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Discoveries in Agriculture and Food Sciences - Vol. 10, No. 4
Publication Date: August 25, 2022
DOI:10.14738/dafs.104.14379.
Kedir, M. (2022). A Review of Combined Use of Biochar with Nitrogen Fertilizer as an Instrument for Improving Maize Yield and
Soil Fertility. Discoveries in Agriculture and Food Sciences, 10(4). 32-38.
Services for Science and Education – United Kingdom
A Review of Combined Use of Biochar with Nitrogen Fertilizer as
an Instrument for Improving Maize Yield and Soil Fertility
Mohammed Kedir
Jimma Agricultural Research Center,
P.O. Box 192, Jimma, Ethiopia
ABSTRACT
The decline of soil fertility is one of the major problems around the world for
producing crops and ensuring food security. Therefore, the review's objective was
to examine how biochar and inorganic nitrogen fertilizers affect soil
physicochemical characteristics, as well as maize production and growth
parameters. Similarly, biochar is a product of the thermochemical decomposition
of biomass produced under limited oxygen. It has potential benefits in agriculture,
such as improving soil fertility, water retention. The nutrient composition of
biochar produced is determined by the type of feedstock used and the pyrolysis
conditions. A study showed that adding biochar and nitrogen fertilizer decreased
soil bulk density and enhanced water-holding capacity and soil chemical properties
like pH, nitrogen, phosphorus, potassium, organic carbon, calcium, ECEC, and base
saturation. Moreover, the review reported that the addition of N fertilizer and
biochar greatly promoted crop N uptake and N content, which then increased leaf
photosynthetic efficiency, dry matter accumulation, and grain yields. The findings
discovered that when the rate of biochar and nitrogen increased, crop productivity
and soil properties also increased significantly. It is concluded that applying
biochar along with nitrogen fertilizer increased maize crop productivity as well as
soil attributes more than applying biochar and nitrogen fertilizer separately.
Therefore, farmers and agricultural experts should consider incorporating these
practices into their land management strategies to improve overall agricultural
sustainability.
Keywords: biochar, nitrogen, soils, yield, rate, maize, growth, combination of biochar,
application
INTRODUCTION
The low yield of crop is due to reduced soil fertility, fluctuating rainfall, pest pressure, poor
farming practices, and limited availability of high-quality seeds (Katungi et al., 2010). Moreover,
soil acidity is one of the problems constraining crop productivity (Mesfin, 2007). Accordingly,
the major problems associated with soil acidity are the toxicity of aluminum (Al) and
magnesium (Mn) and the poor availability of essential plant nutrients (Kochian et al., 2004).
This highlights the importance of efficient nitrogen management practices that ensure optimal
crop yields while minimizing environmental damage (Jaynes et al., 2001). Therefore, it is crucial
to develop and implement sustainable nitrogen management strategies to address this issue.
Biochar is used as a carbon-rich soil amendment material to improve soil characteristics,
prevent nutrient loss, and promote agricultural production (Cui et al., 2020). The pyrolysis
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Kedir, M. (2022). A Review of Combined Use of Biochar with Nitrogen Fertilizer as an Instrument for Improving Maize Yield and Soil Fertility.
Discoveries in Agriculture and Food Sciences, 10(4). 32-38.
URL: http://dx.doi.org/10.14738/dafs.104.14379
process at relatively high temperatures (300–700 ° C) and low oxygen levels (Lehmann and
Joseph, 2009) also produces it. Due to its high carbon content and recalcitrant chemical
composition (Cheng et al., 2008), biochar has considerable promise as a climate change
mitigation tool (Woolf and Lehmann, 2012). This substance is frequently referred to as a "win- win-win" scenario because it produces energy from renewable materials and sequesters carbon
on a long-term basis while improving soil fertility indicators (Laird, 2008). An analysis by Woolf
et al. (2010) estimates that overall, biochar has the potential to sequester 12% of human CO2-
Ce emissions. Various residual biomasses, including manure, crop residues, wood residues,
forest, green, and agricultural wastes, as well as industrial wastes, are used to make biochar
(Novotny et al., 2015).
As different research indicates, biochar application to the soils can increase crop productivity
and also improve soil attributes. For example, Peng et al. (2021) findings suggest that biochar
compound fertilizers can increase carbon stability and nitrogen retention in soil, improve N
uptake by maize, while the loss of nitrogen is minimized, and thus may have an important
potential for improving the agroecosystem and ecological balance. The study showed that
maize yield increased from 28% to 140% after applying 20 t/ha of biochar compared to
untreated soil (Major et al., 2010). In comparison to applying biochar and nitrogen fertilizer
separately, applying the two together increased grain yield, nitrogen use efficiency, water
holding capacity, and soil physicochemical parameters (Oladele et al., 2019). Research by Khan
et al. (2021) has shown that the application of biochar can promote growth by increasing
chlorophyll content in wheat, thereby increasing yield. Wilson (2014) further explained that
from the past to the present, there are several processes in which biochar acts in the soil, with
numerous and diverse layers. As per Zhang et al. (2012), 20 and 40 t/ha of biochar mixed with
nitrogen fertilizer enhanced maize production by 8.8 and 12.1%, respectively. According to
Wang et al. (2016), 80 tons of biochar per acre increased soybean plant development. As a
result, the objective of this review was to examine the impacts of biochar and inorganic nitrogen
fertilizers on soil physicochemical properties as well as maize production and growth indices.
OVERVIEW OF BIOCHAR
Biochar is a product of thermochemical decomposition when heated to temperatures usually
between 300 and 1000 °C with limited oxygen (Domene et al., 2014). It has potential benefits
in agriculture, such as improving soil fertility, water retention, and reducing greenhouse gas
emissions (Jeffery et al., 2017; Major et al., 2018; Wu et al., 2018), but more research is needed
to understand its long-term effects. It has a large surface area, is highly porous, black in color,
lightweight, and has a high pH. The nutrient composition of biochar produced depends on the
type of feedstock and pyrolysis conditions (Shareef et al., 2018). Pyrolysis is classified as fast or
slow depending on the temperature and duration of heating. Both positive and negative effects
on soil quality and crop yield have been reported (Bass et al., 2016; Burrell et al., 2016).
The Soil's Chemical Properties are Affected by Applying Biochar
In general, soil with adequate structure, bulk density, porosity, organic matter, and soil pH
provides the ideal environment for enhanced root system growth and microbial multiplication,
resulting in increased crop yields. Likewise, biochar treated at a dose of 20 t/ha without
fertilizer considerably decreased bulk density by 12% and enhanced porosity by 12%,
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according to Tokova et al. (2020). In addition, applying biochar to the soil changed its microbes,
rooting patterns, aeration, water-holding capacity, and bulk density (Zafar et al., 2018). Thus,
according to a study by Sarfraz et al. (2017) on alkaline calcareous soil in Pakistan, adding
biochar considerably lowers soil pH while increasing electrical conductivity, cation exchange
capacity, and total organic carbon at greater rates. In other study, applying various rates of
biochar to acidic soil raises the carbon content by 35.0%, organic matter content by 35.1%, and
nitrogen content by 35.1% over the control treatment (Bayu et al., 2016).
Biochar, to be considered, is used as soil amendments. Similarly, in a study conducted by
Bhattarai et al. (2015) in Nepal from November 2014 to May 2015, there was a large rise in the
N, P, and K, pH, organic matter, organic carbon, and particle densities, but a decrease in the bulk
density was observed. The high adsorption capacity of biochar, which reduces nutrient loss
while increasing the available nutrient content and promoting crop growth, enhances the
physicochemical attributes of the soils (Wang et al. 2010; Chen et al. 2013). In a different study,
adding biochar raised the pH, cation exchange capacity, and organic carbon content of the soil
by 46%, 20%, and 27%, respectively; the use of biochar also decreased bulk densities by 29%
and improved porosity by 59% (Singh et al., 2022).
Maize Growth and Grain Yield are Affected by Applying Biochar
Biochar has the potential to improve soil attributes (physical, chemical, and biological),
resulting in increased crop growth and production. Accordingly, adding 20 t/ha of biochar
improved maize yield from 28% to 140% when compared to untreated soil (Major et al., 2010).
In addition, they noted that biochar was applied at rates of 8 and 20 t/ha, which decreased
exchangeable Al and Fe and markedly boosted maize production. According to Kuppusamy et
al. (2016), biochar particles have a large specific surface area, which makes them effective soil
modifiers for enhancing crop yield, raising nitrogen use efficiency, and reducing soil acidity.
These effects lead to significantly higher agricultural production and better soil quality.
Maize grain yield rose by 150% and 88% over an untreated plot when biochar was applied at
greater rates of 15 and 20 t/ha, respectively (Uzoma et al., 2011). As reported by (Yan et al.,
2022) from a study conducted on the soil quality and maize yield in Mollisols of Northeast China
from October 2017 to October 2020, higher amounts of biochar application can increase maize
crop yield, while lower amounts of biochar application tend to reduce maize crop yield.
According to Rawat et al. (2019), plant growth and development in biochar-amended soil are
directly related to nutrients released from biochar material and indirectly to favorable
responses owing to biochar application, such as nutrient savings or increased fertilizer-use
efficiency. As a result, past studies have noted a considerable rise in plant height and stem
diameter (Mensah and Frimpong, 2018).
Maize Growth and Grain Yield are Affected by Applying Combined Biochar and Nitrogen
Fertilizer
According to the study by Sarfraz et al. (2017), indicated that the interaction between nitrogen
levels and biochar rates had a substantial impact on maize plant height, fresh biomass, and dry
weight. As their research findings showed that the maximum mean maize plant height, shoot
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Kedir, M. (2022). A Review of Combined Use of Biochar with Nitrogen Fertilizer as an Instrument for Improving Maize Yield and Soil Fertility.
Discoveries in Agriculture and Food Sciences, 10(4). 32-38.
URL: http://dx.doi.org/10.14738/dafs.104.14379
fresh weight, and dry weight were recorded with an application rate of biochar 1% (w/w) and
nitrogen 50%, respectively, while the minimum mean maize plant height, shoot fresh weight,
and dry weight were recorded in the control (44.91cm, 90.33g, and 21.4g). According to these
authors, the treatment at rate of (biochar 1% (w/w) + N 50%) increased maize plant height and
dry weight above the control by 75.3% and 78.8%, respectively. Li et al. (2023) report the
addition of N fertilizer and biochar greatly promoted crop N uptake and N content, which
increased leaf photosynthetic efficiency, dry matter accumulation, and grain yields. They
discovered that the highest yields (14,928 kg/ha) were obtained by combining 276 kg/ha N
fertilizer with 15 t/ha of biochar and the highest NUE value (46.3%) was obtained by combining
204 kg/ha N fertilizer with 30 t/ha biochar. I general, Zhang et al. (2012) discovered that 20
and 40 t/ha biochar mixed with nitrogen fertilizer enhanced maize production by 8.8 and
12.1%, respectively.
Maize Growth and Grain Yield are Affected by Applying Nitrogen Fertilizer
As reported by Sharifi and Namvar (2016), the highest N rate (225 kg/ha) produced the highest
plant height (185.2cm), whereas plots with no N application produced the lowest value
(151.2cm). According to data from Woldesenbet et al. (2016), the application of 69 and 92 N kg
/ha resulted in the highest number of leaves per plant (17.2) while the application of no
nitrogen resulted in the lowest number of leaves per plant (15.8).Their findings indicated that
plant height increased as nitrogen levels rose; hence, the tallest plant (360.66cm) was grown
using 92 N kg/ha, and the shortest (347.33cm) using no nitrogen treatment. In other study,
Investigations conducted on maize crops in the Central Rift Valley of Ethiopia indicated that a
higher number of ears (1.33 per plant) was seen in treatments that received more nitrogen
(100 N kg/ha and 125 N kg/ha), while the control treatment had the lowest number of ears
(Tadesse and Kim, 2015).
Over the 2019 and 2020, growing seasons, the highest values of grains/row (43.7 and 42.1
grains), grains/ear (477.7 and 487.3 grains), and grain yield (4.7 and 4.8 t/ha) were recorded
from the nitrogen level of 366 kg N/ha, whereas the lowest values of grains/row (38.0 and 39.1
grains), grains/ear (417.7 and 425.3 grains), and grain yield (3.5 and 3.4 t/ha) were observed
from the nitrogen level of 192 N kg/ha (Gheith et al, 2022). Furthermore, nitrogen rates
substantially increased the grain yield, ranging from 4744.8 kg/ha of control treatment to
7355.5 kg/ha at an application of 225 N kg/ha (Sharifi and Namvar, 2016). Results of Fosu- Mensah and Mensah (2016) showed that the grain yield of Obatanpa maize in Ghana rose
significantly (p < 0.01) with the use of N fertilizer, reaching 80 N kg/ha.
Soil Properties are Affected by Applying Combined Biochar Along with Inorganic
Nitrogen Fertilizer
Biochar is very important for the improvement of soil properties in general. As a result, Oladele
et al. (2019) discovered that adding biochar to N fertilizer decreased soil bulk density and
enhanced water holding capacity as well as soil chemical properties like pH, nitrogen,
phosphorus, potassium, organic carbon, calcium, ECEC, and base saturation. In addition, as
reported by Tokova et al. (2020), biochar application at a rate of 10 t/ha in conjunction with
108 N kg/ha reduced bulk density and increased plant availability of water. The findings
showed that applying N fertilizer and biochar together might dramatically lower the pH of the
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soil and raise its levels of available phosphorus, potassium, mineral nitrogen, and organic
carbon (Li et al., 2023).
CONCLUSION
Biochar is a product of the thermochemical decomposition of biomass produced under limited
oxygen. It has potential benefits in agriculture, such as improving soil fertility, water retention.
The nutrient composition of biochar produced is determined by the type of feedstock used and
the pyrolysis conditions. A study showed that adding biochar and nitrogen fertilizer decreased
soil bulk density and enhanced water-holding capacity and soil chemical properties like pH,
nitrogen, phosphorus, potassium, organic carbon, calcium, ECEC, and base saturation.
Moreover, the review reported that the addition of N fertilizer and biochar greatly promoted
crop N uptake and N content, which then increased leaf photosynthetic efficiency, dry matter
accumulation, and grain yields. The findings discovered that when the rate of biochar and
nitrogen increased, crop productivity and soil properties also increased significantly. It is
concluded that applying biochar along with nitrogen fertilizer increased maize crop
productivity as well as soil attributes more than applying biochar and nitrogen fertilizer
separately. Therefore, farmers and agricultural experts should consider incorporating these
practices into their land management strategies to improve overall agricultural sustainability.
References
Bass, A. M., Bird, M. I., Kay, G. and Muirhead, B. (2016). Science of the Total Environment Soil properties,
greenhouse gas emissions and crop yield under compost, biochar and co-composted biochar in two tropical
agronomic systems. Science of the Total Environment, The, 550, 459–470.
https://doi.org/10.1016/j.scitotenv.2016.01.143.
Bayu, D., Tadesse, M. and Amsalu, N. (2016). Effect of biochar on soil properties and lead (Pb) availability in a
military camp in South West Ethiopia. African Journal of Environmental Science and Technology, 10(3), 77–85.
https://doi.org/10.5897/AJEST2015.2014
Bhattarai, B., Neupane, J. and Dhakal, S.P., 2015. Effect of biochar from different origin on physio-chemical
properties of soil and yield of garden pea (Pisum sativum L.) at Paklihawa, Rupandehi, Nepal. World Journal of
Agricultural Research, 3(4), pp.129-138.
Burrell, L. D., Zehetner, F., Rampazzo, N., Wimmer, B. and Soja, G. (2016). Geoderma Long-term effects of biochar
on soil physical properties. Geoderma, 282, 96–102. https://doi.org/10.1016/j.geoderma.2016.07.019.
Chen WF, Zhang WM, Meng J (2013) Advances and prospects in research of biochar utilization in agriculture. Sci
Agric Sin 46:3324–3333
Cheng CH, Lehmann J, Engelhard M (2008) Natural oxidation of black carbon in soils: changes in molecular form
and surface charge along a climosequence. Geochim Cosmochim Acta 72:1598–1610
Cui BJ, Cui EP, Hu C, Fan XY, Gao F (2020) Efects of selected biochars application on the microbial community
structures and diversities in the rhizosphere of water spinach (Ipomoea aquatica Forssk.) irrigated with
reclaimed water. Environ Sci 41:5636–5647. https://doi.org/10.13227/j. hjkx.202006087
Domene, X., Mattana, S., Hanley, K., Enders, A., and Lehmann, J. 2014. Medium-term effects of corn biochar
addition on soil biota activities and functions in a temperate soil cropped to corn. Soil Biology and Biochemistry
72:152-162.
Page 6 of 7
37
Kedir, M. (2022). A Review of Combined Use of Biochar with Nitrogen Fertilizer as an Instrument for Improving Maize Yield and Soil Fertility.
Discoveries in Agriculture and Food Sciences, 10(4). 32-38.
URL: http://dx.doi.org/10.14738/dafs.104.14379
Fosu-Mensah, B.Y. and Mensah, M., 2016. The effect of phosphorus and nitrogen fertilizers on grain yield,
nutrient uptake and use efficiency of two maize (Zea mays L.) varieties under rain fed condition on Haplic Lixisol
in the forest-savannah transition zone of Ghana. Environmental Systems Research, 5(1), pp.1-17.
Gheith, E., El-Badry, O.Z., Kandil, E.E., Lamlom, S.F. and Abdelsalam, N.R., 2022. Maize (Zea mays L.) productivity
and nitrogen use efficiency in response to nitrogen application levels and time. Frontiers in Plant Science, p.2149.
Jaynes, D.B., Colvin, T.S., Karlen, D.L., Cambardella, C.A., Meek, D.W., 2001. Nitrate loss in subsurface drainage as
affected by nitrogen fertilizer rate. J. Environ. Qual. 30, 1305–1314.
Jeffery, S., Abalos, D., Prodana, M., Bastos, A.C., van Groenigen, J.W., Hungate, B.A., et al. 2017. Biochar boosts
tropical but not temperate crop yields. Environmental Research Letter 12:053001.
https://doi.org/10.1088/1748-9326/aa67bd.
Katungi, F., Mutuoki, E. A. T., Setegn Gebeyehu, Karanja, D., Fistum Alemayehu, Sperling, L., Beebe, S. Rubyogo, J.
C. and Buruchara, R. 2010. Improving common bean productivity: An Analysis of socioeconomic factors in
Ethiopia and Eastern Kenya. Baseline Report Tropical legumes II. Centro Internacional de Agricultura Tropical -
CIAT. Cali, Colombia.
Khan, Z., Rahman, M., Haider, G., Amir, R., Rao, M. I., and Ahmad, S. (2021). Chemical and biological enhancement
effects of biochar on wheat growth and yield under arid field conditions. Sustainability 13:5890. doi: 10.3390/
su13115890
Kochian, L. V., Hoekenga, O. A. and Pineros, M. A. 2004. How do Crop Plants Tolerate Acid Soils? Mechanisms of
Aluminum Tolerance and Phosphorous Efficiency. Annual Review Plant Biology, 55: 459 - 93.
Laird, D., 2008. The Charcoal Vision: A Win-Win-Win Scenario for Simultaneously Producing Bioeneger,
Permanently Sequestering Carbon, while Improving Soil and Water Quality. Agronomy Journal, 100(1), p.178
Lehmann, J., and Joseph, S. 2009. Biochar for environmental management: an introduction. p. 1-12. In Lehmann,
J., and Joseph, S. (eds.) Biochar for environmental management, science and technology. Earthscan, London, UK.
Li, C., Zhao, C., Zhao, X., Wang, Y., Lv, X., Zhu, X. and Song, X., 2023. Beneficial Effects of Biochar Application with
Nitrogen Fertilizer on Soil Nitrogen Retention, Absorption and Utilization in Maize Production. Agronomy, 13(1),
p.113.
Mensah, A. K. and Frimpong, K. A. (2018). Biochar and/or compost applications improve soil properties, growth,
and yield of maize grown in acidic rainforest and coastal savannah soils in Ghana. International journal of
agronomy, 2018.
Mesfin Abebe. 2007. Nature and Management of Acid Soils in Ethiopia.
Novotny, E.H., Maia, C.M.B. de F., Carvalho, M.T. de M., and Madari, B.E. 2015. Biochar: Pyrogenic carbon for
agricultural use - A critical review. Revista Brasileira de Ciencia do Solo 39:321-344.
Peng, J., Han, X., Li, N., Chen, K., Yang, J., Zhan, X., Luo, P. and Liu, N., 2021. Combined application of biochar with
fertilizer promotes nitrogen uptake in maize by increasing nitrogen retention in soil. Biochar, 3, pp.367-379.
Rawat, J., Saxena, J. and Sanwal, P. (2019). Biochar: a sustainable approach for improving plant growth and soil
properties. In Biochar-An Imperative Amendment for Soil and the Environment. IntechOpen.
Sarfraz, R., Shakoor, A., Abdullah, M., Arooj, A., Hussain, A. and Xing, S., 2017. Impact of integrated application of
biochar and nitrogen fertilizers on maize growth and nitrogen recovery in alkaline calcareous soil. Soil science
and plant nutrition, 63(5), pp.488-498.
Page 7 of 7
38
Discoveries in Agriculture and Food Sciences (DAFS) Vol 10, Issue 4, August- 2022
Services for Science and Education – United Kingdom
Shareef, T. M. E., Zhao, B. and Filonchyk, M. (2018). Characterization of biochars derived from maize straw and
corn cob and effects of their amendment on maize growth and loess soil properties. Fresenius Environmental
Bulletin, 27(5 A), 3678-3686.
Sharifi, R.S. and Namvar, A., 2016. Effects of time and rate of nitrogen application on phenology and some
agronomical traits of maize (Zea mays L.). Biologija, 62(1).
Singh, H., Northup, B.K., Rice, C.W. and Prasad, P.V., 2022. Biochar applications influence soil physical and
chemical properties, microbial diversity, and crop productivity: a meta-analysis. Biochar, 4(1), p.8.
Tadesse, A. and Kim, H.K., 2015. Yield related traits and yield of quality protein maize (Zea mays L.) affected by
nitrogen levels to achieve maximum yield in the central Rift Valley of Ethiopia.
Toková, L., Igaz, D., Horák, J. and Aydin, E., 2020. Effect of biochar application and re-application on soil bulk
density, porosity, saturated hydraulic conductivity, water content and soil water availability in a silty loam
Haplic Luvisol. Agronomy, 10(7), p.1005.
Wang H, Lin K, Hou Z, Richardson B, Gan J (2010) Sorption of the herbicide terbuthylazine in two New Zealand
Forest soils amended with biosolids and biochars. J Soils Sediments 10:283–289. https://doi.org/10.1007/
s11368-009-0111-z
Wang, Y., Wei, Y., and Sun, J. (2016). Biochar application promotes growth parameters of soybean and reduces
the growth difference. Commun. Soil Sci. Plant Anal. 47, 1493–1502. doi: 10.1080/00103624.2016.1194988
Wilson, K. (2014). How biochar works in soil. Biochar J. 32, 25–33.
Woldesenbet, M. and Haileyesus, A., 2016. Effect of nitrogen fertilizer on growth, yield and yield components of
maize (Zea mays L.) in Decha district, Southwestern Ethiopia. International Journal of Research- Granthaalayah, 4(2), pp.95-100.
Woolf D, Amonette JE, Street-Perrott FA, Lehmann J, Joseph S (2010) Sustainable biochar to mitigate global
climate change. Nat Commun 1(1):1–9. https://doi.org/10.1038/ncomms1053
Wu, D., Senbayram, M., Zang, H., Ugurlar, F., Aydemir, S., Bruggemann, N., et al. 2018. Effect of biochar origin and
soil pH on greenhouse gas emissions from sandy and clay soils. Applied Soil Ecology 129:121-127.
Yan, S., Zhang, S., Yan, P. and Aurangzeib, M., 2022. Effect of biochar application method and amount on the soil
quality and maize yield in Mollisols of Northeast China. Biochar, 4(1), p.56.
Zafar, U., Akmal, M., Ahmed, M., Ali, M., and Jamali, A.Z. 2018. Effect of biochar on soil chemical properties and
nutrient availability in sandstone and shale derived soils. Journal of Biodiversity and Environmental Sciences
12(5):272-277.
Zhang, A., Liu, Y., Pan, G., Hussain, Q., Li, L., Zheng, J., et al. (2012). Effect of biochar amendment on maize yield
and greenhouse gas emissions from a soil organic carbon poor calcareous loamy soil from central China plain.
Plant Soil 351, 263–275. doi: 10.1007/s11104-011-0957-x