1 Introduction

With the increasing interest in using renewable energy, the production and subsequent use of biomass energy is seen as an important source. An established, robust technique for biomass energy production is the anaerobic digestion of organic matter (OM), which was shown to solve the environmental problem of excess raw materials and meanwhile contribute to climate change mitigation (Ragauskas et al. 2006). It was predicted that up to 25 % of all biomass energy in the future would comprise biogas (Nielsen and Oleskowicz-Popiel 2007).

Livestock residues provide one well-functioning substrate option for anaerobic digestion. In China, 9166 t of these residues was produced in 2002 (Li et al. 2002) and 10,666 t are predicted to be produced in 2020 (Galloway et al. 2008). However, the intensification of biogas production will produce substantial increases in the volumes of digestate, the disposal of which poses a problem (Galvez et al. 2012). The sustainability of the biogas chain would be greatly improved if a suitable method of utilizing the digestate was developed.

Biogas slurry (BS), the liquid fraction of the digestate, was found to contain substantial organic carbon (C) and crop nutrients that were attractive as fertilizers, to return nutrients to soil ecosystems (Svensson et al. 2004; Odlare et al. 2011). The soil application of BS may represent an effective way to tackle the widespread loss of soil organic C (SOC) (Galvez et al. 2012), which has, for example, occurred in regions of Jiangxi Province, southern China. This could benefit crop growth, if integrated with proper agricultural management (Holm-Nielsen et al. 2009).

Since the invention of the Haber–Bosch process, higher grain yields worldwide have relied on the intensive use of chemical fertilizers (CFs) in agriculture (Erisman et al. 2008; Abubaker et al. 2012). The majority of soil in the subtropical area of southern China has been subjected to the disorderly and massive use of CFs since the 1980s. As a consequence, regionally, the fertilizer uptake efficiency has been reduced, so the CFs applied are wasted, the SOC concentration has decreased, and water eutrophication has occurred (Zhang and Horn 2001; Huang et al. 2010). The application of BS has the potential to solve the above problems, as the BS containing high SOC and nutrient concentrations could partly substitute the overuse of CFs (Insam et al. 2015).

Soil application of BS has been shown to positively impact the soil–plant ecosystems. For instance, Tiwari et al. (2000) showed that a BS treatment resulted in substantially higher soil microbial biomass C (MBC) after wheat harvest in the field, and cumulative CO2 evolution after 20 days of laboratory incubation, compared with a non-amended control. Although Abubaker et al. (2012) found that soil fertilized with biogas residues had similar biomass yields, the treatment increased the N mineralization capacity and potential ammonium oxidation rates, in comparison with CF-only treatment.

Since stable C is the main constituent of humus, BS might be a potential source of SOC (Terhoeven-Urselmans et al. 2009). Limitations associated with BS and extensive use of CF must be immediately addressed (Zhang and Horn 2001; Huang et al. 2010; Abubaker et al. 2012; de la Fuente et al. 2013). However, most studies of BS application have been performed in laboratories, under controlled conditions (Abubaker et al. 2012; de la Fuente et al. 2013). The effects of BS on soil processes in field situations are relatively poorly understood. In particular, there has been little research into the soil fertilizing effect of P in BS–CF combinations, compared to CF only treatments (Li et al. 2014).

The objective of the present study was to evaluate and compare the fertilizing performance of BS–CF combinations against that of no CF or BS, and CF-only treatments, in terms of peanut grain yield, soil nutrients, C storage, and microbial activity. The optimal rate of BS application was determined for a regional soil (Ultisol) in Jiangxi Province, southern China.

2 Materials and methods

2.1 Field experiment

2.1.1 Study site and BS collection

The experiment was conducted during April–August 2013 in an experimental peanut field, located in the Luwang village of YuJiang County, Jiangxi Province, southern China (116° 5ʹ E, 28° 12ʹ N). This region has a typical subtropical monsoon climate with annual precipitation of 1795 mm, annual evaporation of 1318 mm, and a mean annual temperature of 17.6 °C. Regionally, the predominant soil, derived from the Quaternary red clay, is classified as red soil (Genetic Soil Classification of China (Zhou et al. 2013)), and Ultisol (Soil Taxonomy System of the USDA (Zhang and Peng 2006)). The physical and chemical properties of the field soil (0–20 cm depth) were as follows: pH 4.94 (H2O/soil = 2.5:1), clay 32.9 %, silt 61.0 %, sand 6.1 %, organic C (OC) 7.06 g kg−1, total nitrogen (TN) 0.83 g kg−1, total phosphorous (TP) 0.51 g kg−1, NH4 +-N 16.15 mg kg−1, and NO3 −-N 3.90 mg kg−1. Peanut crop and fallow had been alternated in the field during the previous 5 years.

The BS was collected directly from a middle-scale pig farm with a biogas plant that included a well-mixed BS storage facility. The main feedstock of the biogas plant reactor was a mixture of pig manure and urine. The operation temperature ranged from 35 to 40 °C, and the minimum retention time was 1 year. The main characteristics of the BS are shown in Table 1.

Table 1 The main characteristics of the biogas slurry used in this study
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2.1.2 Experimental design

The field experiment was arranged in a single-factor randomized complete block design, with three replicates of each treatment. Each plot was 12.5 m × 4.8 m. Five treatments were applied, in which the BS was used as a substitute, to the CFs, of the source of TN, to varying degrees: T1, control (no CF or BS); T2, CF only; T3, 15 % BS–TN plus 85 % CF–TN; T4, 30 % BS–TN plus 70 % CF–TN; and T5: 45 % BS–TN plus 55 % CF–TN. Thus, the quantities of BS applied in each treatment were calculated based on its TN concentration, and the other macronutrients (phosphorous [P], potassium [K], and additional nitrogen [N]) were adjusted accordingly with CFs. Urea (46 % N), calcium magnesium phosphate (12 % P2O5), and potassium chloride (60 % K2O) were selected as the CF sources of inorganic N, P2O5, and K2O, respectively. For the CF treatment and the BS substitution treatments, the same final quantities of N, P2O5, and K2O were applied (N/P2O5/K2O, 120:90:135 kg ha−1). The actual quantities of the BS applied were 6.41, 12.81, and 19.22 × 104 L ha−1, respectively, for T3, T4, and T5. The organic C and nutrient input by the CFs and BS within each treatment are shown in Table 2.

Table 2 The amounts of organic carbon and nutrient input by the chemical fertilizers and biogas slurry in each treatment for the field and incubation experiments
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The 0–20-cm soil layer was plowed before sowing on April 5, 2013, and then the appropriate quantities of BS for each treatment were manually spread using an open-head drum and ladle on April 6 and 7. After that, the CFs (urea, calcium magnesium phosphate, and potassium chloride) were mixed and then applied manually in sequence on April 8, before the soil layer was plowed for a second time on April 9. Thus, the BS and CFs were used as basal dressings. Two peanut seeds were planted in each hole to achieve a planting density of 140,000 plants per hectare (equivalent to 840 plants per treatment plot) on April 10. Line and row distances of 40 and 20 cm, respectively, were maintained between the holes. Field and crop management practices were conducted in accordance with local agricultural practices. The peanuts were harvested on August 10.

2.1.3 Soil and plant sampling

Five random soil subsamples (0–20 cm) were collected from each of the treatment plots and then mixed together to form a single sample, at the seedling, flowering, pod production, and harvesting stages of the peanut plants. At the same time points, five plant samples were collected (including the roots) from each plot. Once in the laboratory, all visible roots and crop residues were removed from the soil samples. Then, the composite soil samples were divided into two parts: One portion was air-dried at room temperature, ground, and passed through a 0.25-mm sieve, prior to analysis of the soil N and P concentrations, and the other portion was ground directly (without drying) and passed through a 2-mm sieve in preparation for the MBC, microbial biomass N (MBN), and enzyme activity analyses. The soil and plant sample portions were stored at 4 °C and room temperature, respectively, until analysis.

2.2 C mineralization experiment

The soil used in this laboratory incubation trial was sampled from the 0–20-cm soil layer of the control (no CF/BS) treatment plots. In the laboratory, the soil was air-dried and then passed through a 2-mm sieve before use. The incubation trial was performed using 100 g of soil (dry weight, DW) in 500-mL polypropylene jars. Empty polypropylene jars were used to obtain background air values. The relative quantities of BS applied for each treatment of the incubation trial were the same as those applied for the field experiment: T1, T2, T3, T4, and T5 treatments received 0, 0, 4, 8, and 12 mL BS 100 g−1 soil (DW) according to Table 2, respectively. The BS and CFs were thoroughly mixed with the soil prior to the experiment, and the soil was preconditioned to 60 % of its water-holding capacity with deionized water.

The treated soils were incubated under aerobic conditions in darkness at 26 ± 0.5 °C for 70 days. The moisture levels of the soils were checked three times every week, by weighing the soil, and deionized water was added when necessary to maintain constant moisture levels. CO2 evolution from the soil was measured at 2, 4, 7, 10, 14, 18, 21, 28, 35, 42, 49, 56, 63, and 70 days of incubation.

2.3 Analytical methods

The biomass (DW) of the peanut plants at the four growth stages (i.e., seedling, flowering, pod production, and harvesting) was determined by cutting the plants into small pieces (Abubaker et al. 2012) and subsequent drying at 105 °C for 30 min and 75 °C for 10 h. The overall biomass was derived by multiplying the individual plant biomass by the plant density. Grain yield (DW) was measured after harvest and standardized to tons per hectare. The DW of grain yield and biomass was determined by the standard baker oven method (Lu 1999). Each dried plant sample was ground and sieved with a 2-mm sieve. Then, the N concentration was measured colorimetrically, after Kjeldahl digestion (Nishikawa et al. 2012).

The electrical conductivity (EC) and pH of the BS were directly measured using a conductivity and pH meter, respectively. NH4 + and NO3 − were extracted from the soil by adding 1 mol L−1 KCl solution at a 1:10 (w/v) ratio. The extractable soil NH4 + was measured through a modified colorimetric method, based on the Berthelot reaction (Sommer et al. 1992). The concentrations of extractable NO3 − were determined by absorbance at 220 nm. The values obtained were subtracted from the corresponding values at 275 nm, which were attributed to OM (Galvez et al. 2012). The total magnesium (Mg), calcium (Ca), and metals in the BS were analyzed according to Lu (2000).

For soil analysis, MBC and MBN were determined using the fumigation–K2SO4 extraction method (Vance et al. 1987; Joergensen 1996), with an automatic analyzer used for liquid samples. Values were subsequently calculated according to the method of Wu et al. (1990). TP was determined through the colorimetric method (Van Veldhoven and Mannaerts 1987). OM concentration was calculated from loss on ignition at 500 °C for 24 h. Total organic C (TOC) was calculated by dividing the OM concentration by 1.72 (Nelson and Sommers 1982). TN and total K (TK) were determined using the potassium persulfate oxidation–ultraviolet spectrophotometer and flame photometer methods, respectively (Lu 1999). Available P (AP) was measured colorimetrically, after NaHCO3 extraction (Watanabe and Olsen 1965). Soil dehydrogenase and urease activities were determined using the methods of Le et al. (1964) and Perez-Mateos and Gonzalez-Carcedo (1988), respectively.

To determine the CO2 evolution from the amended soil in the incubation trial, NaOH solution was placed in a small beaker inside the 500-mL polypropylene jars. The NaOH solution was titrated with 0.05 M HCl and excess BaCl2, to precipitate the carbonates (de la Fuente et al. 2013).

2.4 Calculations and statistical analyses

The DW results are expressed on oven dry weight basis and represent the means of three replicates. The efficiency of the BS–CF treatments for plant N recovery was quantified by calculating the mean of the relative N fertilizer values (RNFVs), on the basis of the estimated functions previously reported (Sieling et al. 2013). The RNFVs were obtained as the ratio of the apparent N recovery (ANR, %) of each respective BS–CF treatment to that of the CF only treatment (Sieling et al. 2013); (Schröder et al. 2005).

$$ \begin{array}{c}\hfill \mathrm{N}\mathrm{A}\mathrm{A}\left(\mathrm{kg}\kern0.5em {\mathrm{ha}}^{\hbox{-} 1}\right)=\mathrm{N}\kern0.5em \mathrm{concentration}\kern0.5em \mathrm{of}\kern0.5em \mathrm{plant}\left(\mathrm{g}\kern0.5em {\mathrm{kg}}^{\hbox{-} 1}\right)\times \mathrm{D}\mathrm{W}\kern0.5em \mathrm{biomass}\left(\mathrm{kg}\kern0.5em {\mathrm{ha}}^{\hbox{-} 1}\right)/1000\hfill \\ {}\hfill \mathrm{A}\mathrm{N}\mathrm{R}=\left(\mathrm{N}\mathrm{A}\mathrm{A}\kern0.5em \mathrm{of}\kern0.5em \mathrm{fertilizer}\kern0.5em \mathrm{treatment}-\mathrm{N}\mathrm{A}\mathrm{A}\kern0.5em \mathrm{of}\kern0.5em \mathrm{control}\right)/\mathrm{total}\kern0.5em \mathrm{N}\kern0.5em \mathrm{amount}\kern0.5em \mathrm{applied};\ \mathrm{and}\hfill \\ {}\hfill \mathrm{RNFV}={\mathrm{ANR}}_{\mathrm{BS}\hbox{-} \mathrm{C}\mathrm{F}\kern0.5em \mathrm{combination}}/{\mathrm{ANR}}_{\mathrm{CF}}, \hfill \end{array} $$

Mineralization of the OC contained in the soil and BS was calculated as the difference between the CO2 evolved from the BS–CF treatments and the control (no CF/BS) treatment and expressed as the percentage of the TOC concentration (%TOC) contained in the soil and BS (natural and added) (de la Fuente et al. 2013).

The results of the C mineralization in soil were fitted to a first-order kinetic model, according to the following equation (de la Fuente et al. 2013):

$$ {C}_{\mathrm{m}}={C}_0\left(1-{e}^{-kt}\right), $$

where C m is the mineralized C obtained after t days of incubation; C 0 is the potentially mineralizable C; k is the decomposition rate constant for the TOC contained in the soil and BS (day−1); and t is the incubation time.

Statistical analyses were performed with SPSS 13.0 for Windows (SPSS Inc., Chicago, IL, USA). One-way analysis of variance (ANOVA), followed by least significant difference (LSD) pairwise comparisons, was performed to determine the significance of differences among treatments (a significance level of P < 0.05 was used). Linear regressions and coefficients of determination (R 2) were used to describe the relationship between the BS–TN input and peanut grain yield.

3 Results

3.1 Peanut yield, biomass, and soil nutrients

The effects of the different treatments on the yields of the peanut show that the BS–CF combination treatments (T3–T5) had higher yields than the treatment which only used CFs (T2) (Fig. 1a). Of the BC–CF combination treatments, T4 produced the largest yield, with significant difference from T3 and T5. The regression analysis indicated that the relationship between the input of TN by the BS and grain yield conformed to the linear-quadratic equation: y = −1.14x 2 + 59.1x + 2988 (R 2 = 0.98, P < 0.01). In other words, the yield (in terms of DW) was highest at a fertilization rate of 31.2 kg BS–TN ha−1, close to the fertilization rate of T4 (36 kg BS–TN ha−1). Likewise, the total biomass showed a significant response to BS–TN input (Fig. 1b). In T4, the total biomass reached 4.0, 10.6, and 11.9 t ha−1 at the flowering, pod production, and harvesting stages, respectively, which were higher than those in other treatments.

Fig. 1
figure 1

The effects of the biogas slurry (BS) and chemical fertilizer (CF) treatments on a the peanut grain yield at harvest, and b the total peanut biomass at seedling, flowering, pod production, and harvesting growth stages

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The NAAs of the plants in the BS–CF combination treatments (T3–T5; 224.5–248.7 kg ha−1) were higher than those subjected to the control treatment (T1; 153.4 kg ha−1) and CF-only treatment (T2; 200.5 kg ha−1) (Table 3). Additionally, T5 led to higher NAA than T3 (248.7 vs. 224.5 kg ha−1). With the promotion of plant N accumulation due to increased BS–TN input, T3 to T5 produced higher ANRs of the fertilizer applied (51.8–62.0 %) compared with those observed for T2 (38.7 %), and the difference was significant in terms of T4. The resultant RNFV of T3 to T5 ranged from 1.3 to 1.5.

Table 3 Biomass nitrogen accumulation amount (NAA) in the peanut crop, apparent nitrogen recovery (ANR), and relative nitrogen fertilizer value (RNFV) observed for each treatment
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At the seedling stage of the peanut plants, T2, T3, and T4 led to similar soil TN concentrations, which were higher than those produced by T1 and the highest BS–TN treatment T5 (Table 4). The BS–CF treatments (T3–T5) showed significant lower soil TN concentrations than those produced by T2, but were higher than T1 at the flowering stage. Higher soil TN concentrations occurred in T4 or T5 compared with the other treatments at the following two stages. In terms of soil NH4 +-N concentrations, T3 to T5 were lower than T2 at the seedling stage, whereas T4 was higher than other treatments at the harvesting stage. Additionally, T4 led to the highest soil NO3 −-N concentrations across all the four stages, although the differences were not necessarily significant. Overall, T4 and T5 had higher average mineral N (NO3 − + NH4 +) concentrations (24.64–25.91 mg kg−1) than T2 (21.28 mg kg−1) during the whole peanut growth period.

Table 4 Amount of total nitrogen and available nitrogen in the field soils of each treatment at different growth stages of peanut plants
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Additionally, soil C/N of ratio closest to the known optimum ratio (25:1) was observed at the flowering (31.6:1), pod production (33.3:1), and harvesting (23.7:1) growth stages, in T4 (36 kg BS–TN ha−1), compared to all other treatments (except T1; Table 7).

Soil TP and AP concentrations were generally highest in T4 (although not necessarily significantly), except the higher AP value in T5 at flowering. The soil in T3, T4, and T5 had higher TP concentrations than that in T2 at harvest, but not for AP (Table 5).

Table 5 Amount of total and available phosphorus in the field soils of each treatment at different growth stages of peanut plants
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3.2 C mineralization

The amount of CO2-C (expressed as mg CO2-C kg−1 soil day−1) that evolved from the soil throughout the incubation experiment showed a similar pattern among all treatments (Fig. 2a). The amount of CO2-C that evolved from the soil of T3 to T5 was higher than that from T1, from the beginning to the end of the incubation period. After 14 days of incubation, the amount of CO2-C that evolved from T3 to T5 was higher than that from T2. The CO2-C production rates decreased rapidly after the first week of incubation and became fairly constant from day 18 until the end of the incubation period, as the easily mineralizable OM sources were exhausted.

Fig. 2
figure 2

The a daily production of CO2-C and b cumulative mineralization of carbon in the soils of each treatment, during the laboratory incubation trial

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The cumulative accumulation of total CO2-C that evolved from the soils during the 70-day incubation period was greatly affected by the different treatments (Fig. 2b), demonstrated by expressing the results as the %TOC of the OM mineralized that was originally from the BS and soil (added and natural, respectively). At the end of the incubation period, T4 showed the lowest percentage of mineralized C (36.10 % of the TOC from the BS and soil), followed by T3 (39.03 %), T5 (39.82 %), and T2 (39.96 %).

Data from the C mineralization in the soils were fitted to a first-order kinetic model, where the potentially mineralizable C (C 0) ranged from 52.45 to 82.37 % (Table 6). The C 0 in the soils of T2–T5 were 11.99–29.92 % higher than the control (T1). Moreover, the effect of BS increased the C 0 in T3 to T5 from 0.34 to 17.93 % compared with that in T2. However, the decomposition rate of OC (k) was lower when BS was added into in T3 to T5, compared with that in T2.

Table 6 Parameters of the first-order kinetic model (C m = C 0 (1 − e −kt)), used to describe the carbon mineralization in the soils of the different treatments during the incubation experiment
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3.3 Soil microbial biomass and enzymatic activity

Both of the high BS treatments (T4 and T5) led to higher MBC and MBN levels in the soil than the CF only treatment (T2), across all four plant stages (Fig. 3a, b); the results were significantly different among all the treatments. The MBC and MBN of T4 increased at the flowering stage of the peanut plants and then sharply decreased at the pod production and harvesting stages, but the values were still higher than those observed in the other treatments. All the treatments conformed the trend that the MBC and MBN firstly increased before the flowering stage and subsequently decreased.

Fig. 3
figure 3

Changes in the amount of soil microbial biomass a carbon (MBC), and b nitrogen (MBN) at the seedling, flowering, pod production, and harvesting stages of the peanut plants subjected to each treatment

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Similar to the results for the MBC and MBN, T4 resulted in a rapid increase in soil urease and dehydrogenase activities at the pod production and harvesting stages (Fig. 4a, b). The activities of the two enzymes firstly increased from the seedling to the pod production stages and then decreased thereafter. Both enzymes exhibited the highest activities in the soils of T4, showing significant difference from those in T2 at the pod production and harvesting stages (Fig. 4a, b).

Fig. 4
figure 4

Changes in the a soil dehydrogenase and b urease activity at the seedling, flowering, pod production, and harvesting stages of the peanut plants subjected to each treatment

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4 Discussion

4.1 Effect of BS application on peanut yield and biomass

The present study has indicated that fertilization of soil with different ratios of BS and CF produces substantially higher grain yields in peanut, than by fertilizing with only CFs or no CF/BS (Fig. 1a). In particular, fertilization with 36 kg BS–TN ha−1 (T4) increased the grain yields in comparison with the other BS–CF combination treatments (T3 and T5), and a highly significant correlation was observed between BS–TN input and grain yield. A similar effect was observed in rice that a 10 % yield increase occurred with a BS–CF combination that contained 50 % BS–TN (Zuo 2008). Moreover, the combination of BS–CF improved the yields in rapeseed, compared to a CF-only treatment (Zhang et al. 2007). The yield increases in the present study may be attributed to the high biomass levels of the peanut plants at the four stages of growth (Fig. 1b). This hypothesis is supported by a positive correlation previously found between grain yield and biomass in summer maize, which indicates that biomass is the basis of yield formation (Zhao et al. 2006).

The differences in biomass between the treatments in the present study indicated that the accumulation of nutrients in the plants varied, because crop nutrient accumulation promotes biomass accumulation (Zhao et al. 2006). This was found true for the NAAs in this study (Table 3). The application of BS promoted N absorption (NAA) in the peanut plants, and a high ratio of NH4 +-N to TN (0.96) was observed (Table 1), thus resulting in a higher ANR of the fertilizer applied. Consequently, the N fertilizer value observed for the BS–CF treatments (T3–T5) was higher than that for the CF-only treatment (T2), even though the same amounts of TN were applied. Additionally, the extra micronutrients contained in the BS (e.g., S, Ca, and Mg; Table 1) may have promoted peanut growth. Ultimately, it is clear that the addition of BS enhanced the peanut grain yields.

4.2 Effect of BS application on soil nutrient availability

N is a critical nutrient in all plant-based systems. It is transformed by mineralization, nitrification, denitrification, and immobilization, as well as leaching and ammonia volatilization (Insam et al. 2015). The nature of N transformation mainly depends on the form of deposited N, the soil chemistry, and the land use strategy upon entering the soil (Bardgett and Wardle 2010; Insam et al. 2015). In regard of the introduction of N into the soil via the BS, the different amounts of BS added either promoted or suppressed N mineralization, compared to the CF only treatment (Table 4), dependent on the stage of growth of the peanut plants.

The dissolved OC present, and the corresponding OC/TN ratio (C/N) of the dissolved substances, can be considered as the most reliable indicators of biological activity (Alburquerque et al. 2012). Although the same amounts of N, P2O5, and K2O were added in each treatment, the application of 36–54 kg BS–TN ha−1 (T4, T5) led to the highest soil concentrations of TN (1.02–1.15 and 1.00–1.06 g kg−1) at the pod production and harvesting stages and average mineral N (NO3 − + NH4 +) concentrations (24.64–25.91 mg kg−1) during the whole peanut growth period, respectively. This result may be attributed to the organic N added by the BS (Table 2). The soil itself was another major source of N and promoted organic N mineralization after suitable BS–CF application, which likely increased the soil microbial activities (Möller and Müller 2012).

From another aspect, the different amounts of mineral N could have occurred because of different levels of the chemical composition in the BS–CF combination treatments (Diacono and Montemurro 2010). Thus, even if the amounts of TN input into the soil were the same among the treatments, the different levels of organic N mineralization led to variations in the soil TN and mineral N concentration. It seems that 36 kg BS–TN ha−1 (T4) comprised the most appropriate BS–CF combination, because this treatment promoted the concentrations of soil TN and mineral N most effectively. It favored the absorption of N by the peanut plant roots, promoting the growth and N accumulation of the plants. Corresponding to this, the ANR and RNFV (1.3–1.5) of the BS were higher in T4 (36 kg BS–TN ha−1). In fact, the RNFV of the T4 BS–CF combination was higher than pure digestate (0.87) and pig slurry (0.98) (Sieling et al. 2013).

P is an important plant macronutrient, as a constituent of adenylates, nucleic acids, and phospholipids (Insam et al. 2015). The 36 kg BS–TN ha−1 treatment (T4) promoted (not necessarily significantly) the TP and AP concentrations in the soils, across the four growth stages of the peanut plants. This positive effect of T4 may be attributed to the addition of BS affecting soil P availability and plant P nutrition. P can either be directly added by inorganic and organic P compounds, or indirectly, by influencing soil microbial activities (as a consequence of changes to the OC supply; Table 2), and enzyme activities related to P transformation (i.e., alkaline phosphatase) (Insam et al. 2015). The results from the present study were consistent with those obtained by Bachmann et al. that emphasize the potential of biogas residues as valuable and readily available P sources for crops (Bachmann et al. 2014).

Additionally, the C/N ratio is a crucial factor that influences short-term N and P availability and therefore is beneficial to crop growth (Möller et al. 2008; Fouda et al. 2013). In the present work, the C/N ratio closest to the known optimum ratio (25:1) was observed at the flowering, pod production, and harvesting (23.7:1) growth stages, in T4 (36 kg BS–TN ha−1), compared to that in all other treatments (except T1; Table 7). Such an optimum C/N ratio contributed to the highest N and P concentrations at these growth stages (Tables 4 and 5).

Table 7 Organic carbon/total nitrogen (C/N) ratio in the soil of each treatment at different growth stages of peanut plants
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4.3 Effect of BS application on soil microbial activity

Beyond the N, P, and K added by the BS and CFs, the mineralization of OM, contained in the BS and naturally in the soil, was another important nutrient source. As an indicator of soil microbial activity and OM decomposition that occurred in each treatment, the CO2 efflux was measured through a 70-day laboratory incubation experiment. The data from the C mineralization experiment demonstrated that the BS input increased the amount of potentially mineralizable C (C 0) but decreased the mineralization rate (k) (Table 5). This implies that anaerobic digestion converted the labile organic C to CH4 and CO2, and the organic C in the BS was more stable and less readily decomposed by soil microorganisms (De Neve et al. 2003).

Thus, although the amount of potentially mineralizable C (%TOC present in the BS and soil) increased with the application of BS, it seems that the additional mineralized C from the BS slowly degraded and would have been retained in the soil for a long time. Therefore, from a practical point of view, the application of BS benefitted the long-term maintenance of soil fertility and crop growth. These results agree with the findings of Tao et al. (2003), which indicated that the soil OM increased by 58.4 % after 6 years of applying a dressing residue.

The 36 kg BS–TN ha−1 treatment (T4) also resulted in a significant increase of microbial biomass (MBC and MBN, Fig. 3) and enzymatic activities (urease and dehydrogenase, Fig. 4), compared to other treatments at the flowering, pod production, and harvesting stages. This result is in agreement with similar studies, which investigated the soil application of bio-fuel by-products (Alotaibi and Schoenau 2011; Abubaker et al. 2012; Galvez et al. 2012). Similar results were also reported by Ros et al. (2006), who attributed the significant increase in microbial biomass that they observed to the higher availability of C substrates, which stimulated microbial growth.

Previously, the microbial biomass was found to be a much more sensitive indicator of changes in soil conditions than the total soil OC and nutrient concentrations (Powlson et al. 1987). It also played an important role in guaranteeing the capacity of soils to develop important agronomical and environmental functions, such as the transformation of organic C and nutrient cycling (Galvez et al. 2012). Considering these studies, a significant increase in microbial biomass concentration at the flowering, pod production, and harvesting stages in T4 indicated an improvement in the soil’s ecosystem functioning due to combined application of BS–CF at a suitable ratio.

As a member of the hydrolase enzyme family, urease catalyzes the hydrolysis of organic N and urea, to form ammonia and carbamate. This enzyme can therefore be regarded as a sensitive indicator of changes in the N turnover in soil (Balasubramanian and Ponnuraj 2010). In the present study, the addition of BS, with available substrate and nutrients (especially in T4), may have either increased the activity of the microorganisms degrading the organic N, or increased the urease activity, by promoting the growth of microbial species, or by stimulating enzyme synthesis in the microbial cells, respectively (Dilly and Nannipieri 2001). The increase in urease activity recorded in this study was consistent with the findings in another field study (Chen et al. 2015).

Moreover, dehydrogenase plays an essential role in the oxidizing capacity of soil microorganisms. Since this enzyme only exists in live microbial cells, dehydrogenase activity is an important indication of soil microbial activity (Chen et al. 2009). Therefore, the significant increase in soil dehydrogenase activity resulting from 36 kg BS–TN ha−1 treatment (T4), at the flowering, pod production, and harvesting stages, demonstrated an enhancement of soil microbial activities, associated with OM transformation and nutrient cycling.

5 Conclusions

This study has clearly demonstrated that the combination of BS and CFs, at an appropriate ratio, was superior to no CF/BS and CF only, in terms of promoting peanut grain yields, soil nutrients, C storage, and microbial activities in the red soil. The application of 36 kg BS–TN ha−1 led to the highest plant biomass at the flowering, pod production, and harvesting stages, which corresponded to the highest grain yields and plant N uptake efficiency, as well as the maximum N accumulation and recovery. Additionally, soil microbial biomass (C and N), urease, and dehydrogenase activities markedly increased following the integrated use of 36 kg BS–TN ha−1, at the flowering stage, with their maximum values observed at the flowering, pod production, and harvesting stages. Although the application of BS increased the potentially mineralizable C, the additional C seemed to slowly degrade, and so would be retained in the soil for a long time. The combined application of BS and CFs (e.g., 36 kg BS–TN ha−1), together with proper management techniques, may represent an effective practical substitution of CF use, to improve the quality and nutrient balance of amended soils. These results help to establish the suitable agronomic use of BS, which could reduce the consumption of CFs and thereby alleviate environmental pollution. Further studies that focus on the performance of the long-term field application of BS–CF combination treatments need to be performed to verify the present findings.