 80% of N and 100% of N without the biofertilizer.

High-cost materials are usually used for the fermentation of Bacillus subtilis such as corn starch and peptone. Due to this fact, there is a need to find cheaper and more readily available alternatives. Corn steep liquor (CSL) is a concentrated organic wastewater that is produced from corn wet milling. It is rich in amino acids and protein. In He et al. (2020) , it was found that, as the concentration of CSL increased, it inhibited the growth of Bacillus bacteria. Therefore, the best concentration was between 100 to 200 g L -1 . Similarly, organic wastes from agricultural activities such as sugar cane byproduct and cane molasses can be used as a cheap liquid media to produce liquid biofertilizers. Cane molasses is rich in sugar (46–52%) which is an energy and carbon source for Azotobacter and Bacillus . It is also rich in acids, as well as calcium, potassium, sulfate, sulfite, chloride, sodium, and magnesium which are important for the growth of the bacteria. In Hindersah et al. (2020) , two types of Bacillus ( B. magaterium and B. subtilis ) and Azotobacter ( A. chroococcum and A. vinelandii ) were used and kept on nutrient agar and Ashby’s mannitol agar. Both Azotobacter and Bacillus species produced phytohormone IAA, exopolysaccharide, cytokinin (Cks) and gibberellins (GAs). In this experiment, molasses was the only carbon source while ammonium chloride was added as a nitrogen source. The 1:1:1:1 composition gave the best result over one month of storage time where the viable cell count did not differ significantly. The presence of IAA, Cks, GAs, and zeatin indicates that the waste product of sugar cane industries is a good source for producing liquid biofertilizers.

Dairy wastewater and mixed mackerel and brown seaweed wastewater were also used as the liquid media sources as they are nutritionally rich ( Halder et al., 2020 ; Jung and Kim, 2020 ). In Halder et al. (2020) , dairy wastewater was converted into biofertilizer and tested on mung bean in India. Four treatment sets were compared – raw effluent, microbially treated effluent, tap water with chemical fertilizer and tap water (as the control). Microbially treated dairy effluent yielded the best results in terms of percentage survival, nodulation, and seed yield, indicating that the treated effluent can be fully used for irrigation, resulting in zero liquid discharge, thus increasing the economic benefits of dairy industries. Similarly in Jung and Kim (2020) , mixed fishery wastewater from mackerel and brown seaweed was converted into biofertilizer using Bacillus species. The 72-hour culture broth yielded a biofertilizer which met the standard content of N, P, K, heavy metals and the number of viable cells. When applied to one-month-old lettuce plants, an enhanced growth rate was observed compared with controls, with high chlorophyll and carotenoid content, high antioxidant activity and no permeation of pathogens.

4. Effects of liquid biofertilizers on plant growth

Table 5 summarizes some selected studies conducted on different crops with different liquid inoculants and bacteria strains. Buntić et al. (2019) did an experiment on alfalfa seed, which is a leguminous plant of the pea family (Fabaceae) used to fix nitrogen to other plants, because it houses rhizobia bacteria. Alfalfa is planted as a cover crop to enhance the soil properties and increase its nutrient levels. It can also tolerate drought, heat, and cold weather. The Sinorhizobium meliloti L3Si strain was grown in yeast mannitol broth (YMB). As for the liquid inoculant, ten different media were prepared. They were added in combination or separately. For the survival of L3Si during a storage time of 150 days, the most suitable liquid inoculant was found to be a glycerol medium formulated with agar or sodium-alginate. Sinorhizobium meliloti L3Si’s effectiveness on alfalfa seeds were studied on nodulation, plant height, shoot dry weight, and nitrogen content in the shoot dry weight. After one-month storage, alfalfa seeds pre-inoculated with YMB, YMB with agar, and YMB with sodium-alginate for up to three months produced successful alfalfa plants with nitrogen content ranging from 3.72 to 4.19%.

Table 5

Selected studies conducted on different crops with different liquid inoculants and bacteria strains in recent years.

Lu et al. (2020) did an experiment on Vitis vinifera L. (grapes) by preparing four different concentrations of P. putida Rs-198 in a nutrient agar liquid medium. The most effective number of Rs-198 was 1.44 × 10 13 CFU mL −1 in the sample, called BFP3 in terms of soil physiochemical properties, appearance, and quality of grape. The use of Rs-198 increased the growth and quality of grapes as it increased the grape width by 4.4%, length by 6.2%, and weight by 17.2% compared to non-inoculated grapes. The physiochemical properties and fertility of soil was increased significantly by the application of Rs-198 due to the increased enzymes’ activity. The alkaline phosphate and invertase activities were increased by 27.15% and 48.33%, respectively, and the urease was almost the same. Another experiment was done on pepper seeds by He et al. (2019) where they compared inoculated and non-inoculated seeds. The inoculated plants had higher contents of chlorophyll a, chlorophyll b, and carotenoids, with 162%, 152%, 84%, 108%, 97%, and 131% more flowers, leaves, root fresh weight, shoot fresh weight, root dry weight, and shoot dry weight, respectively. The contents of N, P, K and Na in the stems and leaves were increased because Rs-198 induced the alteration of Na uptake by modifying the expression of Na + /H + antiporter.

In Nasarudin et al. (2020) , three samples were prepared using different ratios of glycerin pitch and Lactobacillus bacteria. Glycerin pith was used successfully as a growth medium and carbon source for Lactobacillus bacteria. When applied to cucumber, its height was almost doubled when compared to commercial fertilizers. Guimarães et al. (2020) did an experiment on Oryza sativa L. (rice) at different locations in Brazil that had different soil types to study the efficiency of the Azospirillum brasiliense liquid and solid biofertilizers. Seven samples were prepared using commercial liquid and solid biofertilizers. The sample with 40 kg N ha −1 of Nitro 1000 liquid biofertilizer containing 2 × 10 8 CFU mL −1 Azospirillum brasiliense showed the best results in the four different regions of Toledo, Palotina, Cascavel, and São Miguel do Iguaçu. This liquid biofertilizer sample also showed better performance and efficiency than that using solid inoculant.

Microalgae-based biofertilizers have also been evaluated. In Dineshkumar et al. (2020) , liquid biofertilizers extracted from Chlorella vulgaris and Spirulina platensis were applied on green gram Vigna radiata (L.). Among all the treatment concentrations, the two treatments at 100% showed the highest yield of green gram yielding 29 and 30 pods plant −1 for Chlorella vulgaris and Spirulina platensis, respectively. Also, the plant height, root and shoot dry weight, nutrient compositions were increased significantly. Amino acids were found to be higher in plants treated with Chlorella vulgaris, whereas N, P, and K were found to be higher in plants treated with Spirulina platensis ( Dineshkumar et al., 2020 ) .

He et al. (2016) experimented with the effect of cotton plant growth treated by free and encapsulated Pseudomonas putida Rs-198 under salt stress. The encapsulated Pseudomonas putida Rs-198 with 2% salt stress condition did not increase the plant height but the root length, fresh and dry weights. While the encapsulated Pseudomonas putida Rs-198 without salt stress enhanced the plant height, fresh and dry weight. It can be concluded that the encapsulation of bacteria with alginate can enhance plant growth in nutrient deficient soils. Also, Abd_Allah et al. (2018) tested the adaptive mechanism of chickpea plants treated by Bacillus subtilis under saline conditions. The treated plants with Bacillus subtilis under saline conditions reduced sodium accumulation and enhanced nitrogen, potassium, calcium, and magnesium contents in plants, as well as enhancing the membrane stability under salinity and non-salinity conditions.

Jain et al. (2021) experimented with the effects of bacterial consortia consisting of Azotobacter , phosphorus solubilizing bacteria, potassium mobilizing bacteria, and zinc solubilizing bacteria on the growth of wheat in two successive rabi seasons of 2017–2018 and 2018–2019. Two microbial consortia where prepared – one of them contained all the mentioned bacterial strains above (BF 2 ) and the other with the absence of ZSB (BF 1 ). The best results were obtained from the treatment combination of using BF 2 in addition to the inorganic chemical fertilizer at 100% recommended doses of NPK (120 kg N + 60 kg P + 40 kg K), where it enhanced plant growth, grain yield, and benefit-cost ratio. Statistically, BF 1 and BF 2 with 75% of the recommended dose of inorganic fertilizer can be used, yielding very close results to BF 2 + 100%, so it could save about 25% of inorganic chemical fertilizer. In a similar manner, Tinna et al. (2020) experimented with a combination of a bacterial consortia with an inorganic chemical fertilizer. They reached the same conclusion that a combination of both chemical and biofertilizer could save up to 25% of chemical fertilizer, enhancing the plant height, bulb yield, and number of leaves of onions.

5. Challenges and future perspectives

Most of the biofertilizers produced are effective on certain crops, soil types, and climates. Plant growth and development is affected by several biotic and abiotic stresses in the soil environment ( Bramhachari et al., 2018 ). Moisture is needed for nutrient uptake and absorption by plants. Yet, due to climate change, drought stress is considered one of the most serious abiotic environmental stresses affecting the hemostasis of soil, and the morphological, physiological, and nutritional traits of plants ( Anli et al., 2020 ; Borowik and Wyszkowska, 2016 ). The results of applying liquid biofertilizers are sometimes unpredictable like what happened in Belgium in the 1999–2000 season when a biofertilizer had positive effects at the start of the winter season, but as weather conditions worsened, the final yield did not reach its full potential ( Stamenković et al., 2018 ). The same happened in Uruguay, where at first plant growth was observed, but decreased with time with no significant difference between inoculated and non-inoculated plants. When the experiment was done outside of the growth season, the results were negligible ( Dobbelaere et al., 2001 ). Therefore, biofertilizers must be developed to resist drought stress and other environmental stresses due to seasonal changes, as well as to search for microbial strains that can withstand stressful conditions. By doing so, farmers in harsh environments or developing countries will benefit from such biofertilizers ( Santos et al., 2019 ).

From the literature review presented here, it is apparent that there is a lack of field tests to test the efficiency of biofertilizers. The effect of Bradyrhizobial bacteria on peanut production in Argentina was studied at four different locations to test the inoculation efficiency. The results showed that there was a response only at one location because the soil was N-deficient ( Valetti et al., 2016 ), suggesting that biofertilizer efficiency varies through different soil types in different ecological regions. Hence, more field trials to test biofertilizer efficacy and limitations are essential on a case-by-case basis to better understand the relationships among crops, nutrients, and microorganisms present in the soil, keeping in mind that biofertilizers are not a source of nutrients ( Raimi et al., 2021 ).

When transforming liquid biofertilizer from laboratory scale to large scale, it may act poorly due to other variables not being studied on the lab scale. These variables must be taken into consideration to produce liquid biofertilizers suitable for various weather conditions and soil types. Another challenge is that for liquid biofertilizers, different or more advanced machinery might be required for large-scale application, thus making it energy intensive. Therefore, liquid biofertilizers must be produced in a way that can be used on the current or low-cost machinery.

Since a viable cell count is the most important factor in evaluating the quality of liquid biofertilizers, there is a need to develop new technologies to target the additives and carriers that are cheap, easy to use, and effective in supporting a large number of viable cells count with over 1 × 10 8 CFU mL −1 over long periods of time for transportation and storage ( Hindersah et al., 2020 ; Mitter et al., 2021 ). Waste by-products that are rich in valuable sources such as nutrients, chemical oxygen demand, sulfates, chlorine, ammonia, and other non-toxic, environmentally friendly substances, can be used as an alternative source for biofertilizer carriers because some industries have difficulties in treating their wastes and wastewater or have to pay to dispose of them ( Arumugam et al., 2021 ) ( Arumugam et al., 2021 ; Namfon et al., 2017 ; Nasarudin et al., 2020 ; Rai et al., 2022 ). This would be a step towards circular economy where wastes or wastewaters can be applied as the liquid media to produce liquid biofertilizers. More research is needed in this area to explore which potential by-products that are rich in beneficial substances to support the growth of bacteria for producing biofertilizers that are cost effective while ensuring the safety of workers and the environment in the long term.

To evaluate their viability, a cost-benefit analysis must be done to deduce the profitability of biofertilizer. After discounting the gross cost and benefit, an organization will be profitable if the benefit-to-cost ratio surpasses 1. For example, the benefit-cost ratio was found to be 17 for soybean by fixing 100 kg N ha −1 , and 416 for clover by fixing 200 kg kg N ha −1 based on n-fixation since they are legume crops ( Mulongoy et al., 1992 ). Also, the biofertilizer energy requirement is fully paid by nature when compared to chemical fertilizers that require 80 MJ for N, 12 MJ for P, and 8 MJ for K leaving many small-holder farmers unable to afford the expensive energy bill. In legume plants, 48–300 kg N ha −1 is fixed in a season. The amount of biofertilizers required to supply plants with the same amount of nutrients is much less than chemical fertilizers. Additionally, this low-cost method of supplying nutrients to soil makes it attractive to small-holder farmers ( Raimi et al., 2017 ). Therefore, more studies are required to conduct cost-benefit analyses of biofertilizers based on plant yields.

Some biological molecules such as flavonoids, strigolactones, and polysaccharides can promote a symbiotic relationship between arbuscular mycorrhiza fungi and the host plant, as well as rhizobium during nodule formation. For improved product formulation, these compounds should be explored ( Raimi et al., 2021 ). The existing bacterial strains help in improving one trait of the plant, but scientists may need to develop genetically engineered strains that are more efficient while ensuring that these developed strains do not cause any hazards or risk ( Mahanty et al., 2017 ; Mitter et al., 2021 ).

Some studies have shown that biofertilizers can affect the surrounding environment by introducing microorganisms that can affect the structure of native microflora and some non-target effects like changes in biogeochemical cycles, soil texture, and soil properties. However, it is still unknown how these microorganisms react with the presented microflora. In addition, the severity of the changes on the ecological systems have yet to be revealed. No recent studies have explored the safety of bioinoculants for commercial use ( Mahanty et al., 2017 ).

In addition, there is a need to improve education about biofertilizers and their long-term benefits compared with chemical fertilizers, and to correct the misconception about microorganisms being a source of disease. Biofertilizers will require new and innovative techniques for the growth, transportation, formulation, storage, and application of microorganisms as they go from small scale (laboratory and greenhouse tests) to large scale production. More investment is needed in the existing and future technologies via research to produce cost-effective and environmentally friendly biofertilizers. However, there is a lack of communication between farmers, industry, researchers, and governmental sectors. Multi-stakeholder partnerships are definitely crucial in order to develop biofertilizers that do the best job possible.

6. Conclusion

Liquid biofertilizers consist of living microorganisms that enhance soil properties and increase plant growth and yield. Liquid biofertilizers have been applied to different crops and yielded the best results when compared to other types of chemical or carrier-based fertilizers. In some cases, plant growth increased two-fold. Biofertilizers can be produced by using a single or a mix of microorganisms based on the role the biofertilizer is produced for. Also, liquid biofertilizers can be made from wastes and by-products of some industries as they could be a suitable and low-cost option for the growth of the bacterial cells instead of using specially made media. Finally, in order to develop effective liquid biofertilizers, more research is needed to overcome their limitations in the aspects of better climate adaptation, longer shelf life, better liquid inoculant, and use of low-cost or existing machinery for large-scale application. Cost-benefit analyses, field trials, long-term safety and effectiveness evaluations, and multi-stakeholder partnerships are the essential elements to evaluate the feasibility of the liquid biofertilizer on a case-by-case basis, taking into consideration the location, crop type, soil type, and climate.

Declarations

Author contribution statement.

All authors listed have significantly contributed to the development and the writing of this article.

Funding statement

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Data availability statement

Declaration of interest’s statement.

The authors declare no competing interests.

Additional information

No additional information is available for this paper.

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Open Access

Peer-reviewed

Research Article

Effects of different fertilization rates on growth, yield, quality and partial factor productivity of tomato under non-pressure gravity irrigation

Contributed equally to this work with: Qing-Jie Du, Huai-Juan Xiao

Roles Formal analysis, Writing – original draft

Affiliation College of Horticulture, Henan Agricultural University, Zhengzhou, Henan, China

Roles Writing – original draft, Writing – review & editing

Roles Data curation, Writing – review & editing

Roles Conceptualization, Data curation

Roles Methodology

Roles Formal analysis, Validation, Writing – review & editing

* E-mail: [email protected]

• Qing-Jie Du, 
• Huai-Juan Xiao, 
• Juan-Qi Li, 
• Jia-Xin Zhang, 
• Lu-Yao Zhou, 
• Ji-Qing Wang

• Published: March 12, 2021
• https://doi.org/10.1371/journal.pone.0247578
• Reader Comments

To select the optimum fertilizer application under specific irrigation levels and to provide a reliable fertigation system for tomato plants, an experiment was conducted by using a microporous membrane for water-fertilizer integration under non-pressure gravity. A compound fertilizer (N:P 2 O 5 :K 2 O, 18:7:20) was adopted for topdressing at four levels, 1290 kg/ha, 1140 kg/ha, 990 kg/ha, and 840 kg/ha, and the locally recommended level of 1875 kg/ha was used as the control to explore the effects of different fertilizer application rates on growth, nutrient distribution, quality, yield, and partial factor of productivity (PFP) in tomato. The new regime of microporous membrane water-fertilizer integration under non-pressure gravity irrigation reduced the fertilizer application rate while promoting plant growth in the early and intermediate stages. Except for the 990 kg/ha fertilizer treatment, yields per plant and per plot for each fertilizer application rate were higher than or equal to those of the control. The new regime could effectively improve PFP and reduce soil nutrient enrichment. Fertilizer at 840 kg/ha showed the optimum results by increasing PFP by 75.72% as compared to control. In conclusion, the fertilizer rate at 840 kg/ha has not only maintained the productivity of soil but also tomato growth and quality of fruit which makes the non-pressure gravity irrigation a potential and cost-effective way for fertilizer application.

Citation: Du Q-J, Xiao H-J, Li J-Q, Zhang J-X, Zhou L-Y, Wang J-Q (2021) Effects of different fertilization rates on growth, yield, quality and partial factor productivity of tomato under non-pressure gravity irrigation. PLoS ONE 16(3): e0247578. https://doi.org/10.1371/journal.pone.0247578

Editor: Zhihui Cheng, Northwest Agriculture and Forestry University, CHINA

Received: July 22, 2020; Accepted: February 10, 2021; Published: March 12, 2021

Copyright: © 2021 Du et al. This is an open access article distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Data Availability: All relevant data are within the manuscript and its Supporting Information files.

Funding: The work was supported by the Special Support Project for the Construction of Technology Systems for the Bulk Vegetable Industry in Henan Province (CZ2015S003). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Competing interests: The authors have declared that no competing interests exist.

Introduction

Fertilizers, which are indispensable and the most important material input in modern agricultural production [ 1 , 2 ], have played a vital role in improving the yield and quality of crops [ 3 – 5 ]. However, over-fertilization not only inhibits the improvement of crop yield and quality, it also results in serious issues, such as hardening and acidification of the soil, aggravation of crop pests, leaching loss of soil nutrients, and threats to groundwater safety. These issues exert a serious impact on agricultural sustainability and the ecological environment [ 6 – 8 ]. In recent years, integrated techniques of water and fertilizer application have been widely developed and popularized. These studies have conducted irrigation and fertilization trials according to the soil nutrient status and the crop water and fertilizer requirements, thus achieving the purpose of saving water and fertilizer, increasing production and quality, and protecting the ecological environment [ 9 – 11 ]. The microporous membrane water-fertilizer integration technique is newly developed. By adopting microporous membranes as a substitute for drip irrigation tapes and pipes, which involves placing a perforated membrane in the furrow between two cultivation ridges and covering it with a plastic film, water can flow between the plastic film and the perforated membrane and infiltrate into the soil through pores on the membrane under non-pressure gravity irrigation. This technique not only saves irrigation equipment costs, but it also eradicates blocking, and has better irrigation uniformity [ 12 ].

To date, numerous studies have explored the effects of fertilizer application rate on crop growth, yield, and quality [ 4 , 9 , 13 ]. For example, Qu et al. [ 14 ] found that the yield increased with a rising fertilizer application rate up to a point, after which yield decreased in cucumbers grown in substrate bags in spring. Zhang et al. [ 15 ] noticed that, compared to the conventional fertilizer application method, a controlled-release fertilizer management method significantly increased yield, with more accumulated total dry weight in bitter gourd. Currently, the techniques integrating microporous membrane water and fertilizer application are largely based on drip irrigation tapes, and the possibility of non-pressure gravity irrigation by water-fertilizer integration using microporous membranes has rarely been explored.

In this research, we employed the integrated microporous membrane water and fertilizer technique for non-pressure gravity irrigation, to determine the optimal fertilizer application rate of spring tomato cultivated in a plastic greenhouse under a specific irrigation level and to clarify the fertilizer requirements of tomato, to thus provide a theoretical basis for efficient fertilizer application and cultivation.

Material and methods

Experimental material, site, and time.

The ‘K1602’ tomato variety was employed in this study. Water-soluble fertilizer (N:P 2 O 5 :K 2 O, 18:7:20) and base fertilizer (N:P 2 O 5 :K 2 O, 15:15:15) were obtained from Yichuan Fufeng Plant Nutrients & Fertilizers Co., Ltd. The perforated plastic film was 60 cm wide and 6.4 m long. Holes (3-mm diameter) in the film were spaced at intervals of 20 cm lengthwise and 12.5 cm across, with three holes punched in each row. The experiment was performed at Zhengzhou Zhengyan International Seed Technology Exhibition Park (Xinzheng, China) (34°16′ to 34°39′ N, 113°30′ to 113°54′ E), from March 16 to July 12, 2017.

Experimental design and treatment

Four different fertilizer levels were examined in this experiment: 1290 kg/ha (FA), 1140 kg/ha (FB), 990 kg/ha (FC), and 840 kg/ha (FD), respectively. The local traditional fertilizer application level (1875 kg/ha) was set as the control (CK). The irrigation amount and target yield of all treatments were 1650 m 3 /ha and 11.25 t/ha, respectively.

Tomato seedlings were planted at the six-leaf stage. Each plot area was 7.8 m 2 (6 m × 1.3 m), with three biological replicates. The base fertilizer was applied in the form of dried chicken manure (1.5 × 10 4 kg/ha) and compound fertilizer (N:P 2 O 5 :K 2 O, 15:15:15, 525 kg/ha). The CK treatment used furrow irrigation to fertilize plants, and integrated irrigation and fertilizer application was performed in other treatments. The times and amounts of irrigation and fertilization are listed in Table 1 .

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https://doi.org/10.1371/journal.pone.0247578.t001

Measurements of crop parameters

For analysis, seven plants were randomly selected from each treatment from one replicate. Plant height, stem diameter, and leaf number were measured 20, 40, and 60 d after planting. Fresh and dry weight as well as the nitrogen (N), phosphorus (P), and potassium (K) contents of plants were measured after uprooting. Soil samples before transplanting and after uprooting were collected from the 0–20, 20–40, and 40–60 cm soil layers using a five-point sampling method [ 16 ]. The third truss fruits were picked to determine fruit quality.

Data analysis

All data are presented as the mean ± standard error (SE) of three replicates and were analyzed using Data Processing Software (DPS, version 7.05) following one-way analysis of variance (ANOVA). Significant differences ( P < 0.05) among treatment means after controlling for multiple comparisons were determined from a least significant difference (LSD) test.

Effects of different fertilizer application rates on plant growth at different periods

Fertilizer application rate affected plant growth ( Table 2 ). At the 20 th d after planting, plant height and stem diameter of FB and FC plants and leaf number of FA and FC plants, were significantly higher than those of CK plants. By the 40 th d, plant height of FA and FB plants, stem diameter of FC plants, and leaf number of FA plants were respectively increased by 17.70%, 17.04%, 15.54%, and 8.14%, compared to CK plants. By the 60 th d, there were no significant differences among various fertilizer treatments in plant height, stem diameter, or leaf number. These results indicated that fertilizer mainly had an effect during the early and intermediate stages of plant growth, among which the effect of the FC treatment was best.

https://doi.org/10.1371/journal.pone.0247578.t002

Effects of different fertilizer application rates on fresh and dry weight

Fresh and dry weight of roots under FA treatment were highest, which were 37.31% and 47.00% higher than those under the CK treatment, respectively ( Table 3 ). The fresh weight of stems was not significantly different among the FB, FC, and CK treatments, but significantly greater than that in the FD treatment. The dry weight of stems was not significantly different among the FB, FC, FD, and CK treatments, which were each significantly lower than that in the FA treatment. Fresh and dry weights of leaves increased as fertilizer application amount decreased except for the FD treatment; those of the FA, FB, and FC treatments were significantly higher than those in the CK treatment, with the FC treatment having the highest values, 97.37% and 95.69% higher than those in the CK treatment, respectively.

https://doi.org/10.1371/journal.pone.0247578.t003

Effects of different fertilizer application rates on N, P, and K contents of tomato plants

Total N content in the roots was not significantly different among the FC, FD, and CK treatments and significantly greater than that in the FA and FB treatments ( Table 4 ). Total N content in the stems and leaves were lowest under the FD and FC treatments, respectively, which were not significantly different compared with the CK treatment. The P content of the roots under the FC treatment was higher than that in the CK treatment; no significant differences in P content of the roots or stems were recorded between any other fertilizer treatment and the CK treatment. P content of the leaves under the FA treatment was higher than in the CK treatment, while that in the other fertilizer application treatments was lower than that in the CK treatment. The K content of the roots and stems were greatest under the FD and FC treatments, respectively, and significantly greater than that in the CK treatment. However, the K content of leaves in the FC and FD treatments were lower than in the CK treatment.

https://doi.org/10.1371/journal.pone.0247578.t004

Effects of different fertilizer application rates on N, P, and K contents in different soil layers

To analyze the nutrient surpluses in the soil, the N, P, and K contents of soil before planting and after uprooting in different layers were measured ( Table 5 ). The N content of the CK treatment in the top soil layer (0–20 cm) was not significantly different from the soil before transplanting, while the same layers of FA and CK soil were greatly higher in N content than those of the FC and FD treatments. The P content of the soil before transplanting was sharply lower than the FA and FC soil, and that no significant differences were found among the FB, FD, and CK treatments. For K content, there were no significant differences among fertilizer levels, and that of each treatment was significantly lower than in the soil before transplanting. In the 20–40 cm soil layer, the N contents of the CK treatment was remarkably greater than in the soil before transplanting and other fertilizer treatments. The P content in CK soil was significantly lower than that in the soil before transplanting and FA soil and sharply higher than in the soil in the other treatments. Except for the FB treatment soil, the K content of CK soil was not notably different from the other treatments. In the drip soil layer (40–60 cm), the N content of FC and FD soils were significantly lower than that of CK soil. The P content of CK soil was highest, while that of FC soil was lowest. The K content of CK soil was significantly lower than of FA and FB soils and not different from that of basic soil or the other fertilizer levels. Thus, N, P, and K enrichment under the FC and FD treatment was decreased in drip soil.

https://doi.org/10.1371/journal.pone.0247578.t005

Effects of different fertilizer application rates on tomato quality

Soluble sugar content under the FD treatment was highest, 2.4% higher than that under the FC and CK treatments ( Table 6 ). There was no significant difference in organic acid content under the CK, FC, and FD treatments. The sugar-acid ratio of under the FA, FB, and FD treatments were markedly greater than that of the CK treatment (16.57%, 17.71%, and 11.14% higher, respectively), while those of the FD and FC treatments were not notably different. The lycopene content under the FB, FC, and FD treatments were all significantly higher than that under the CK treatment, with that of the FC treatment being the highest, 39.58% higher than that of the CK treatment. The soluble protein content of the CK treatment was significantly lower than that of the FA treatment (by 8.19%), but greater than that of the other fertilizer treatments. The soluble solid content under the CK treatment was highest, but not significantly different than that under the FA, FC, and FD treatments. The vitamin C content under the FA treatment was greatest, but that was not distinctly different from that of the CK treatment. On the whole, fertilizer treatments FC and FD were more effective in improving tomato fruit quality.

https://doi.org/10.1371/journal.pone.0247578.t006

Effects of different fertilizer application rates on yield and PFP

The FA yield per plant was highest, being significantly higher than that of the CK treatment (by 8.82%), while those of the other fertilizer treatments were not significantly different from that of the CK treatment ( Table 7 ). Plot yield for the FA and FB treatments were significantly higher than that under the CK treatment (5.65% and 6.89%, respectively). PFP under the four fertilizer levels were significantly (39.71%, 54.08%, 47.83%, and 75.72%, respectively) greater than that under the CK treatment, while the FD treatment had the highest PFP, with a plot yield that was not significantly different from that of the CK treatment.

https://doi.org/10.1371/journal.pone.0247578.t007

Compared to the use of furrow irrigation to apply fertilizer, the microporous membrane water-fertilizer integration technique (which functions like drip irrigation technology) was able to reduce topdressing amounts and promote normal growth in tomato plants. The drip irrigation equipment needs a large initial investment, however, the microporous membrane used in this study was made from a used shed film, which is more economic for growers than installing a drip irrigation system.

Scientific fertilizer application offers an important means of improving crop growth, protecting the ecological environment, and maintaining agricultural sustainability. Plant fresh and dry weight, which reflect the accumulation of plant biomass to some extent, constitute important indicators of growth vigor [ 15 , 22 ]. In general in this study, under the same irrigation conditions, plant growth in the early and intermediate stages increased with decreasing fertilizer application up to a point, after which they decreased. Fertilizer application improved availability of NPK in root zone, leading to an increase in uptake of nutrients to the plant. Many studies have demonstrated this increment in nutrients contributed to plant biomass accumulation is due to higher leaf photosynthetic capacity [ 1 , 23 ]. However, excess fertilizer application would result in low water availability to plant due to high osmotic conditions in soil, and therefore stunted plants [ 24 ]. Our results also showed that the total NPK contents of FC plants were the highest, corresponding to the best plant growth and highest dry weight.

Nutrient content in the surface soil is influenced by fertilizer application rate, irrigation, and plant species, as nutrients are partially taken up by plants and partially migrate downward deep into soil as moisture moves [ 25 , 26 ]. In the present study, N and K were enriched in deep soil, especially under high fertilizer application, but the contents of N and K in 0–20 cm soil were similar or lower than that in soil before treatment. In soil, N and K are mobile nutrients. Displacement of N and K through the soil profile often occur with irrigation during over application [ 27 , 28 ]. This may be responsible for the N and K distribution in soil under high fertilizer application. On the contrary, P enrichment was found in topsoil, which may be due to high Ca 2+ concentrations in water and soil in experimental site [ 29 , 30 ]. In calcareous soils, P can be immobilized into insoluble compound, such as calcium-phosphate minerals, leading to low mobility [ 31 , 32 ]. The high residues of nutrient would increase the risk of groundwater pollution. Thus, the 840 kg/ha fertilizer application rate met the nutrient needs of tomato plants, without leaving excess residues in the soil, making it the optimal fertilizer application rate.

In this study, the PFP under four fertilization levels were significantly higher than that of the CK treatment. This suggested that the microporous membrane water-fertilizer integration technique could improve PFP. Moreover, PFP is greatly affected by fertilizer supply level. We found that the highest PFP occurred under the lowest fertilizer amount (840 kg/ha). Previous studies also confirmed that the highest PFP often occur under a low fertilizer supply level [ 26 , 33 ]. According to fertilizer response function, positive effects of fertilizer on yield may be responsible for the high PFP under low fertilizer supply level [ 34 ]. On the other hand, high fertilizer input increased nutrient leaching losses, and therefore low PFP [ 22 , 35 ].

Fertilizer is an important determinant for yield formation. High fertilizer application under non-pressure gravity irrigation enhanced yield compared with CK while no significant difference in yield was observed between lowest fertilizer treatment (840 kg/ha) and CK. Interestingly, the yield was lowest under 990 kg/ha treatment. This may be attributed to more photosynthate allocation to vegetative growth, thereby impacting their reproduction. Under non-pressure gravity irrigation, the fertilizer application rate was declined by 31.2%-53.6% compared with CK. Thus, the decreased fertilizer supply under non-pressure gravity irrigation have no negative effect on tomato plant growth and yield. Specifically, the 840 kg/ha fertilizer treatment achieved the highest economic value under non-pressure gravity irrigation. Although the per plant and plot yields under 840 kg/ha fertilizer treatment were 8.8% and 5.7% lower than that under the 1290 kg/ha fertilizer treatment, the fertilizer input decreased by 34.8%. Considering the fertilizer input, nutrient residues and yield, 840 kg/ha fertilizer application is recommended.

In conclusion, the 840 kg/ha fertilizer application rate most effectively improved the yield, PFP, and soil productivity maintenance, with better quality of tomato fruits. Our results preliminarily identified a specific irrigation and fertilization regime for tomato cultivation under non-pressure gravity irrigation. In future work, the optimal application proportion of NPK for tomato should be assessed under non-pressure gravity irrigation.

Supporting information

https://doi.org/10.1371/journal.pone.0247578.s001

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• Introduction

Essential plant nutrients

Determining nutrient needs, the economics of fertilizers, synthetic fertilizers, farm manure, green manuring, methods of application.

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• Table Of Contents

fertilizer , natural or artificial substance containing the chemical elements that improve growth and productiveness of plants. Fertilizers enhance the natural fertility of the soil or replace chemical elements taken from the soil by previous crops.

Soil fertility is the quality of a soil that enables it to provide compounds in adequate amounts and proper balance to promote growth of plants when other factors (such as light, moisture, temperature, and soil structure) are favourable. Where fertility of the soil is not good, natural or manufactured materials may be added to supply the needed plant nutrients. These are called fertilizers, although the term is generally applied to largely inorganic materials other than lime or gypsum .

In total, plants need at least 16 elements, of which the most important are carbon , hydrogen , oxygen , nitrogen , phosphorus , sulfur , potassium , calcium , and magnesium . Plants obtain carbon from the atmosphere and hydrogen and oxygen from water; other nutrients are taken up from the soil. Although plants contain sodium , iodine , and cobalt , these are apparently not essential. This is also true of silicon and aluminum .

Overall chemical analyses indicate that the total supply of nutrients in soils is usually high in comparison with the requirements of crop plants. Much of this potential supply, however, is bound tightly in forms that are not released to crops fast enough to give satisfactory growth. Because of this, the farmer is interested in measuring the available nutrient supply as contrasted to the total nutrient supply. When the available supply of a given nutrient becomes depleted , its absence becomes a limiting factor in plant growth. Excessive quantities of some nutrients may cause a decrease in yield, however.

Determination of a crop’s nutrient needs is an essential aspect of fertilizer technology . The appearance of a growing crop may indicate a need for fertilizer, though in some plants the need for more or different nutrients may not be easily observable. If such a problem exists, its nature must be diagnosed, the degree of deficiency must be determined, and the amount and kind of fertilizer needed for a given yield must be found. There is no substitute for detailed examination of plants and soil conditions in the field, followed by simple fertilizer tests, quick tests of plant tissues, and analysis of soils and plants.

Sometimes plants show symptoms of poor nutrition. Chlorosis (general yellow or pale green colour), for example, indicates lack of sulfur and nitrogen. Iron deficiency produces white or pale yellow tissue. Symptoms can be misinterpreted, however. Plant disease can produce appearances resembling mineral deficiency, as can various organisms. Drought or improper cultivation or fertilizer application each may create deficiency symptoms.

After field diagnosis , the conclusions may be confirmed by experiments in a greenhouse or by making strip tests in the field. In strip tests, the fertilizer elements suspected of being deficient are added, singly or in combination, and the resulting plant growth observed. Next it is necessary to determine the extent of the deficiency.

An experiment in the field can be conducted by adding nutrients to the crop at various rates. The resulting response of yield in relation to amounts of nutrients supplied will indicate the supplying power of the unfertilized soil in terms of bushels or tons of produce. If the increase in yield is large, this practice will show that the soil has too little of a given nutrient. Such field experiments may not be practical, because they can cost too much in time and money. Soil-testing laboratories are available in most areas; they conduct chemical soil tests to estimate the availability of nutrients. Commercial soil-testing kits give results that may be very inaccurate, depending on techniques and interpretation. Actually, the most accurate system consists of laboratory analysis of the nutrient content of plant parts, such as the leaf. The results, when correlated with yield response to fertilizer application in field experiments, can give the best estimate of deficiency. Further development of remote sensing techniques, such as infrared photography, are under study and may ultimately become the most valuable technique for such estimates.

The practical goal is to determine how much nutrient material to add. Since the farmer wants to know how much profit to expect when buying fertilizer, the tests are interpreted as an estimation of increased crop production that will result from nutrient additions. The cost of nutrients must be balanced against the value of the crop or even against alternative procedures, such as investing the money in something else with a greater potential return. The law of diminishing returns is well exemplified in fertilizer technology. Past a certain point, equal inputs of chemicals produce less and less yield increase. The goal of the farmer is to use fertilizer in such a way that the most profitable application rate is employed. Ideal fertilizer application also minimizes excess and ill-timed application, which is not only wasteful for the farmer but also harmful to nearby waterways. Unfortunately, water pollution from fertilizer runoff , which has a sphere of impact that extends far beyond the farmer and the fields, is a negative externality that is not accounted for in the costs and prices of the unregulated market.

Fertilizers can aid in making profitable changes in farming . Operators can reduce costs per unit of production and increase the margin of return over total cost by increasing rates of application of fertilizer on principal cash and feed crops. They are then in a position to invest in soil conservation and other improvements that are needed when shifting acreage from surplus crops to other uses.

Modern chemical fertilizers include one or more of the three elements that are most important in plant nutrition: nitrogen , phosphorus , and potassium . Of secondary importance are the elements sulfur, magnesium, and calcium.

Most nitrogen fertilizers are obtained from synthetic ammonia ; this chemical compound (NH 3 ) is used either as a gas or in a water solution, or it is converted into salts such as ammonium sulfate, ammonium nitrate , and ammonium phosphate, but packinghouse wastes, treated garbage, sewage, and manure are also common sources of it. Because its nitrogen content is high and is readily converted to ammonia in the soil, urea is one of the most concentrated nitrogenous fertilizers. An inexpensive compound, it is incorporated in mixed fertilizers as well as being applied alone to the soil or sprayed on foliage . With  formaldehyde  it gives methylene-urea fertilizers, which release nitrogen slowly, continuously, and uniformly, a full year’s supply being applied at one time.

Phosphorus fertilizers include calcium phosphate derived from phosphate rock or bones. The more soluble superphosphate and triple superphosphate preparations are obtained by the treatment of calcium phosphate with sulfuric and phosphoric acid , respectively. Potassium fertilizers, namely potassium chloride and potassium sulfate, are mined from potash deposits. Of commercially produced potassium compounds, almost 95 percent of them are used in agriculture as fertilizer.

Mixed fertilizers contain more than one of the three major nutrients—nitrogen, phosphorus, and potassium. Fertilizer grade is a conventional expression that indicates the percentage of plant nutrients in a fertilizer; thus, a 10–20–10 grade contains 10 percent nitrogen, 20 percent phosphoric oxide, and 10 percent potash. Mixed fertilizers can be formulated in hundreds of ways.

Organic fertilizers and practices

The use of manure and compost as fertilizers is probably almost as old as agriculture. Many traditional farming systems still rely on these sustainable fertilizers, and their use is vital to the productivity of certified organic farms , in which synthetic fertilizers are not permitted.

Among sources of organic matter and plant nutrients, farm manure has been of major importance. Manure is understood to mean the refuse from stables and barnyards, including both excreta and straw or other bedding material. Large amounts of manure are produced by livestock ; such manure has value in maintaining and improving soil because of the plant nutrients, humus , and organic substances contained in it.

Due to the potential for harbouring human pathogens, the USDA National Organic Standards mandate that raw manure must be applied no later than 90 or 120 days before harvest, depending on whether the harvested part of the crop is in contact with the ground. Composted manure that has been turned five times in 15 days and reached temperatures between 55 and 77.2 °C (131 and 171 °F) has no restrictions on application times. As manure must be managed carefully in order to derive the most benefit from it, some farmers may be unwilling to expend the necessary time and effort. Manure must be carefully stored to minimize loss of nutrients, particularly nitrogen. It must be applied to the right kind of crop at the proper time. Also, additional fertilizer may be needed, such as phosphoric oxide, in order to gain full value of the nitrogen and potash that are contained in manure.

Manure is fertilizer graded as approximately 0.5–0.25–0.5 (percentages of nitrogen, phosphoric oxide, and potash), with at least two-thirds of the nitrogen in slow-acting forms. Given that these nutrients are mostly in an unmineralized form that cannot be taken up by plants, soil microbes are needed to break down organic matter and transform nutrients into a bioavailable “mineralized” state. In comparison, synthetic fertilizers are already in mineralized form and can be taken up by plants directly. On properly tilled soils, the returns from synthetic fertilizer usually will be greater than from an equivalent amount of manure. However, manure provides many indirect benefits. It supplies humus, which improves the soil’s physical character by increasing its capacity to absorb and store water, by enhancement of aeration, and by favouring the activities of lower organisms. Manure incorporated into the topsoil will help prevent erosion from heavy rain and slow down evaporation of water from the surface. In effect, the value of manure as a mulching material may be greater than is its value as a source of essential plant nutrients.

In reasonably humid areas the practice of green manuring can improve yield and soil qualities. A green manure crop is grown and plowed under for its beneficial effects, although during its growth it may be grazed. These green manure crops are usually annuals , either grasses or legumes , whose roots bear nodule bacteria capable of fixing atmospheric nitrogen. Among the advantages of green manure crops are the addition of nitrogen to the soil, an increase in general fertility, a reduction of erosion , an improvement of physical condition, and a reduction of nutrient loss from leaching. Disadvantages include the chance of not obtaining satisfactory growth; the possibility that the cost of growing the manure crop may exceed the cost of applying commercial nitrogen; possible increases in disease , insect pests, and nematodes (parasitic worms); and possible exhaustion of soil moisture by the crop.

Green manure crops are usually planted in the fall and turned under in the spring before the summer crop is sown. Their value as a source of nitrogen, particularly that of the legumes, is unquestioned for certain crops such as potatoes , cotton , and corn (maize); for other crops, such as peanuts (groundnuts; themselves legumes), the practice is questionable.

Compost is used in agriculture and gardening primarily as a soil amendment rather than as fertilizer, because it has a low content of plant nutrients. It may be incorporated into the soil or mulched on the surface. Heavy rates of application are common.

Compost is basically a mass of rotted organic matter made from waste plant residues. Addition of nitrogen during decomposition is usually advisable. The result is a crumbly material that when added to soil does not compete with the crop for nitrogen. When properly prepared, it is free of obnoxious odours. Composts commonly contain about 2 percent nitrogen, 0.5 to 1 percent phosphorus, and about 2 percent potassium. The nitrogen of compost becomes available slowly and never approaches that available from inorganic sources. This slow release of nitrogen reduces leaching and extends availability over the whole growing season . Composts are essentially fertilizers with low nutrient content, which explains why large amounts are applied. The maximum benefits of composts on soil structure (better aggregation, pore spacing, and water storage) and on crop yield usually occur after several years of use.

In practical farming, the use of composted plant residues must be compared with the use of fresh residues. More beneficial soil effects usually accrue with less labour by simply turning under fresh residues; also, since one-half the organic matter is lost in composting, fresh residues applied at the same rate will cover twice the area that composted residues would cover. In areas where commercial fertilizers are expensive, labour is cheap, and implements are simple, however, composting meets the need and is a logical practice.

Sewage sludge, the solid material remaining from the treatment of sewage, is not permitted in certified organic farming, though it is used in other, nonorganic settings. After suitable processing, it is sold as fertilizer and as a soil amendment for use on lawns, in parks, and on golf courses. Use of human biosolids in agriculture is controversial, as there are concerns that even treated sewage may harbour harmful bacteria, viruses, pharmaceutical residues, and heavy metals.

Liming to reduce soil acidity is practiced extensively in humid areas where rainfall leaches calcium and magnesium from the soil, thus creating an acid condition. Calcium and magnesium are major plant nutrients supplied by liming materials. Ground limestone is widely used for this purpose; its active agent, calcium carbonate , reacts with the soil to reduce its acidity. The calcium is then available for plant use. The typical limestones, especially dolomitic, contain magnesium carbonate as well, thus also supplying magnesium to the plant.

Marl and chalk are soft impure forms of limestone and are sometimes used as liming materials, as are oyster shells. Calcium sulfate ( gypsum ) and calcium chloride, however, are unsuitable for liming, for, although their calcium is readily soluble , they leave behind a residue that is harmful. Organic standards by the European Union and the U.S. Food and Drug Administration restrict certain liming agents; burnt lime and hydrated lime are not permitted for certified organic farms in the U.S., for example.

Lime is applied by mixing it uniformly with the surface layer of the soil. It may be applied at any time of the year on land plowed for spring crops or winter grain or on permanent pasture. After application, plowing, disking, or harrowing will mix it with the soil. Such tillage is usually necessary, because calcium migrates slowly downward in most soils. Lime is usually applied by trucks specially equipped and owned by custom operators.

Fertilizers may be added to soil in solid, liquid, or gaseous forms, the choice depending on many factors. Generally, the farmer tries to obtain satisfactory yield at minimum cost in money and labour.

Manure can be applied as a liquid or a solid. When accumulated as a liquid from livestock areas, it may be stored in tanks until needed and then pumped into a distributing machine or into a sprinkler irrigation system. The method reduces labour, but the noxious odours are objectionable. The solid-manure spreader, which can also be used for compost, conveys the material to the field, shreds it, and spreads it uniformly over the land. The process can be carried out during convenient times, including winter, but rarely when the crop is growing.

Application of granulated or pelleted solid fertilizer has been aided by improved equipment design. Such devices, depending on design, can deposit fertilizer at the time of planting, side-dress a growing crop, or broadcast the material. Solid-fertilizer distributors have a wide hopper with holes in the bottom; distribution is effected by various means, such as rollers, agitators, or endless chains traversing the hopper bottom. Broadcast distributors have a tub-shaped hopper from which the material falls onto revolving disks that distribute it in a broad swath. Fertilizer attachments are available for most tractor-mounted planters and cultivators and for grain drills and some types of plows. They deposit fertilizer with the seed when planted, without damage to the seed, yet the nutrient is readily available during early growth. Placement of the fertilizer varies according to the types of crops; some crops require banding above the seed, while others are more successful when the fertilizer band is below the seed.

The use of liquid and ammonia fertilizers is growing, particularly of anhydrous ammonia, which is handled as a liquid under pressure but changes to gas when released to atmospheric pressure . Anhydrous ammonia, however, is highly corrosive, inflammable, and rather dangerous if not handled properly; thus, application equipment is specialized. Typically, the applicator is a chisel-shaped blade with a pipe mounted on its rear side to conduct the ammonia 13 to 15 cm (5 to 6 inches) below the soil surface. Pipes are fed from a pressure tank mounted above. Mixed liquid fertilizers containing nitrogen, phosphorus, and potassium may be applied directly to the soil surface or as a foliar spray by field sprayers where close-growing crops are raised. Large areas can be covered rapidly by use of aircraft, which can distribute both liquid and dry fertilizer.