Shikha et al.

Carbon Research (2023) 2:10

https://doi.org/10.1007/s44246-023-00043-7

ORIGINAL ARTICLE Open Access

Effects of biochar and biofertilizer

on groundnut production: a perspective
for environmental sustainability in Bangladesh
Fouzia Sultana Shikha1†, Md Mashiur Rahman2*† , Naznin Sultana3, Md Abdul Mottalib4 and Monira Yasmin1

Abstract
Regular large-scale application of fertilizers, pesticides, and mulching can lead to soil health degradation and increase
negative environmental impacts, contributing significantly to greenhouse gas (GHG) emissions. Considering these
factors by applying biochar and biofertilizer (rhizobium inoculants) in groundnut production, a novel experiment was
conducted for increasing soil fertility, groundnut productivity, and soil carbon stock in Bangladesh’s Charland agro-
ecosystems. The two-year experiment involved seven treatments consisting of ­T1 (control), ­T2 (soil test based (STB)
fertilizer dose following fertilizer recommendation guide (FRG) 2018), ­T3 ((T2 minus nitrogen fertilizer) + biofertilizer),
­T4 ­( T3 + biochar), ­T5 ­( T2 + biochar), ­T6 (only biofertilizer), and ­T7 (only biochar). The result showed that the ­T4 treatment
had the highest nodule counts (78.17 ­plant−1), nodule weights (122.97 mg ­plant−1), root weight (1.47 g p ­ lant−1) and
−1
nut yields (2.30 t ­ha ), all of which were statistically identical compared to the other treatments. In addition, the ­T3
treatment had the highest recorded shoot weight (35.47 g ­plant−1), whereas the control ­T1 treatment had the low-
est (16.50 g p ­ lant−1) shoot weight. Results showed that biochar-based rhizobium inoculants increased nodulation,
root weight, shoot weight, nut yield and soil nutrient uptake in plant growth at all four stages (seedling, flowering,
pod formation and harvesting). The result revealed that biochar-based rhizobium inoculants modulated the abun-
dance of functional microbes through increased soil nitrification and reduced denitrification compared to the N-use
treatments. Moreover, this interactive system significantly improved soil ­NO3−, leading to an increase in N uptake,
thereby promoting plant growth and increasing nut yield. Considering all parameters, the soil amended biochar as a
carrier of rhizobium inoculants had the highest soil organic carbon (SOC) stock (1.76 t h ­ a−1), about 26% higher than
−1
other treatments, which saved a considerable amount of 6.6 kg ­CO2eq ­ha GHG emissions and aided in promoting
environmental sustainability towards climate-smart agriculture.

Highlights
1. A novel biochar-based biofertilizer (rhizobium inoculants) application in groundnut production has been proposed.

†
Fouzia Sultana Shikha and Md Mashiur Rahman contributed equally to this
work.
Handling Editor: Yilai Lou.
*Correspondence:
Md Mashiur Rahman
[email protected]
Full list of author information is available at the end of the article

© The Author(s) 2023. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which
permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the
original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or
other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line
to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory
regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this
licence, visit http://​creat​iveco​mmons.​org/​licen​ses/​by/4.​0/.
Shikha et al. Carbon Research (2023) 2:10 Page 2 of 15

2. The combined system’s impact helps uptake soil nutrients, improving plant growth, nut yield and soil organic car-
bon (SOC) stock.
3. Interactive impact of these two reduces the need for N fertilizer while also lowering GHG emissions by sequestering
SOC.
Keywords Biochar, Biofertilizer, Environmental sustainability, Groundnut production, Nitrification, Soil organic carbon
accumulation
Graphical Abstract

1 Introduction Layek et al. 2022). Moreover, biochar act as a rhizobium

Biochar can be quickly produced from wood or bio- bacteria carrier and has also been shown to change soil
mass, which has a carbon (C) content of about 50%, biological community composition (Hardy et al. 2019);
whereas biochar has a carbon content of about 70% to such changes might have positive impacts on nutrient
80% and its use in the soil may store more than 50% cycles (Steiner et al. 2008) or soil structure (Rillig and
of the C in a highly stable way (Qambrani et al. 2017; Mummey 2006), which would then indirectly improve
Panwar et al. 2019; Layek et al. 2022). For this reason, the plant growth, yield productivity (Warnock et al.
biochar has been proposed as a way to increase soil 2010), and soil organic matter (SOC) cycling (Kuzya-
fertility in agroecosystems as well as other ecosystem kov et al. 2009; Liang et al. 2010; Tender et al. 2021; Lin
services and sequester C to mitigate climate change et al. 2022). Nonetheless, nitrification, denitrification
(Woolf et al. 2010; Yeboah et al. 2020; Bellè et al. 2022; and methane oxidation (Yanai et al. 2007; Van Zwieten
Shikha et al. Carbon Research (2023) 2:10 Page 3 of 15

et al. 2012), C mineralization (Kuzyakov et al. 2009; meeting the growing oil requirements in recent years and
Liang et al. 2010), and nutrient transformations (Gun- ensuring nutritional security for a population of over 1.6
dale and DeLuca 2006) were all found to either increase million (Miah and Mondal 2017; Shakil 2022). Though
or decrease in the presence of biochar (Romero et al. nutritionally, groundnut seeds contain about 48–50%
2021). edible oil, 22–29% protein, and 20% carbohydrate, with
Biochar has been employed as a soil additive or an an average yield of 2.30 – 3.00 t ­ha−1 (Morshed Al et al.
inoculant carrier, like other inoculant carriers, for exam- 2002; Dun et al. 2019). Groundnut is cultivated on about
ple, Azotobacter, Bacillus, Clostridium, Blue-green algae, 32,000 ha of land, and the total groundnut production is
or Rhizobium, but little is understood in terms of their about 47,000 Mt in Bangladesh (Azad et al. 2020). Being a
mode of action, even as far as the relatively well-studied legume crop, groundnut improves soil quality by biologi-
rhizobia are concerned (Kumari et al. 2019; Van Beek cally fixing nitrogen without consuming non-renewable
et al. 2019; Wei et al. 2020). Biochar-type materials have energies and disturbing agroecological balance. Further-
long been suggested as inoculant carriers substituting for more, the economically vital part of the groundnut plant
the increasingly expensive, rare, greenhouse gas-releasing is the pod that encloses the seeds. From this point of
and non-renewable peat (Lehmann et al. 2010). Adding view, groundnut is an unpredictable crop due to under-
biochar-type residues from vegetation fires to soil signifi- ground pod development (Zaman et al. 1970). The size
cantly increased the nodulation of plants, enhancing soil and number of seeds per pod are essential criteria that
fertility and thereby led to yield productivity (Lehmann determine the market value of groundnut in general.
et al. 2011). Inoculation of legumes with biofertilizer (rhizobium
However, soil fertility decline and greenhouse gas bacteria) increased the nodule and nitrogen-fixing activ-
(GHG) emissions have been perceived as widespread ity of the plants (Argaw 2017). When inoculated with the
treating challenges globally (Hartemink 2006). Accord- proper strain of bacteria, legumes can supply up to 90%
ing to scientific reports, crop production contributed of their nitrogen. Comparably, the researcher reported
roughly 10–12% of world GHG emissions, while land that inoculation with rhizobium bacteria brings about
conversion from grassland and forest to croplands, soil, significant increases in all the growth and yield param-
and biomass carbon accounted for an additional 12 to eters than when not inoculated; biochar addition to
20%. For this reason, to overcome these bottlenecks, soil increases soil nutrient concentrations and micro-
biochar amendment has been identified as the optimum bial activity, leading to the development of plant growth
technique (Smith et al. 2015; Carlson et al. 2016; Meier (Sajid et al. 2011; Asante et al. 2020). The symbiotic
et al. 2020). The International Biochar Initiative (IBI) performance of legumes with rhizobia can be signifi-
defined biochar as a solid material obtained from the cantly enhanced by biochar-based rhizobial inoculants,
thermo-chemical conversion of biomass in an oxygen- reducing N fertilizer demand and thus promoting the
limited environment for use in sustainable environmental sustainability of crop production in any agroecosystems
and agricultural practices (International Biochar Initia- (Egamberdieva et al. 2018), including Charland agro-
tive 2015; Mulabagal et al. 2021). In recent days, biochar ecosystems. Legumes have symbiotic relationships with
has been gaining popularity owing to its capacity to miti- rhizobia and are known as the most efficient system for
gate climate change and helps to ensure environmental biological nitrogen fixation (Reckling et al. 2016).
sustainability due to its high carbon sequestration capac- Ghazi and Karnwal (2017) evaluated biochar pro-
ity (Liang et al. 2010; Lehmann et al. 2010; Rahman et al. duced from rice straw as a carrier material for rhizobia
2022). Besides, soil amendments that disintegrate slowly, and found evidence for improved colonization and sur-
such as compost and biochar, are another essential man- vival of bacterial inoculants. The biochar-based inoculant
agement approach for enhancing SOC stocks (Dignac increased root and shoot biomass, nodulation and nutri-
et al. 2017), resulting in reduced greenhouse gas (GHG) ent uptake (Egamberdieva et al. 2017; Tripti et al. 2017).
emissions to combat the climate change effect. In addi- Hence, biochar addition for the Charland agroecosystem
tion, biochar may have altered other GHG chemicals, improvement is a hot research issue at present in Bang-
such as nitrous oxide ­(N2O) or methane (­CH4), by con- ladesh. Biochar-based inoculant carrier with rhizobia
verting them into another accessible chemical utilized by has not been studied before in groundnut cultivation in
the soil and plant (Tesfahun 2018; Zhang et al. 2020). Bangladesh, which has significantly improved the symbi-
Groundnut (Arachis hypogaea L.) or peanut is the otic performance of legumes with rhizobia (biofertilizer),
sixth most important oilseed crop in the world culti- resulting in reduced N fertilizer demand and promoted
vated throughout tropical and subtropical areas, fol- the sustainability of crop production. Therefore, the dis-
lowed by cereal crops. In Bangladesh, groundnut is the cussions mentioned above might be taken into account
second most oilseed crop and has played a pivotal role in while this study was conducted to broaden the knowledge
Shikha et al. Carbon Research (2023) 2:10 Page 4 of 15

of the impact of biochar amendment with biofertilizer on strain BARI RAh-892) containing 1­ 08 cells g­ −1 inoculum
rhizobium nodulation, groundnut growth performance was used at the rate of 1.5 kg ­ha−1. Groundnut seeds
and yield productivity. Additionally, the additional focus were mixed thoroughly with the inoculum before sowing.
of the current study in groundnut cultivation was on Seeds were used at the rate of 75 kg ­ha−1. The rhizobium
evaluating the interaction effects of biochar and biofer- inoculant and the groundnut variety were sourced from
tilizer on the growth, yield potential, and ease of GHG the Bangladesh Agricultural Research Institute (BARI),
emissions, which contribute to environmental sustain- Gazipur, Bangladesh.
ability towards climate-smart agriculture.
2.4 Sowing, fertilization and weeding practices
2 Materials and methods The seeds were planted by dibbling, and they were sown
2.1 Experimental site
for the first year on November 22, 2017. Here note that
The experiment was conducted during the 2017–19 the uninoculated seeds were sown first to avoid contami-
academic years at the Regional Agricultural Research nation. Nitrogen (N), phosphorus (P), potassium (K),
Station (RARS) research field in Jamalpur, Bangladesh. sulfur (S), zinc (Zn) and boron (B) were used as urea,
Before beginning the tillage operation, soil samples were TSP, MoP, gypsum, zinc sulfate, and boric acid, respec-
collected at a depth of 0–15 cm for each replicate. The tively. All P, K, S, Zn, B and one-third of the urea-N were
chemical properties of soils in the experimental site were applied at the time of final land preparation, and the
silt clay loam in texture belonging to the Sonalata series remaining urea-N was applied in two equal installments
under Agro-Ecological Zone-9 (AEZ-9), and the research on the ­30th and ­50th days of sowing. All the intercultural
field was located at an altitude of 16.46 m, 24 56′11"N lat- operations (such as irrigation, weeding, insect control)
itude, and 89 55′54"E longitude. were done when necessary. The weeding operation was
controlled by hand pulling.

2.2 Experimental design and treatments 2.5 Soil parameters and nutrients analysis

The experiment was designed as a randomized complete Composite soil samples were collected from the soil sur-
block (RCB) design with seven treatments each of which face at 0–15 cm depth in pre-sowing and post-sowing
replicated three times. The unit plot size was 6 m­ 2 (3 m stages and analyzed for their physiochemical properties.
x 2 m) with a buffer distance of 1 m. A 1.5 m space was The soil’s physical and chemical properties were ana-
left between the experimental plots and the plot’s outside lyzed using standard methods proposed by Olsen et al.
border to avoid any side effects or influences from other (1954) and Page et al. (1989). Soil pH was determined in
plots. Each repetition (plot) was enclosed by bunds (als) a 1:5 (w:v) soil to water ratio using a pH meter (AB150,
30 cm wide and 15 cm tall to prevent soil nutrient seep- Fisher Scientific, USA). Soil organic matter (SOM) was
age. Seven treatments were adopted for this study based determined using an oxidation method with potassium
on the different fertilizer management packages, biochar dichromate. An automated azotometer (KDN-102F,
and biofertilizer, as shown in Table 1. Qianjian limited, Shanghai, China) was used to test soil
nitrogen (N). ­NO3−-N and ­NH4+-N were extracted with
2.3 Biochar incorporation and rhizobium inoculation the 2 M KCl solution at a soil/water ratio of 1:5 at 25 °C
Biochar was used in the furrow at the rate of 10 t ­ha−1. and measured using a smart continuous flow analyzer
The tested crop was groundnut (i.e., BARI Chinab- (SmartChem200, Shenzhen, China). Potential nitrifica-
adam-8). Peat-based rhizobial inoculum (Bradyrhizobium tion rates were measured using the chlorate inhibition

Table 1 Experimental treatments for this study

Crop Experimental treatments Fertilizer dose (kg ­ha−1)

Groundnut T1 = Control Native fertility

T2 = Soil test based (STB) fertilizer dose following fertilizer recommendation guide N36P36K45S36Zn2B1.4 ­Mo0.5
(FRG) 2018 (Ahmmed et al. 2018)
T3 = ­ ( T2 treatment minus nitrogen fertilizer) + biofertilizer
T4 = ­T3 treatment + biochar
T5 = ­T2 treatment + biochar
T6 = only biofertilizer
T7 = only biochar
Shikha et al. Carbon Research (2023) 2:10 Page 5 of 15

method (He et al. 2007; Liao et al. 2020). Soil parameters material that was locally collected. The rice husk was loaded
of bulk density were determined using the core sam- in the iron drum covered with a metal sheet with a chimney
pling method (Blake 2015; Rahman et al. 2021), and soil at the top which was placed into an earthen kiln (developed
organic carbon (SOC) was determined both before the by Soil Science Division, RARS, Jamalpur, Bangladesh). The
experiment started and after the two-year cropping. The rice husk was burnt in the presence of partial oxygen condi-
SOC stock was estimated with the following equation by tion. Biochar was produced for three hours at temperatures
Milne et al. (2007); and Zeng et al. (2021). between 490-5500C with a heating rate of 5-100C ­min−1 in a
laboratory-scale pyrolysis unit comprising of a reactor kiln,
SOC stock = SOC content of soil × BD × A × D (1)
where the pyrolysis temperature was recorded at 30-min
intervals by a digital temperature recorder by placing the sen-
sor into the kiln through an aeration hole. All preparations
( ) ( ) ( )
Carbon accumulation tha−1 = Final C stock tha−1 − Initial C stock tha−1

(2) were carried out in duplicate. The burnt husks were then
where, SOC stock = soil organic carbon stock (t h ­ a ); −1 grounded and allowed to be cooled to room temperature.
SOC content of soil = soil organic carbon content of The final product was used as biochar. Chemical analysis was
soil (%), BD = bulk density, A = area of a farm (­m2) and done at the Soil Science Division, BARI, Gazipur, following
D = soil sampling depth (m). The nutrient status of the the standard methods. An elemental analyzer (Flash model
initial soil prior to fertilization is presented in Table 2.Soil EA-1112, Thermo Scientifics) was used to determine the key
was sampled during the seedling stage (7 weeks), bolting analyses for the biochar characterization, including total car-
stage (11 weeks), flowering stage (15 weeks), and harvest bon (TC) and N content. For elemental composition, 200 mg
stage (24 weeks) from the beginning of the experiment in of each biochar was burnt in a muffle at 500 °C for eight hours
order to measure plant physiological parameters and soil and digestion was carried out with nitric acid and hydrogen
properties. Each sample was measured in triplicate. The peroxide (Enders et al. 2012). Ca, Mg, Fe, Mn, Cu and Zn
activity of the root was determined by the triphenyltetra- contents were measured by an atomic absorption spectrom-
zolium chloride method (Luo et al. 2015). N concentra- eter (Analyst 200-PerkinElmer) and P content was measured
tion was measured using a Foss Auto Analyzer Unit by using a spectrophotometer (BEL model S05) (Murphy and
(Kjeldahl 8,400). At the time of harvest, grain yields were Riley 1962). The chemical compositions (such as total carbon
estimated. The sum of the total dry matter weight and (TC), N, P, K, S, B, Cu, Fe, Mn, Zn, Mg, Ca and pH) of biochar
the concentration of N in all the plant parts were used to were determined, which can be seen in Table 3.
determine the accumulation of N.
2.7 Data Collection and statistical analysis
2.6 Biochar production and chemical analysis Data were collected on the following parameters: plant
The biochar was produced using a slow-pyrolysis with the height (cm) using the meter rule, number of nut p ­ lant−1,
oxygen-limited condition, and the rice husk was used as a raw 100 nut weight (g), kernel weight of 100 nuts (g), 100 ker-
nel weight (g), nut yield (t ­ha−1), Shelling (%), stover yield (t
­ha−1), nodule number p ­ lant−1, nodule weight (mg) p ­ lant−1),
Table 2 Initial soil chemical properties of the experimental soils −1 −1
root weight (g ­plant ), and shoot weight (g ­plant ). Nod-
Parameter Unit Value Critical level ules were collected by carefully uprooting 10 (ten) sample
plants selected randomly from each unit plot at the 50 per-
pH (1:5 ­H2O) - 6.0 - cent flowering stage. Nodules were separated from the roots,
Organic matter (%) 0.83 - counted, and then dried in the oven. After that, they were
Organic carbon (OC) (%) 0.48 - weighted by a weight meter. Yield and yield components data
Bulk density (g ­cm−3) 1.46 - were collected at the maturity stage. Similarly, yield and yield
Calcium (Ca) meq 100 ­g−1 5.2 2 contributing characters data were recorded and analyzed
Magnesium (Mg) meq 100 ­g−1 1.8 0.5 statistically using the statistical software STAR developed
Potassium (K) meq 100 ­g−1 0.12 0.12 by IRRI. Then, significant differences were assessed at a 5%
Nitrogen (N) (%) 0.044 - (p = 0.05) significance level, and the treatment means were
Phosphorus (P) µg ­g−1 15.6 10 separated using Duncan’s Multiple Range Test (DMRT).
Sulphur (S) µg ­g−1 10 10
Boron (B) µg ­g−1 0.3 0.2 3 Results and discussion
Copper (Cu) µg ­g−1 1.5 0.2 3.1 Biochar and Biofertilizer effects on Postharvest soil
Iron (Fe) µg ­g−1 28 4 physicochemical properties
Manganese (Mn) µg ­g−1 2.2 1 Table 4 shows the impact of biochar and biofertilizer on
Zinc (Zn) µg ­g−1 1.42 0.6 the post-harvest soil nutrients results following the
Shikha et al. Carbon Research (2023) 2:10 Page 6 of 15

Table 3 The chemical composition of rice husk biochar used for of biochar is capable of changing nutrient availability and
the experiment might provide additional N, P, or bioavailable C sources
Parameter Unit Value for microbial proliferation in the rhizosphere, depending
on the type of biochar (Rutigliano et al. 2014; Liao et al.
pH (1:5) - 8.7 2019). The researcher observed a considerable rise in bio-
Total carbon (%) 39.2 available K, Ca, and Mg contents following the applica-
Calcium (Ca) meq 100 ­g−1 1.81 tion of biochar at a rate of 5 t ­ha−1 (Karim et al. 2020).
Magnesium (Mg) meq 100 ­g−1 0.92 Additionally, Gundale and DeLuca (2006) observed that
Potassium (K) meq 100 ­g−1 0.92 adding biochar at a rate of 10 t ­ha−1 boosted the soil
Nitrogen (N) (%) 1.1 ­NH4+ content and net N mineralization rate. From the
Phosphorus (P) µg ­g−1 0.73 analysis, it can be noted that improved soil character-
Sulphur (S) µg ­g−1 0.27 istics resulted from the effects of applying biochar and
Boron (B) µg ­g−1 0.011 biofertilizer.
Copper (Cu) µg ­g−1 0.0012 Zoghi et al. (2019) reported that by adding biochar and
Iron (Fe) µg ­g−1 0.12 biofertilizer to the soil, plants are given better conditions
Manganese (Mn) µg ­g−1 0.03 to absorb nutrients, which increases the soil’s ability to
Zinc (Zn) µg ­g−1 0.016 store water and support plant growth. According to the
findings, adding biochar to the Charland poor water-defi-
cient soil might significantly reduce damage caused by
completion of the experiment, revealing that the bio- drought stress to biomass production.
char and biofertilizer application produced significant Soil bulk density (BD) is the most crucial physical indi-
variations in the soil physiochemical characteristics. The cator of soil quality and fertility, influencing plant growth
highest pH value was observed in the treatment (­T4) of and nut yield. Asadi et al. (2021) found that applying 3%
biochar-biofertilizer combined application, while the rice husk biochar to clayey soil and loamy soil reduced
lowest values were recorded in the control (­T1) treat- BD by 8% and 22%, respectively. The results from Table 4
ment. Numerous studies have examined how adding bio- indicate that BD was decreased by a certain amount fol-
char to the soil might raise its pH value (Ding et al. 2016). lowing postharvest soil analysis, compared to the origi-
Based on the findings of this study, the pH of the soil had nal BD of 1.46 g ­cm−3. Changes in altering soil physical
been slightly raised for all treatments. The total N ranged conditions in the rhizosphere can cause significant dif-
from 0.041 to 0.067% for all the treatments except the ferences in biomass and yield observed under the vari-
control. In T­ 4 (biochar and biofertilizer) treatment, about ous soil compaction levels. This could indirectly impact
63% of soil’s available N content was increased com- physiological processes like photosynthesis and respira-
pared to the control (­ T1). P and exchangeable K increased tion by influencing the soil’s hydrological characteris-
from 10.55 to 16.3 meq 100 ­g−1, and 0.14 to 0.18 meq tics, which impact nutrient mobilization. Furthermore,
100 ­g−1, respectively, which were about 54.5% and 28.57% this could lead to variations in the number of nuts, mass
increases in the ­T4 treatment in comparison to the con- of nuts, and total biomass of groundnut. According to
trol ­T1 treatment for P and K, respectively. The addition Dauda et al. (2019), there were also high yields in soils

Table 4 Nutrient status of post-harvest soil in groundnut production

Treatments pH Total N K P S B Zn SOC Bulk density
(%) meq 100 ­g−1 µg ­g−1 (%) (g ­cm−3)

T1 6.53 0.041 0.14 10.55 13.62 0.25 1.12 0.46 1.46

T2 6.60 0.048 0.16 13.82 16.25 0.39 1.73 0.45 1.45
T3 6.73 0.064 0.18 13.60 18.48 0.45 2.11 0.52 1.44
T4 6.98 0.067 0.18 16.3 21.61 0.56 2.43 0.58 1.41
T5 6.91 0.057 0.17 15.6 20.17 0.44 2.00 0.54 1.42
T6 6.62 0.053 0.14 12.2 15.2 0.37 1.65 0.50 1.44
T7 6.85 0.049 0.15 11.6 16.3 0.42 1.71 0.57 1.42
Initial soil 6.50 0.044 0.12 9.6 12.6 0.30 1.42 0.48 1.46
T1 – control; ­T2- STB fertilizer dose following fertilizer recommendation guide (FRG) 2018; ­T3 = ­ ( T2 treatment minus nitrogen fertilizer) + biofertilizer; ­T4 = ­T3
treatment + biochar; ­T5 = ­T2 treatment + biochar; ­T6 = only biofertilizer; ­T7 = only biochar
Shikha et al. Carbon Research (2023) 2:10 Page 7 of 15

with minimal compaction and lower yields in soils with stages than the biofertilizer with biochar-related treat-
higher compaction. The same phenomenon was observed ments, whereas control, only biochar, and biofertilizer
in the present study. Table 4 analysis results noted that treatments observed lower amounts. During the seed-
the highest total SOC stock was obtained where biochar ling stage, the ­ NO3−-N content under T ­ 5 treatment
and biofertilizer were applied, leading to increased soil (urea + biochar) significantly differed from that under
carbon stock. Urea ­(T2) and biofertilizer with biochar (­ T4) treatments.
The ­NO3−-N contents under urea and biofertilizer with
3.2 Impact of biochar‑biofertilizer based management biochar treatments were not significantly different dur-
practices on soil nitrification and denitrification ing the flowering stage, but both were significantly
Figure 1 shows the amount of ammonium N ­(NH4+-N) higher than those with control, only biofertilizer and
and nitrate N (­NO3−-N) in the soils for the different only biochar treatments. However, during the pod for-
treatments under the plant growth stages of seedling, mation and harvesting stage, the soil ­NO3−-N content
flowering, pod formation and harvesting. The highest under ­T5 treatment was the highest among all samples.
­NH4+-N content was observed for all the stages in the The combination treatment with nitrogen, biofertilizer
­T4 (biochar and biofertilizer) treatment followed by the and biochar affected the potential nitrification rates in
­T5, ­T3 and ­T2 treatments, respectively. It was observed the soil (Fig. 2). No differences were observed under the
under the treatment ­T5 (Urea together with biochar) that various treatments during the flowering and harvesting
ammonium N was increased significantly rather than stages, but nitrification rates were significantly increased
­T2 treatment, which belonged to only urea application. in the nitrogen and biochar-treated soils during the flow-
The ­T4 treatments related to the biochar and biofertilizer ering and pod formation stages. The nitrification rates
showed the highest amount due to the presence of nitro- under the T ­ 4 treatment were significantly greater than
gen-fixing rhizobium bacteria, where bacteria served as those under the treatments of nitrogen and biofertilizer
a converting agent to convert from supplied nitrogen to application during the flowering and harvest stages. The
ammonia, resulting in nitrogen becoming available to nitrification rate is crucial in global N cycling by regu-
plants. During the flowering and pod formation stages, lating ammonia-oxidizing rhizobium bacteria (Li et al.
there was no difference between these two, with the 2015). Soil potential nitrification rates describe the ability
same growth happening for all the treatments. During of soil-nitrifying microbes to convert N ­ H4+ to ­NO3− and
the harvest stage, there were no differences among bio- are regulated by the quantity of nitrifying populations.
char and biofertilizer-related treatment (­ T4), but all sig- In this study, higher soil potential nitrification rate was
nificantly increased N­ H4+-N content compared to that observed in ­T4 treatment than in other treatments. This
observed with Urea treatment. might be because the soil’s nitrifying bacteria converted
For the N ­ O3−-N content, urea with biochar treat- more ­NH4+ to N ­ O3−, increasing the concentration of
-
ment ­(T5) showed the highest amount for plant growth ­NO 3-N that was seen in the treatment soils. Besides soil

Fig. 1 Effects of the different treatments on the soil’s (a) nitrate nitrogen and (b) ammonium nitrogen at different stages of plant growth in
groundnut production. Here, ­T1 – control; ­T2- STB fertilizer dose following fertilizer recommendation guide (FRG) 2018; ­T3 = ­ ( T2 treatment minus
nitrogen fertilizer) + biofertilizer; ­T4 = ­T3 treatment + biochar; ­T5 = ­T2 treatment + biochar; ­T6 = only biofertilizer; ­T7 = only biochar
Shikha et al. Carbon Research (2023) 2:10 Page 8 of 15

Fig. 2 Effect of different growth stages in different treatments on potential nitrification rate. Note: ­T1- control; ­T2- STB fertilizer dose following
fertilizer recommendation guide (FRG) 2018; ­T3 = ­ ( T2 treatment minus nitrogen fertilizer) + biofertilizer; ­T4 = ­T3 treatment + biochar; ­T5 = ­T2
treatment + biochar; ­T6 = only biofertilizer; ­T7 = only biochar

N content, higher C input has been reported to stimulate ­(T1) treatment. Furthermore, the highest plant height
organic matter mineralization and enhance ammonia-oxi- (50.53 cm) was obtained from the T ­ 5 (urea + Biochar) treat-
dizing bacteria growth (Simonin et al. 2015). Our finding ment (Table 5), and the lowest plant height (19.15 cm) was
showed that biofertilizer combined with biochar signifi- recorded from the control ­(T1) treatment. Previous studies
cantly increased SOC (Table 4), supporting the findings of reported that biochar-based inoculants increased root and
Simonin et al. (2015). shoot biomass, nodulation, and nutrient uptake by ground-
Previous studies have reported contrasting results nut plants in pot and field experiments (Egamberdieva et al.
about the impact of biochar on microbial community 2018). Moreover, applying biochar and rhizobium inocula-
composition and N nutrients in the soil (Kolton et al. tion on groundnut plants increased the number of effective
2017; Yan et al. 2022; Wang et al. 2022; Li et al. 2023). nodules, shoot, and root dry weights (Yusif et al. 2016). In
However, no previous study has reported how biochar this study, the highest nodule number performed in the
with biofertilizer impacts soil microbes in groundnut ­T4 treatment might be due to the effect of biochar and
production. This indicates that biochar combined with biofertilizer, as this application to soil helps in increasing
urea and microbes stimulates microbial activity more the nutrients levels either by influencing the metabolism
effectively than applying the parameters alone. of the plant, which alters the composition of root exudates
or influencing the solubility and availability of nutrients
3.3 Effects of biochar and biofertilizer on nodulation, dry (Kumar et al. 2022). Additionally, the studies proved that
matter production, and plant height of groundnut microbes based on biochar and biofertilizer enhanced plant
cultivation growth and nutrient absorption (Tripti et al. 2017).
The effect of biochar and biofertilizer on the nodulation, A systematic cycle of biochar and biofertilizer in the soil–
physical characteristics and plant height was significant plant system within the system boundary is presented in
compared with that in the control treatment (Table 5). Fig. 3. Rhizobium biofertilizers are compounds that con-
Table results indicate that the highest number of the nodule tain symbiotic bacteria, which are the essential nitrogen-
(avg. 78.18 ­plant−1) and nodule weight (122.97 mg p ­ lant−1) fixing organisms capable of driving atmospheric nitrogen
were obtained from the T ­ 4 treatment, followed by the T ­3 ­(N2) and delivering it to the roots of legume plants, as well
treatment’s of nodule number (avg. 68.01 p ­ lant−1) and nod- as inducing nodules to grow. These nodules fix ­N2 by con-
ule weight (115.33 mg ­plant−1), whereas the lowest number verting it into ammonia (­ NH4+) as part of the essential pro-
of the nodule (43.83 p ­ lant−1) and nodule weight (53.67 mg cess known as nitrification, which plants can then use for
­plant−1) were recorded from the control ­(T1) treatment. growth and development (Fig. 1). In this study, higher rates
Also, the highest root weight (1.47 g p ­ lant−1) was found of soil potential nitrification were seen in the ­T4 (biochar
from the T ­ 4 treatment, and the highest shoot weight plus biofertilizer) treatment than in the other treatments
(35.47 g ­plant−1) was recorded from the ­ T3 treatment, (Table 4 & Fig. 2), which could explain the increased con-
whereas the lowest root weight (0.65 g ­plant−1) and shoot centration of nitrate nitrogen ­(NO3−-N) in the ­T4 treat-
weight (16.50 g p­ lant−1) were recorded from the control ment soils (Fig. 1). This was caused by the transformation
Shikha et al. Carbon Research (2023) 2:10 Page 9 of 15

Table 5 Effects of biochar and biofertilizer on nodulation, dry matter production and plant height in groundnut production during
2017–2019
Treatments Nodule number (­ plant−1) Nodule weight Root weight Shoot weight Plant height
2017–18 2018–19 Average (mg ­plant ) −1
(g ­plant )
−1
(cm)

T1 46.00d 41.67d 43.83 53.67e 0.65e 16.50e 19.15f

T2 55.84 cd 60.00c 57.92 75.55d 0.98bc 28.18bc 32.78 cd
T3 62.57bc 73.53b 68.01 115.33a 1.10b 35.47a 36.90c
T4 73.67a 82.67a 78.17 122.97a 1.47a 30.44b 43.97b
T5 62.51 bc 72.00b 67.28 106.09b 0.97bcd 25.71c 50.53a
T6 61.17bc 62.33c 61.75 103.25bc 0.80cde 21.44d 27.12de
T7 59.67bc 55.67c 57.67 96.46c 0.74de 18.37de 22.34ef
CV (%) 11.61 9.63 - 2.91 8.63 4.38 6.39
LSD (0.05) * * * * * *
Values in a column having the same letter(s) do not differ significantly at 5% level by LSD. ­T1 – control, farmers practice; ­T2- STB fertilizer dose following fertilizer
recommendation guide (FRG) 2018; ­T3 = ­ ( T2 treatment minus nitrogen fertilizer) + biofertilizer; ­T4 = ­T3 treatment + biochar; ­T5 = ­T2 treatment + biochar; ­T6 = only
biofertilizer; ­T7 = only biochar. * = Significant (p ≤ 0.05)

Fig. 3 Systematic conceptual cycle of the effects of biochar and biofertilizer on soil and related plant growth in the soil plant system within the
system boundary in the framework of environmental sustainability
Shikha et al. Carbon Research (2023) 2:10 Page 10 of 15

80
120

Nodule weight (mg plant-1)

70

Nodule number (plant-1)

60 100
50 80
40 60
30
40
20
10 20
0 0
T1
T3 T4 T5 T6 T7T2 T1 T2 T3 T4 T5 T6 T7
Treatments Treatments
Fig. 4 Effects of rhizobium biofertilizer on the nodule number ­(plant-1) and nodule weight in groundnut production

of a higher amount of ­NH4+ to ­NO3− due to the nitrifying presented tables show that inoculation with rhizobium
rhizobium in the soil. Furthermore, increasing the copy significantly increases all the growth and yield param-
number of the rhizobium that sped up the N nitrification eters than when not inoculated; biochar addition to soil
process changed the rhizobium community composi- increases soil nutrient concentrations and microbial
tion and enhanced soil enzyme activities. This made more activity, leading to plant growth and yield productivity.
nodules form in T­ 4 treatment (Fig. 4), which then assured Potential soil nitrification rate might be altered by the
the availability of N nutrients throughout various growth treatment ­( T4) using biochar and biofertilizer (Fig. 2),
stages in groundnut production. These findings show that as it can be seen that the total nodule number and
­T4 treatment continuously ensures the supply of available nodule weight were increased in the T ­ 4 treatment. No
N fertilizer even during the groundnut’s late growth stages changes were noticed throughout the seedling and bolt-
to support growth, thereby promoting N uptake (Fig. 2). ing stages in the T­ 4 treatment; however, it was observed
from the experimental field that the flowering and nut
3.4 Biochar and biofertilizer effects on nut characters, nut formation stages in biochar and biofertilizer-treated
yield and yield contributing characters of groundnut soils were identical with those in the other treatments.
cultivation This development might be from the improved nitrifi-
The effect of biochar and biofertilizer on nut char- cation rates throughout these two stages (Rawat et al.
acteristics, yield productivity, and yield contributing 2019; Ramasamy et al. 2020). Eventually, the T ­ 4 treat-
characteristics of groundnut cultivation can be seen in ment successfully enhanced the highest yield by nodu-
Table 6. The table shows that insignificant results were lating the abundance of functional rhizobium through
obtained for nut p ­ lant−1, stover output (t h­ a−1), and increased soil nitrification and reduced denitrification,
shelling (%). The highest 100 nut weight (96.33 g) was as compared to the other treatments, thereby promot-
obtained for the ­T4 ­(T3 + biochar) treatment, which was ing groundnut growth and subsequently increasing nut
statistically similar to that in the treatments of T ­ 3 ((T2 productivity (Fwanyanga et al. 2022).
–N) + biofertilizer) and T ­ 5 (STB + biochar), which had
(86.33 g) and (84.00 g) respectively, whereas the lowest 3.5 Biochar impact on soil organic carbon accumulation
100 nuts weight (66.67 g) was recorded from the control The soil organic carbon (SOC) content has increased
­(T1) treatment. The highest 100 kernel weight (50.92 g) significantly (p < 0.05) as a result of the addition of bio-
was obtained from the ­T4 ­(T3 + biochar) treatment, fol- char to the soil (Table 7). Generally, most SOC is accu-
lowed by the ­T5 treatment (45.52 g), whereas the low- mulated in the topsoil between 0–30 cm (Rahman et al.
est 100 kernel weight (30.07 g) was recorded from the 2021). At this portion of the topsoil, over the two years
control ­(T1) treatment. Likewise, the highest nut yield of experimentation, the highest SOC accumulation rates
(2.30 t ­ha−1) was obtained from the ­T4 ­(T3 + biochar) were estimated for the treatments related to biochar
treatment, while the lowest nut yield (0.79 t ­ha−1) was application ­(T4 & ­T7), which were 1.76 and 1.49 t ­ha−1,
recorded from the control (­T1) treatment. The highest respectively. Previous studies also reported a similarly
nut yield obtained from the ­T4 treatment might be due significant effect on SOC accumulation for soils under
to the nodulation effect of biochar and biofertilizer. Fur- the biochar-related amendment (Rehman and Razzaq
thermore, Biochar-based inoculants also enhanced plant 2017; Jatav et al. 2020). The initial SOC (%) and soil car-
growth and nut yield, which is validated by previous bon stock were 0.48% and 10.50 t h ­ a−1, respectively. Irre-
research findings (Egamberdieva et al. 2018). Previously spective of treatments, the highest SOC was recorded in
Shikha et al. Carbon Research (2023) 2:10 Page 11 of 15

Table 6 Effects of biochar and biofertilizers on nut characters, yield and yield contributing characteristics of groundnut during 2017-
2019
Treatments Nut ­(plant−1) 100 nut weight 100 kernel weight Shelling Stover yield Nut yield (t h
­ a−1)
(g) (g) (%) (t ­ha−1) 2017–18 2018–19 Average

T1 15.93 66.67c 30.07f 62.07 13.07 0.81d 0.77d 0.79

T2 20.13 78.67bc 35.92d 73.76 13.37 1.73b 1.75b 1.74
T3 23.87 86.33ab 40.07c 65.68 13.80 1.83b 1.86b 1.85
T4 25.07 96.33a 50.92a 72.50 13.30 2.38a 2.23a 2.30
T5 22.33 84.00ab 45.52b 73.36 12.97 1.96b 1.90b 1.93
T6 23.33 72.33bc 30.67f 70.57 12.57 0.95d 0.91 cd 0.93
T7 22.20 73.06bc 33.96e 72.40 12.63 1.24c 1.08c 1.16
CV (%) 13.55 7.34 9.03 8.75 8.03 6.26 11.2 -
LSD (0.05) - * * - - * * -
Values in a column having the same letter(s) do not differ significantly at the 5% level by LSD. ­T1 – control, farmers practice; ­T2 - STB fertilizer dose following fertilizer
recommendation guide (FRG) 2018; ­T3 = ­ ( T2 treatment minus nitrogen fertilizer) + biofertilizer; ­T4 = ­T3 treatment + biochar; ­T5 = ­T2 treatment + biochar; ­T6 = only
biofertilizer; ­T7 = only biochar. * = Significant (p ≤ 0.05)

soil amended biochar after the experiment, about 20.08% increased SOC content. Dejene and Tilahun (2019) also
more than the control treatment of 0.46%. It is seen from reported that significantly more SOC was accumulated
Table 7 that the soil carbon stock increased significantly when biochar was added at a rate of 5 t h ­ a−1. The main
from 10.07 to 12.26 t ­ha−1 for the treatment ­T4; this may explanation for these discoveries might be the biochar’s
be attributed to the significant carbon content of biochar stable carbon content, which makes it difficult to degrade
which is confirmed by the report (Yang et al. 2020); simi- in soil environments and contributes to the soil carbon
lar findings were reported by Nigussie et al. (2012). pool. On the other hand, it can be predicted that other
Biochar utilization may be added to soils to improve GHG of N ­ 2O breaks down to form the atmospheric N ­ 2,
soil functions, soil fertility and reduce GHG emis- as the observed nodulation numbers increased in bio-
sions that would otherwise naturally degrade to GHGs. char and biofertilizer treatments (seen from the previous
Without application of biochar and biofertilizer, lack tables) that come from the ­N2, which might then be fixa-
of external utilization of organic inputs and microbial tion by the nodule formation, consequences the reduc-
breakdown of absorbed carbon hinder carbon seques- tion of GHG emissions in the atmosphere.
tration. Therefore, applying biochar with biofertilizer
in the soil in groundnut cultivation helps in organic 3.6 Environmental benefits of biochar and biofertilizer
carbon accumulation to meet the ultimate goal of car- application
bon sequestration in soil. It is clear from the reports by Biochar can make substantial breakthroughs in reducing
Blanco-Canqui et al. (2020) that introducing biochar greenhouse gas (GHG) emissions, reducing soil nutrient

Table 7 SOC accumulation and GHG emissions reduced for related SOC accumulation under adopting different treatments in
groundnut production
Treatments Initial soil Post-harvest soil SOC accumulation GHG emissions saved
for SOC accumulation
SOC BD Soil C Stock SOC Bulk density Soil C Stock
(%) (g ­cm )
−3
(t ­ha )
−1
(%) (g ­cm )
−3
(t ­ha−1) (t ­ha−1) (kg ­CO2eq ­ha−1)

T1 0.48 1.45 10.50 0.46 1.46 10.07 (-) 0.43 (-) 1.613
T2 0.48 1.45 10.50 0.45 1.45 10.07 0.37 1.388
T3 0.48 1.45 10.50 0.52 1.44 11.23 0.73 2.738
T4 0.48 1.45 10.50 0.58 1.41 12.26 1.76 6.60
T5 0.48 1.45 10.50 0.54 1.42 11.50 1.00 3.750
T6 0.48 1.45 10.50 0.50 1.44 10.8 0.30 1.125
T7 0.48 1.45 10.50 0.57 1.42 12.04 1.49 5.588
T1 – control, farmers practice; ­T2 - STB fertilizer dose following fertilizer recommendation guide (FRG) 2018; ­T3 = ­ ( T2 treatment minus nitrogen fertilizer) + biofertilizer;
­T4 = ­T3 treatment + biochar; ­T5 = ­T2 treatment + biochar; ­T6 = only biofertilizer; ­T7 = only biochar
Shikha et al. Carbon Research (2023) 2:10 Page 12 of 15

leaching losses, sequestering atmospheric carbon into characters. Based on the findings, it was evident that the
the soil, and thereby increasing environmental sustain- biochar and biofertilizer treatment was the best manage-
ability. Nevertheless, biochar can reduce the need for ment treatment, whereas biochar-only treatment was
chemical fertilizers, resulting in reduced GHG emissions the second most excellent treatment. Biochar generally
from fertilizer manufacture. Results from Table 7 show improves the soil’s physical environment, is a measure to
that the highest GHG emissions saved for the SOC accu- reduce chemical fertilizer inputs and alleviates GHG emis-
mulation in treatments T ­ 4 and ­T7 related to the biochar sions because of the increase in SOC accumulation. The
utilization were 6.6 and 5.588 kg C ­ O2eq ­ha−1, respec- results of this study are based on two years of experiments;
tively. It is noted that biochar has significantly helped the thus, these processes will be further studied to evaluate
environment by saving a certain amount of GHG emis- the effects of biochar and biofertilizer on N availability in
sions to accumulate SOC. On the other hand, the capac- plants, soil nitrification rate and environmental sustain-
ity of biochar to absorb and hold ammonium in soils ability in the Charland agroecosystems in Bangladesh.
reduces nitrogen availability for the denitrification pro-
cess, resulting in lower N ­ 2O emissions to the atmosphere
Abbreviations
(Rehman and Razzaq 2017). The study showed that the AEZ Agro-ecological zone
­T4 treatment significantly increased soil SOC (Tables 4 BARI Bangladesh agricultural research institute
and 7), supporting the findings of Liao et al. (2020). As BD Bulk density
CO2 Carbon dioxide
a result, the ­T4 treatment regulated by the nitrification CO2eq Carbon dioxide equivalent
oxidizing rhizobium abundance during the flowering and DMRT Duncan’s multiple range test
harvest stages is an important microbiological mecha- GHG Greenhouse gas
IBI International biochar initiative
nism for enhancing soil N ­ O3−-N (Fig. 1); the higher MoP Muriate of potassium
−
­NO3 -N concentration results in reduced denitrification. NO3−-N Nitrate nitrogen
As a result, it was assumed that variables such as bio- NO3− Nitrate
N2O Nitrous oxide
char and higher soil potential nitrification rates caused NH4+ Ammonium ion
high ­NO3−-N concentrations in ­T4 treatment soil while OC Organic carbon
reducing ­N2O emissions. According to several research- RARS Regional agricultural research station
RCB Randomized complete block
ers, adding biochar typically results in a reduction in ­N2O SOC Soil organic carbon
emissions of about 83 percent. Thus, our findings indi- STAR​ Statistical tool for agricultural research
cated that the ­T4 treatment might have enhanced envi- TSP Triple superphosphate

ronmental benefits over the other treatments. Acknowledgements

Authors would like to acknowledge the personnel of institutes of BARI, Soil
4 Conclusion Resource Development Institute (SRDI), Bangladesh Bangladesh Institute
of Nuclear Agriculture (BINA), and Bangladesh Sugarcrop Research Institute
In this study, the effects of biochar with the rhizobium (BSRI), who are all involved in this study.
biofertilizer on plant-soil interactions in soil microbial
communities in the Charland agroecosystems in Bangla- Authors’ contributions
Fouzia Sultana Shikha: investigation, funding acquisition, methodology, devel-
desh were comprehensively evaluated for the first time. opment or design of methodology, data curation, formal analysis, software,
The use of biochar and biofertilizer for the growth of writing—original draft; Md Mashiur Rahman: Conceptualization, investiga-
groundnut is the main factor underlying the elevated tion, validation, formal analysis, resources, data curation, writing – review &
editing, visualization, proofreading; Naznin Sultana: formal analysis, resources,
yield productivity and environmental sustainability, as data curation, writing – review & editing; Md Abdul Mottalib: formal analysis,
the N nutrient affects rhizobium involved in nitrifica- resources, data curation, visualization, proofreading; Monira Yasmin: Investiga-
tion and denitrification. The study evaluated the underly- tion, provision of study material, resources. All authors read and approved the
final manuscript.
ing mechanisms and found that the treatment related to
biochar and biofertilizer improves soil microbial activity Funding
and shifts bacterial rhizobium community composition This research was carried out as part of the ongoing research program for
sustainable production systems. The Bangladesh Agricultural Research Insti-
toward increasing N nitrification. This process improves tute (BARI) generously provided financial support for this study, while the Soil
the abundance of ammonia-oxidizing rhizobium and Resource Development Institute (SRDI), Bangladesh Bangladesh Institute of
stimulates nitrification, accelerating the transforma- Nuclear Agriculture (BINA), and BSRI generously provided the necessary labo-
ratory facility. The authors would like to acknowledge all collaborators who
tion of N­ H4+ to ­NO3− and reducing ­NO3− (gas) loss. helped make this research successful. This paper’s content and opinions are
Our results also indicate that ­N2O emissions might be those of the authors and do not reflect those of BARI, BINA, or BSRI.
reduced by increasing the abundance of these factors in
Availability of data and materials
biochar and biofertilizer treatment soil. Authors are certify that all essential data is included in the publication. The
Applying biochar and biofertilizer inoculation on datasets used or analyzed during the current study are available from the cor-
groundnut plants increases the yield and yield contributing responding author on reasonable request.
Shikha et al. Carbon Research (2023) 2:10 Page 13 of 15

Declarations fruits (but not leaves) is associated with changes in the rhizosphere
microbiome. Front Plant Sci 12:1758. https://​doi.​org/​10.​3389/​FPLS.​2021.​
Ethics approval and consent to participate 700479/​BIBTEX
No. Dignac MF, Derrien D, Barré P, Barot S, Cécillon L, Chenu C, Chevallier T,
Freschet GT, Garnier P, Guenet B, Hedde M, Klumpp K, Lashermes G,
Consent for publication Maron PA, Nunan N, Roumet C (2017) Basile-Doelsch I (2017) Increasing
Agree. soil carbon storage: mechanisms, effects of agricultural practices and
proxies. a review. Agron Sustain Dev 37(2):1–27. https://​doi.​org/​10.​1007/​
Competing interests S13593-​017-​0421-2
All authors declare that there are no competing interests. Md Mashiur Rah- Ding Y, Liu Y, Liu S, Li Z, Tan X, Huang X, Zeng G, Zhou L, Zheng B (2016)
man is a member of the Carbon Research youth editorial board and was not Biochar to improve soil fertility a review. Agron Sustain Dev. 36(2):1–18.
involved in the editorial review, or the decision to publish this article. https://​doi.​org/​10.​1007/​S13593-​016-​0372-Z
Dun Q, Yao L, Deng Z, Li H, Li J, Fan Y, Zhang B (2019) Effects of hot and cold-
Author details pressed processes on volatile compounds of peanut oil and correspond-
1
Soil Science Division, Regional Agricultural Research Station, Bangladesh Agri- ing analysis of characteristic flavor components. LWT. 112:107648. https://​
cultural Research Institute, Jamalpur 2000, Bangladesh. 2 Agricultural Engineer- doi.​org/​10.​1016/J.​LWT.​2018.​11.​084
ing Division, Pulses Research Center & Regional Agricultural Research Station, Egamberdieva D, Reckling M, Wirth S (2017) Biochar-based Bradyrhizobium
Bangladesh Agricultural Research Institute, Ishurdi, 6620 Pabna, Bangladesh. inoculum improves growth of lupin (Lupinus angustifolius L.) under
3
Entomology Division & Biological Control Laboratory, Bangladesh Sugarcrop drought stress. Eur J Soil Biol 78:38–42. https://​doi.​org/​10.​1016/J.​EJSOBI.​
Research Institute, Ishwardi, Pabna 6620, Bangladesh. 4 Agricultural Engi- 2016.​11.​007
neering Division, Spices Research Center, Bangladesh Agricultural Research Egamberdieva D, Hua M, Reckling M, Wirth S (2018) Bellingrath-Kimura
Institute, Shibgonj, Bogura, Bangladesh. SD (2018) Potential effects of biochar-based microbial inoculants
in agriculture. Environ Sustain 1(1):19–24. https://​doi.​org/​10.​1007/​
Received: 4 July 2022 Revised: 17 January 2023 Accepted: 12 February S42398-​018-​0010-6
2023 Enders A, Hanley K, Whitman T, Joseph S, Lehmann J (2012) Characterization of
biochars to evaluate recalcitrance and agronomic performance. Bioresour
Technol 114:644–653. https://​doi.​org/​10.​1016/J.​BIORT​ECH.​2012.​03.​022
Fwanyanga FM, Horn LN, Sibanda T, Reinhold-Hurek B (2022) Prospects of
rhizobial inoculant technology on Bambara groundnut crop production
References and growth. Front Agron 4:94. https://​doi.​org/​10.​3389/​FAGRO.​2022.​10047​
Ahmmed S, Jahiruddin M, Razia S, Begum RA, Biswas JC, Rahman ASMM, 71/​BIBTEX
Ali MM, Islam KMS, Hossain MM, Gani N, Hossain MA, Sattar MA (2018) Ghazi AA, Karnwal A (2017) Potential for biochar as an alternate carrier to peat
Fertilizer Recomendation Guide- 2018 moss for the preparation of rhizobia bio inoculum. Microbiol Res J Int
Argaw A (2017) Development of environmental friendly bioinoculate for 18(4):1–9. https://​doi.​org/​10.​9734/​MRJI/​2017/​30828
peanut (Arachis hypogea L.) production in Eastern Ethiopia. Environ Syst Gundale MJ, DeLuca TH (2006) Temperature and source material influence
Res. 6(1):1–12. https://​doi.​org/​10.​1186/​S40068-​017-​0100-Y ecological attributes of ponderosa pine and Douglas-fir charcoal. For Ecol
Asadi H, Ghorbani M, Rezaei-Rashti M, Abrishamkesh S, Amirahmadi E, Chen- Manage 231(1–3):86–93. https://​doi.​org/​10.​1016/j.​foreco.​2006.​05.​004
grong C, Gorji M (2021) Application of rice husk biochar for achieving Hardy B, Sleutel S, Dufey JE, Cornelis JT (2019) The long-term effect of biochar
sustainable agriculture and environment. Rice Sci 28(4):325–343. https://​ on soil microbial abundance, activity and community structure is over-
doi.​org/​10.​1016/j.​rsci.​2021.​05.​004 written by land management. Front Environ Sci 7:110. https://​doi.​org/​10.​
Asante M, Ahiabor BDK, Atakora WK (2020) Growth, Nodulation, and Yield 3389/​FENVS.​2019.​00110/​BIBTEX
Responses of Groundnut (Arachis hypogaea L.) as Influenced by Com- Hartemink AE (2006) assessing soil fertility decline in the tropics using soil
bined Application of Rhizobium Inoculant and Phosphorus in the Guinea chemical data. Adv Agron 89:179–225. https://​doi.​org/​10.​1016/​S0065-​
Savanna Zone of Ghana. Int J Agron 2020. https://​doi.​org/​10.​1155/​2020/​ 2113(05)​89004-2
86917​57 He JZ, Shen JP, Zhang LM, Zhu YG, Zheng YM, Xu MG, Di H (2007) Quantita-
Azad AK, Miaruddin M, Wohab MA, Sheikh MHR, Nag B lal, Rahman MHH tive analyses of the abundance and composition of ammonia-oxidizing
(2020) KRISHI PROJUKTI HATBOI (Handbook on Agro-Technology), bacteria and ammonia-oxidizing archaea of a Chinese upland red soil
9th edn. Bangladesh Agricultural Research Institute, Gazipur-1701, under long-term fertilization practices. Environ Microbiol 9(9):2364–2374.
Bangladesh https://​doi.​org/​10.​1111/J.​1462-​2920.​2007.​01358.X
Bellè SL, Riotte J, Backhaus N, Sekhar M, Jouquet P, Abiven S (2022) Tailor-made International Biochar Initiative (2015) Standardized Product Definition and
biochar systems: Interdisciplinary evaluations of ecosystem services and Product Testing Guidelines for Biochar That Is Used in Soil
farmer livelihoods in tropical agro-ecosystems. PLoS One. 17(1):e0263302. Dejene D, Tilahun E (2019) Role of biochar on soil fertility improvement and
https://​doi.​org/​10.​1371/​JOURN​AL.​PONE.​02633​02 greenhouse gases sequestration. Hortic Int J. 3(6):291–8. https://​doi.​org/​
Blake GR (2015) Bulk Density. Methods Soil Anal Part 1 Phys Mineral Prop Incl Stat 10.​15406/​HIJ.​2019.​03.​00144
Meas Sampl. 374–390. https://​doi.​org/​10.​2134/​AGRON​MONOG​R9.1.​C30 Jatav HS, Singh SK, Jatav SS, Rajput VD, Parihar M, Mahawer SK, Singhal RK,
Blanco-Canqui H, Laird DA, Heaton EA, Rathke S, Acharya BS (2020) Soil carbon Sukirtee, (2020) Importance of Biochar in Agriculture and Its Conse-
increased by twice the amount of biochar carbon applied after 6 years: quence. Appl Biochar Environ Saf. https://​doi.​org/​10.​5772/​INTEC​HOPEN.​
field evidence of negative priming. GCB Bioenergy 12(4):240–251. https://​ 93049
doi.​org/​10.​1111/​GCBB.​12665 Karim MR, Halim MA, Gale NV, Thomas SC (2020) Biochar effects on soil physi-
Carlson KM, Gerber JS, Mueller ND, Herrero M, MacDonald GK, Brauman KA, ochemical properties in degraded managed ecosystems in Northeastern
Havlik P, O’Connell CS, Johnson JA, Saatchi S, West PC (2016) Greenhouse Bangladesh. Soil Syst. 4:69. https://​doi.​org/​10.​3390/​SOILS​YSTEM​S4040​069
gas emissions intensity of global croplands. Nat Clim Chang. 71(1):63–68. Kolton M, Graber ER, Tsehansky L, Elad Y, Cytryn E (2017) Biochar-stimulated
https://​doi.​org/​10.​1038/​nclim​ate31​58 plant performance is strongly linked to microbial diversity and metabolic
Dauda A, Usman B, Shekhar Kapoor C, Michael Ubi G (2019) Effect of soil com- potential in the rhizosphere. New Phytol 213(3):1393–1404. https://​doi.​
paction and bulk density on the growth and yield of soybean (Glycine org/​10.​1111/​NPH.​14253
max) on sandy clay loam soil of the semi-arid region of Northern Nigeria Kumar S, Diksha, Sindhu SS, Kumar R. (2022) Biofertilizers: An ecofriendly tech-
as Influenced by tractor wheel traffic. J Agric Ecol Res Int 18(1):1–6. nology for nutrient recycling and environmental sustainability. Curr Res
https://​doi.​org/​10.​9734/​JAERI/​2019/​V18I1​30048 Microb Sci. 2022;3:https://​doi.​org/​10.​1016/J.​CRMICR.​2021.​100094
De Tender C, Vandecasteele B, Verstraeten B, Ommeslag S, Kyndt T, Debode Kumari B, Mallick MA, Solanki MK, Solanki AC, Hora A, Guo W (2019) Plant
J (2021) Biochar-enhanced resistance to botrytis cinerea in strawberry Growth Promoting Rhizobacteria (PGPR): Modern Prospects for
Shikha et al. Carbon Research (2023) 2:10 Page 14 of 15

Sustainable Agriculture. Plant Heal Under Biot Stress :109–127. https://​ Murphy J, Riley JP (1962) A modified single solution method for the deter-
doi.​org/​10.​1007/​978-​981-​13-​6040-4_​6/​COVER/ mination of phosphate in natural waters. Anal Chim Acta. 27(C):31–36.
Kuzyakov Y, Subbotina I, Chen H, Bogomolova I, Xu X (2009) Black carbon https://​doi.​org/​10.​1016/​S0003-​2670(00)​88444-5
decomposition and incorporation into soil microbial biomass estimated Nigussie A, Kissi E, Misganaw M, G Ambaw (2012) Effect of biochar application
by 14C labeling. Soil Biol Biochem 41:210–219. https://​doi.​org/​10.​1016/j.​ on soil properties and nutrient uptake of lettuces (Lactuca sativa) grown
soilb​io.​2008.​10.​016 in chromium polluted soils. Am J Agric Environ Sci 12(3):369–376
Layek J, Narzari R, Hazarika S, Das A, Rangappa K, Devi S, Balusamy A, Saha S, Olsen SR, Cole CV, Watandbe F, Dean L (1954) Estimation of available phos-
Mandal S, Idapuganti RG, Babu S, Choudhury BU, Mishra VK (2022) Pros- phorus in soil by extraction with sodium bicarbonate. J Chem Inf Model
pects of biochar for sustainable agriculture and carbon sequestration: an 53(9):1689–1699
overview for Eastern Himalayas. Sustainability 14(11):6684. https://​doi.​ Page AL, Miller RHH, Keny DR, Kuny DR (1989) Methods of soil analysis-Part 2:
org/​10.​3390/​su141​16684 Chemical and Microbiological properties. (2nd edition). Am Soc Agron
Lehmann J, Rillig MC, Thies J, Masiello CA, Hockaday WC, Crowley D (2011) Inc PublMadison, USA 9(2):403–30
Biochar effects on soil biota - a review. Soil Biol Biochem 43(9):1812–1836. Panwar NL, Pawar A, Salvi BL (2019) Comprehensive review on production
https://​doi.​org/​10.​1016/j.​soilb​io.​2011.​04.​022 and utilization of biochar. SN Appl Sci 1(2):1–19. https://​doi.​org/​10.​1007/​
Lehmann J, Amonette JE, Roberts K (2010) Role of Biochar in Mitigation of S42452-​019-​0172-6/​FIGUR​ES/9
Climate Change. In: Handbook of Climate Change and Agroecosystems. Qambrani NA, Rahman MM, Won S, Shim S, Ra C (2017) Biochar properties and
pp 343–363 eco-friendly applications for climate change mitigation, waste manage-
Li J, Nedwell DB, Beddow J, Dumbrell AJ, McKew BA, Thorpe EL, Whitby C ment, and wastewater treatment: A review. Renew. Sustain. Energy Rev.
(2015) amoA gene abundances and nitrification potential rates suggest Rahman MM, Aravindakshan S, Hoque MA, Rahman MA, Gulandaz MA,
that benthic ammonia-oxidizing bacteria and not archaea dominate N Rahman J, Islam MT (2021) Conservation tillage (CT) for climate-smart
cycling in the Colne estuary. United Kingdom Appl Environ Microbiol sustainable intensification: Assessing the impact of CT on soil organic
81(1):159–165. https://​doi.​org/​10.​1128/​AEM.​02654-​14/​SUPPL_​FILE/​ carbon accumulation, greenhouse gas emission and water footprint of
ZAM99​91058​90SO1.​PDF wheat cultivation in Bangladesh. Environ Sustain Indic 10:100106. https://​
Li W, Hou Y, Long M, Wen X, Han J, Liao Y (2023) Long-term effects of biochar doi.​org/​10.​1016/j.​indic.​2021.​100106
application on rhizobacteria community and winter wheat growth on Rahman MM, Miah MS, Rahman MA, Riad MI, Sultana N, Yasmin M, Shikha FS,
the Loess Plateau in China. Geoderma. 429:116250. https://​doi.​org/​10.​ Kadir MM (2022) Designing an Energy Use Analysis and Life Cycle Assess-
1016/J.​GEODE​RMA.​2022.​116250 ment of the Environmental Sustainability of Conservation Agriculture
Liang B, Lehmann J, Sohi SP, Thies JE, O’Neill B, Trujillo L, Gaunt J, Solomon D, Wheat Farming in Bangladesh. Environ Footprints Eco-Design Prod Pro-
Grossman J, Neves EG, Luizão FJ (2010) Black carbon affects the cycling of cess :111–137. https://​doi.​org/​10.​1007/​978-​981-​19-​0534-6_​5/​TABLES/9
non-black carbon in soil. Org Geochem 41(2):206–213. https://​doi.​org/​10.​ Ramasamy M, Geetha T, Yuvaraj M, Ramasamy M, Geetha T, Yuvaraj M (2020)
1016/j.​orgge​ochem.​2009.​09.​007 Role of biofertilizers in plant growth and soil health. Nitrogen Fixat.
Liao H, Li Y, Yao H (2019) Biochar amendment stimulates utilization of plant- https://​doi.​org/​10.​5772/​INTEC​HOPEN.​87429
derived carbon by soil bacteria in an intercropping system. Front Micro- Rawat J, Saxena J, Sanwal P, Rawat J, Saxena J, Sanwal P (2019) Biochar: A
biol. 10(JUN):1361. https://​doi.​org/​10.​3389/​FMICB.​2019.​01361/​BIBTEX Sustainable Approach for Improving Plant Growth and Soil Properties.
Liao J, Liu X, Hu A, Song H, Chen X (2020) Zhang Z (2020) Effects of biochar- Biochar - an Imp Amend Soil Environ. https://​doi.​org/​10.​5772/​INTEC​
based controlled release nitrogen fertilizer on nitrogen-use efficiency of HOPEN.​82151
oilseed rape (Brassica napus .L). Sci Rep. 10(1):11063. https://​doi.​org/​10.​ Reckling M, Bergkvist G, Watson CA, Stoddard FL, Zander PM, Walker RL, Pristeri
1038/​S41598-​020-​67528-Y A, Toncea I, Bachinger J (2016) Trade-Offs between Economic and Envi-
Lin S, Wang W, Sardans J, Lan X, Fang Y, Singh BP, Xu X, Wiesmeier M, Tariq A, ronmental Impacts of Introducing Legumes into Cropping Systems. Front
Zeng F, Alrefaei AF, Peñuelas J (2022) Effects of slag and biochar amend- Plant Sci 7(MAY2016). https://​doi.​org/​10.​3389/​FPLS.​2016.​00669
ments on microorganisms and fractions of soil organic carbon during Rehman HA, Razzaq R (2017) Benefits of biochar on the agriculture and envi-
flooding in a paddy field after two years in southeastern China. Sci Total ronment - a review. J Environ Anal Chem 04(03):3–5. https://​doi.​org/​10.​
Environ. 824:153783. https://​doi.​org/​10.​1016/J.​SCITO​TENV.​2022.​153783 4172/​2380-​2391.​10002​07
Luo HH, Zhang YL (2016) Zhang WF (2015) Effects of water stress and rewa- Rillig MC, Mummey DL (2006) Mycorrhizas and soil structure. New Phytol
tering on photosynthesis, root activity, and yield of cotton with drip 171:41–53. https://​doi.​org/​10.​1111/j.​1469-​8137.​2006.​01750.x
irrigation under mulch. Photosynth 54(1):65–73. https://​doi.​org/​10.​1007/​ Romero CM, Hao X, Li C, Owens J, Schwinghamer T, McAllister TA, Okine E
S11099-​015-​0165-7 (2021) Nutrient retention, availability and greenhouse gas emissions from
Meier EA, Thorburn PJ, Bell LW, Harrison MT, Biggs JS (2020) Greenhouse gas biochar-fertilized Chernozems. CATENA. 198:105046. https://​doi.​org/​10.​
emissions from cropping and grazed pastures are similar: a simulation 1016/J.​CATENA.​2020.​105046
analysis in Australia. Front Sustain Food Syst 3:121. https://​doi.​org/​10.​ Rutigliano FA, Romano M, Marzaioli R, Baglivo I, Baronti S, Miglietta F, Castaldi S
3389/​FSUFS.​2019.​00121/​BIBTEX (2014) Effect of biochar addition on soil microbial community in a wheat
Miah M, Mondal M (2017) Oilseeds sector of Bangladesh: challenges and crop. Eur J Soil Biol 60:9–15. https://​doi.​org/​10.​1016/J.​EJSOBI.​2013.​10.​007
opportunities. SAARC J Agric 15(1):161–172. https://​doi.​org/​10.​3329/​sja.​ Sajid M, Rab A, Noor S, Shah M, Jan I, Khan MA (2011) Influence of Rhizobium
v15i1.​33146 Inoculation on growth and yield of groundnut cultivars. Sarhad J Agric
Milne E, Al AR, Batjes NH, Bernoux M, Bhattacharyya T, Cerri CC, Cerri CEP, 27(4):573–576
Coleman K, Easter M, Falloon P, Feller C, Gicheru P, Kamoni P, Killian K, Shakil M (2022) Peanut cultivation: Peanut Emerging as a Major Cash Crop. In:
Pal DK, Paustian K, Powlson DS, Rawajfih Z, Sessay M, Williams S, Wokabi Dly. Star. https://​www.​theda​ilyst​ar.​net/​busin​ess/​econo​my/​news/​peanut-​
S (2007) National and sub-national assessments of soil organic carbon emerg​ing-​major-​cash-​crop-​29884​16. Accessed 29 Jun 2022
stocks and changes: the GEFSOC modelling system. Agric Ecosyst Environ Simonin M, Le Roux X, Poly F, Lerondelle C, Hungate BA, Nunan N, Niboyet
122(1):3–12. https://​doi.​org/​10.​1016/J.​AGEE.​2007.​01.​002 A (2015) Coupling between and among ammonia oxidizers and nitrite
Morshed Al ATM (2002) MARS, MAH, MMI, MSH, MH (2002) yield and quality oxidizers in grassland mesocosms submitted to elevated CO2 and
of groundnut (Arachis hypogaea L.) as affected by hill density and nitrogen supply. Microb Ecol. 70(3):809–818. https://​doi.​org/​10.​1007/​
number of plants per hill. J Agron. 1(2):74–76. https://​doi.​org/​10.​3923/​ S00248-​015-​0604-9
JA.​2002.​74.​76 Smith P, Bustamante M, Ahammad H, Clark H (2015) Agriculture, Forestry and
Mulabagal V, Baah DA, Egiebor NO, Sajjadi B, Chen W-Y, Viticoski RL, Hayworth Other Land Use (AFOLU). In: Climate Change 2014 Mitigation of Climate
JS (2021) Biochar from Biomass: A Strategy for Carbon Dioxide Sequestra- Change. pp 811–922
tion, Soil Amendment, Power Generation, ­CO2 Utilization, and Removal of Steiner C, Glaser B, Teixeira WG, Lehmann J, Blum WEH, Zech W (2008) Nitrogen
Perfluoroalkyl and Polyfluoroalkyl Substances (PFAS) in the Environment. retention and plant uptake on a highly weathered central Amazonian
Handbook of Climate Change Mitigation and Adaptation. Springer, New Ferralsol amended with compost and charcoal. J Plant Nutr Soil Sci
York, NY, pp 1–64 171:893–899. https://​doi.​org/​10.​1002/​jpln.​20062​5199
Shikha et al. Carbon Research (2023) 2:10 Page 15 of 15

Tesfahun, 2018 W Tesfahun 2018 Effects of Biochar in Soil Chemical and Bio-
logical Property and Mitigating Climate Change : Review 10 1 2012 2015
Tripti KA, Usmani Z, Kumar V, Anshumali (2017) Biochar and flyash inoculated
with plant growth promoting rhizobacteria act as potential bioferti-
lizer for luxuriant growth and yield of tomato plant. J Environ Manage
190:20–27. https://​doi.​org/​10.​1016/J.​JENVM​AN.​2016.​11.​060
Van Beek CL (Christy), Elias E, G. Selassie Y, Gebresamuel G, Tsegaye A, Hun-
dessa F, Tolla M, Mamuye M, Yemane G, Mengistu S (2019) Soil organic
matter depletion as a major threat to agricultural intensification in the
highlands of Ethiopia. Ethiop J Sci Technol 11(3):271. https://​doi.​org/​10.​
4314/​ejst.​v11i3.5
Van Zwieten L, Singh B, Joseph S, Kimber S, Cowie A, Chan KY (2012) Biochar
and emissions of non-CO2 greenhouse gases from soil. In: Biochar for
Environmental Management: Science and Technology. pp 227–249
Wang H, Zhang R, Zhao Y, Shi H, Liu G (2022) Effect of biochar on rhizosphere
soil microbial diversity and metabolism in tobacco-growing soil. Ecol.
3(4):539–556. https://​doi.​org/​10.​3390/​ECOLO​GIES3​040040
Warnock DD, Mummey DL, McBride B, Major J, Lehmann J, Rillig MC (2010)
Influences of non-herbaceous biochar on arbuscular mycorrhizal fungal
abundances in roots and soils: results from growth-chamber and field
experiments. Appl Soil Ecol 46:450–456. https://​doi.​org/​10.​1016/j.​apsoil.​
2010.​09.​002
Wei M, Liu X, He Y, Xu X, Wu Z, Yu K, Zheng X (2020) Biochar inoculated with
Pseudomonas putida improves grape (Vitis vinifera L) fruit quality and
alters bacterial diversity. Rhizosphere. 16:100261. https://​doi.​org/​10.​
1016/J.​RHISPH.​2020.​100261
Woolf D, Amonette JE, Street-Perrott FA, Lehmann J, Joseph S (2010) Sustain-
able biochar to mitigate global climate change. Nat Commun. 1(1):1–9.
https://​doi.​org/​10.​1038/​ncomm​s1053
Yan H, Cong M, Hu Y, Qiu C, Yang Z, Tang G, Xu W, Zhu X, Sun X, Jia H (2022)
Biochar-mediated changes in the microbial communities of rhizosphere
soil alter the architecture of maize roots. Front Microbiol 13:3909. https://​
doi.​org/​10.​3389/​FMICB.​2022.​10234​44/​BIBTEX
Yanai Y, Toyota K, Okazaki M (2007) Effects of charcoal addition on N2O
emissions from soil resulting from rewetting air-dried soil in short-term
laboratory experiments: original article. Soil Sci Plant Nutr 53(2):181–188.
https://​doi.​org/​10.​1111/j.​1747-​0765.​2007.​00123.x
Yang S, Chen X, Jiang Z, Ding J, Sun X, Xu J (2020) Effects of biochar applica-
tion on soil organic carbon composition and enzyme activity in paddy
soil under water-saving irrigation. Int J Environ Res Public Health.
17(1):333. https://​doi.​org/​10.​3390/​IJERP​H1701​0333
Yeboah et al., 2020 S Yeboah P Oteng-Darko J Adomako ARA Malimanga 2020
Biochar application for improved resource use and environmental quality
Appl Biochar Environ Saf https://​doi.​org/​10.​5772/​INTEC​HOPEN.​92427
Yusif SA, Muhammad I, Hayatu NG, Sauwa MM, Tafinta IY, Mohammed MA,
Lukman SA, Abubakar GA, Hussain AM, Koller M (2016) Effects of biochar
and rhizobium inoculation on nodulation and growth of groundnut in
sokoto state. Nigeria J Appl Life Sci Int 9(2):1–9. https://​doi.​org/​10.​9734/​
JALSI/​2016/​27297
Zaman M, Tuhina-Khatun M, Ullah M, Moniruzzamn M, Alam K (1970) Genetic
variability and path analysis of groundnut (Arachis hypogaea L). Agric.
9(1–2):29–36. https://​doi.​org/​10.​3329/​agric.​v9i1-2.​9476
Zeng R, Wei Y, Huang J, Chen X, Cai C (2021) Soil organic carbon stock and
fractional distribution across central-south China. Int Soil Water Conserv
Res 9(4):620–630. https://​doi.​org/​10.​1016/J.​ISWCR.​2021.​04.​004
Zhang Q, Xiao J, Xue J, Zhang L (2020) Quantifying the effects of biochar
application on greenhouse gas emissions from agricultural soils: a global
meta-analysis. Sustain 12(8):1–14. https://​doi.​org/​10.​3390/​SU120​83436
Zoghi Z, Hosseini SM, Kouchaksaraei MT, Kooch Y, Guidi L (2019) The effect
of biochar amendment on the growth, morphology and physiology of
Quercus castaneifolia seedlings under water-deficit stress. Eur J for Res
138(6):967–979. https://​doi.​org/​10.​1007/​S10342-​019-​01217-Y/​FIGUR​ES/3

Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in pub-
lished maps and institutional affiliations.