Shifting paradigms: development of high-efficiency biochar fertilizers based on nano-structures and soluble components

The potential of biochar to improve crop yields [1–3], increase resistance to plant disease [4–7], remove toxic substances from soil [8,9] and sequester carbon [10–12] is well documented. However, high application rates of biochar (between 2.5 and 20 tonnes ha-1) appear to be required to see significant improvements in plant yields [13]. The present cost of biochar in developed countries can vary from US$300 to $7000 tonne-1. At high appli-cation rates, therefore, the cost may not lead to a return on investment for the farmer/horticulturalist, and is certainly prohibitive for low input, extensive field crops. In developing countries, constraints on biochar used in agricultural applications relate more to the limited availability of biomass residues and to the time needed to manufacture large amounts of biochar, rather than to the production costs [14,15].

At least three approaches are being implemented to produce cost-effective biochar products that can be

applied at less than 500 kg ha-1 for use as fertilizer. In the first approach, biochar is incorporated at rates of approximately 100–200 kg ha-1 into bands with min-eral and chemical fertilizers (CFs) to increase N and P uptake efficiency [16]. The second approach involves the addition of approximately 5–20% biochar to organic material during composting, which is reported to reduce the time needed to obtain mature compost and to decrease N losses [17–19]. This has the potential to improve compost quality and reduce composting costs. Minerals, NPK fertilizer or an organic N source can also be added to the compost–biochar product before it is applied, generally at relatively high rates such as 10 tonnes ha-1. The third approach involves creating biochar-based fertilizers by pre- or post-pyrolysis treat-ments. In pre-pyrolysis methods, a mixture of biomass, ground rocks or minerals (e.g., clay, lime, basalt or ilmenite) and nutrients is subjected to slow, relatively

Carbon Management (2013) 4(3), 323–343

Shifting paradigms: development of high-efficiency biochar fertilizers based on nano-structures and soluble components

S Joseph*1,2,3, ER Graber4, C Chia1, P Munroe1, S Donne2, T Thomas5, S Nielsen5, C Marjo6, H Rutlidge6, GX Pan3, L Li3, P Taylor7, A Rawal8 & J Hook8

Many biochars have a complex carbon lattice structure with aromatic and aliphatic domains, acidic and basic groups, vacancies, metallic and non-metallic elements, and free radicals. Biochars also have separate mineral oxide, silicate and salt phases, and small and large organic molecules. In the rhizosphere, such constituents can be involved in chemical and biological processes along a soil–microbe–plant continuum, including nutrient cycling, metal chelation and stabilization, redox reactions, and free radical scavenging. It is hypothesized that the greater the amount of these nanoparticles and dissolved components, the greater will be plant and microbial responses. We provide suggestions for developing low-dose, high-efficiency biochar–nanoparticle composites, as well as initial field trial results and detailed characterization of such a biochar–fertilizer composite, to highlight the potential of such biochars.

PersPective

1School of Materials Science & Engineering, University of New South Wales, Sydney, NSW 2052, Australia 2Discipline of Chemistry, University of Newcastle, Callaghan, NSW 2308, Australia 3Nanjing Agricultural University, Nanjing 210095, China 4Institute of Soil, Water & Environmental Sciences, The Volcani Center, Agricultural Research Organization, POB 6, Bet Dagan 50250, Israel 5School of Biotechnology & Biomolecular Sciences & Centre for Marine Bio-Innovation, University of New South Wales, NSW 2052, Australia 6Solid State & Elemental Analysis Unit, Mark Wainwright Analytical Centre, University of New South Wales, NSW 2052, Australia 7Biochar Solutions, 73 Mount Warning Road, Mount Warning, NSW 2484, Australia 8NMR Facility, Analytical Centre, University of New South Wales, NSW 2052, Australia *Author for correspondence: Tel.: +61 243 695 108; Fax: +61 243 695 108; E-mail: [email protected]

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low temperature (350–450°C) pyrolysis. In post-pyrolysis meth-ods, biochar is mixed with ground rocks or minerals, nutrients and/or manures. These mixtures may be heated, or alternatively, reacted under ambient conditions [20]. For instance, an N-rich biochar was produced by reacting ammonia, CO

2 and water with biochar at

atmospheric pressure and ambient temperature [21].

In all these approaches, the micro- and nano-structures of the biochars and biochar com-

posites are highly heterogeneous and varied [22]. Our view is that such structures have a critical role in the agronomic value of biochars, and we suggest it is pos-sible to enhance these structures in order to develop low-dose, high-potency biochar-based fertilizers. This paper synthesizes data from a variety of disciplines to support this contention, and presents new data from a field trial comparing the efficacy of a post-pyrolysis biochar–mineral–nutrient blend with standard fertilizer practice in rice cultivation. The micro- and nano-scale features of the original biochar and biochar blend are intensively characterized and compared. We also pro-vide future perspectives detailing an expanding role for low-dose, high-efficiency biochar fertilizers, and suggest guidelines for their development.

How does mineral matter affect biochar properties?It is now well documented that biochar bulk physical and chemical properties vary as a function of the pyroly-sis process conditions (e.g., temperature and time), the type and concentration of mineral matter in the feed-stock, and the ratios of lignin, cellulose and hemicellu-lose in the biomass [23–26]. Micro- and nano-structures of biochars are also affected by many of the same param-eters, such that structures of biochars can be highly heterogeneous and complex [27,28].

Pure lignin starts to depolymerize at 160°C in an inert environment and is still converting at 900°C, while depolymerization of hemicellulose starts at approximately 220°C and is completed by 315°C [29]. Cellulose starts to depolymerize at 315°C and finishes at approximately 400°C. However, in natural composite materials such as biomass, the onset of depolymeriza-tion and reaction rates are much more complex. For example, using thermal gravimetry mass spectrometry ana lysis, Gray et al. reported a change in the endotherm of wood and an increase in surface area at approximately 425–475°C, which they attributed to the decomposition

of the complex polysaccharides [30]. Giuntoli et al. and Xu and Sheng carried out thermal gravimetry mass spectrometry on raw and leached high mineral ash agri-cultural residues [31,32]. They found that during pyroly-sis, a larger weight percentage of matter was volatilized at a given temperature from the leached biomass than the unleached biomass. The unleached biomass was also found to be more resistant to high-temperature oxida-tion. However, the maximum rate of release of volatiles from the leached biomass occurred at a higher tem-perature when compared with the unleached biomass. These observations indicate that the quantity and type of soluble mineral phases and elements that are part of the organic matrix change both the energy requirements for depolymerization and its kinetics.

In a detailed study of the transformation of high-ash grass and low-ash pinewood during heating in the absence of oxygen between 100 and 700°C, examined using near-edge x-ray absorption fine structure spectros-copy, Fourier transform infrared spectroscopy (FTIR) and x-ray diffraction [33], four general types of biochars consisting of unique mixtures of chemical phases and physical states were categorized:

� Transition chars, where the crystalline character of the precursor materials is preserved;

� Amorphous chars, where the heat-altered molecules and incipient aromatic polycondensates are randomly mixed;

� Composite chars, consisting of poorly ordered graphene stacks embedded in amorphous phases;

� Turbostratic chars, dominated by disordered graphitic crystallites.

However, the detailed fine structures were significantly different in the low- and high-mineral ash biochars, especially in those produced between 300 and 500°C. X-ray diffraction showed a significant increase in the surface concentration of inorganic phases in the high-ash grass biochars, and lower intensity and change in the lattice spacing of the graphene sheets compared with the low-ash chars. Similarly, FTIR spectra of the two chars had differences in peak absorbance and peak posi-tions between wave numbers of 1600 and 1000 cm-1. The near-edge x-ray absorption fine structure spectrum also indicated either greater abundance of oxygenated functional groups and/or differences in size and nature of the graphene sheets in the grass chars as compared with the wood chars.

Differences between biochars produced from high- and low-ash feedstocks were also found by Harvey et al., who studied depolymerization of the lignocellulose hydrogen bonding network and development of charge in biochars from grassy and woody feedstocks produced

Key terms

Biochar: Solid co-product of pyrolysis that is used as a soil amendment.

Pyrolysis: Thermal degradation of biomass in the near absence of air, producing gaseous, liquid and solid co-products that have energetic value.

Depolymerize: Process whereby the complex biopolymers (cellulose, hemicellulose and lignin) in biomass break down upon heating to form lower molecular weight organic molecules.

Redox reactions: Reactions involving gain (reduction) or loss (oxidation) of electrons.

Carbon Management (2013) 4(3) future science group324

Perspective Joseph, Graber, Chia et al.

along a highest treatment temperature (HTT) gradi-ent between 200 and 650°C [34]. They showed that the highest concentration of carboxylic functional groups occurred when a grass with a high content of cellulose, alkali salts and alkali metal oxides was pyro-lyzed between 400 and 450°C. They attributed this to a higher degree of cycloreversion oxidation as well as to more efficient oxidation of lignocellulose fragments to carboxylic acids. In contrast, cleavage of H-C bonds and their subsequent oxidation to carbonyls was less efficient in the woody feedstocks, leading to reduced surface charge at any given HTT as compared with the grassy feedstock.

In many cases, agricultural residues and woody wastes have significant amounts of attached soil parti-cles, which can be rich in Si, Al, Ca, Fe and Mg. Clays in the attached soil particles can give off volatiles (includ-ing hydrochloric and hydrofluoric acid) that assist in the pyrolysis of large organic molecules and, during pyroly-sis, may lead to increased functional groups at the car-bon surfaces [35]. Additional insights into the effects that the presence of soil minerals during biomass pyrolysis may have on biochar properties can be obtained from a study by Chen et al., in which three novel magnetic biochars were prepared by chemical co-precipitation of Fe3+/Fe2+ on orange peel powder that was subsequently pyrolyzed under different temperatures (250, 400 and 700°C) [36]. Transmission electron microscopy (TEM) revealed the formation of Fe

2O

3 magnetic nanoparticles

on the surface of the biochar. FTIR spectra showed a much greater concentration of C=O, C-O and aromatic carbon in the magnetic chars than in the chars that were not pretreated. At 400°C, the composite adsorbed more organic molecules (napthalene and p-nitrotoluene) than the composites manufactured at the other temperatures, and also more than the standard biochar.

We envision biochars that contain a significant quan-tity of soluble minerals and elemental metals as a series of microscopic voltaic (galvanic) cells in which there can be a flow of cations and anions, electrons and pro-tons between areas of different electrochemical potential (Figure 1) [37]. Mineral and carbon phases in biochar have different electrochemical potentials [38,39]. The carbon phase has a series of tubular pores (part of the original biomass structure) that can connect the different min-eral phases. These tubular pores are themselves porous at the nanometer scale, and there is also connectivity across the carbon phases. This porous structure can have similar properties to a semipermeable membrane, whereby two parallel carbon tubular pores with different concentrations of soluble metals can act as a galvanic cell [40]. When these biochars are placed in the soil and a rain or irrigation event takes place, the pores are filled with nutrient-rich water, which acts as an electrolyte. A series

of complex redox reactions can then take place, which are similar to those seen in electrochemical cells and in corrosion of metals in the environment (including soil). This especially applies for phases having redox-active elements such as Fe and Mn (Figure 1).

In many respects, the reactions that take place when there is movement of gases, cations and anions into and out of the pores of biochars are expected to be similar to the reactions of gases, cations and anions that take place in metals having crevices with multiple contami-nant phases (Figure 2) [41]. Previously reported results on the electrochemical properties of biochars indicate that the ability of biochars to donate electrons is greatest in biochars with high mineral ash content produced at lower temperatures (e.g., chicken manure biochar pro-duced between 400 and 450°C, compared with a high temperature wood biochar produced at 600°C) [38].

Shifting paradigms: development of high-efficiency biochar fertilizers Perspective

future science group www.future-science.com 325

Surface-bonded OH- flowdown the walls afteroxidation of carbon

Cations move downand anions move

up the pore

Root hair

Electrons used forbiofilm/microbial growth

Conformationchanges in proteins

Minerals

Deposit of inorganicand organiccompounds

Nanopores actas semi-permeable

membrane Root hairexudates

∆V, ∆pH

e-e-

Carbon Management © Future Science Group (2013)

Figure 1. Possible electrochemical and chemical reactions in a biochar pore.

The role of labile organic moleculesLike mineral components, labile organic molecules (LOM) of both low- and high-molecular weight, which accumulate at biochar surfaces and condense in pores during biochar production, have the poten-tial to inf luence multiple processes across the soil–rhizosphere–plant continuum. This is for a number of separate and interrelated reasons. Many LOM compounds, known to be phytotoxic or biocidal at high concentrations, could have hormonal effects at low concentrations; for example, inducing plant resis-tance to stress [7,42]. Another way in which LOM can indirectly affect plant responses is by changing the structure of the soil microbial community, perhaps by providing carbon compounds that only specific members of the microbial consortium can utilize, or by being toxic to weaker members of the consortium [43]. Biochar-induced changes in soil microbial com-munity structure could result in widespread changes in microbial functioning in the soil, thus affecting both nutrient cycling and soil gas emissions [44–47]. Biochar additions can increase microbial diversity in the soil and encourage beneficial soil microorganisms, which can directly enhance plant growth and induce systemic resistance [42].

While some LOM compounds are phytotoxic, others may induce seed germination. Karrikans, for instance, which are formed during pyrolysis and combustion of biomass, are known to promote seed germination and are believed to contribute to the germination bursts that frequently follow forest fires [48]. Other com-pounds formed during biomass pyrolysis may also play yet undetermined roles in plant growth. In particular, biochar macromolecular LOM are similar in character to humic substances [49], which have been long known to positively impact seed germination, root initiation, plant nutrition and total plant biomass [48].

Chemical assays measuring the ability of aqueous extracts of biochars to reduce metals revealed that the soluble fraction indeed has substantial ability to reduce oxidized metals, with extracts of low-HTT biochars being much more redox active than extracts of high-HTT biochars [50]. Aqueous extracts of low- and high-HTT biochars also reduced and solubilized Mn and Fe from different soils over a wide range of pH values, with the extract of the lower HTT biochar having a greater variety and concentration of soluble reducing agents, solubilizing more Mn and Fe than the extract of the higher HTT biochar [50]. In the studied systems, the dissolved organic matter fraction, in particular phenolic



Soil water film

Biofilm

O2 (g) OH-

Ca, Mg,P and FeKCl

K+

Anodic area

e- e-

e-

Cathodic area

Carbon matrix

Mineral phase high inFe compounds

MnS + 2H+ = Mn2 + H2S

Precipitates

Fe2O3

FeOOH

Cl-

O2 (g) + 2H2O + 4e- = 4OH-

Fe3+ + 2H2O = Fe(OOH) + 3H+

2Al3+ + 2OH- -> Al2O3 + 3H2O

Fe2O3 + 2H2O = 2Fe(OOH)

Fe2O3 + 6H-COONH4 =2(R-COO)3 Fe + 6NH3 + 3H2O

Al2 O3 + 4Cl- (adsorbed) = AlCl4-

2H+ + 2e- = H2

Fe2+ + H2O -> Fe(OH)+ + H+

Carbon Management © Future Science Group (2013)

Figure 2. Possible reactions in soils within a high-iron phase in biochar. In this schematic there is a complex series of redox reactions where Fe and Mn are being released into the soil solution and gases are being formed. Cl anions are being adsorbed into an alumina phase and then the resultant reaction results in the solubilizing of Al. Electrons from these reactions flow to the surface of the biochar where they take part in the reaction with oxygen to form hydroxide anions. This then results in formation of different Fe and Al oxide phases on the surface of the pore. Organic high-nitrogen compounds can react with iron oxides to precipitate on the iron phases. It should be noted that these are typical reactions of metals when placed in soils.

compounds, was proposed to be responsible for the main part of the reducing capacity, which was on a par with the reducing capacities of various humic and fulvic substances.

The implications of these results for the role of bio-char in a wide range of chemical and biological redox-mediated reactions in the soil could be wide reaching [50]. Redox-related processes in soil include microbial electron shuttling, nutrient cycling, free radical scavenging, pol-lutant degradation and contaminant mobilization or immobilization. Redox reactions mediated by biochar-derived chemicals could play a role in abiotic formation of humic structures in soils, resulting in increased soil organic carbon content and improved soil aggregation. Redox active structures could serve as electron shuttles between bacterial cells and Fe(III)-bearing minerals, taking part in bacterial reduction and immobilization of metals [51]. Since oxidation of biochar surfaces leads to continued release of redox-active, acidic and phenolic organics of both low- and high-molecular weight [52,53], as well as to sustained release of various soluble inorganic species [54], biochar is expected to continue to participate in redox reactions as it ages in the soil.

Besides expediting redox reactions, many LOM com-pounds are ligands possessing multiple carboxylate, phe-nol, alcohol or enol groups, known to form stable metal–organic complexes with metals having different oxidation states [42,49]. Formation of water-soluble metal–organic complexes can increase the concentration of metals in the aqueous phase and their bioavailability. This effect is well known for root exudates and humic substances. For instance, chelation of Fe and Zn by humic substances enhanced the metals’ solubility in nutrient solution and improved the growth of melons, soybean and ryegrass [55]. Formation of water-insoluble metal–organic complexes can also occur, resulting in an increase in soil organic matter content. When oxidized by Mn oxides, o- and p-polyhydroxyphenols precipitate as polymeric humic-like substances that are effective chelators of Al [56,57].

Changes that can occur after biochar is added to soilBiochar particles undergo substantial chemical changes during their residence in the soil, including disappear-ance of many of the inorganic phases. While some bio-char minerals are highly water soluble (e.g., KCl), others weather more slowly in soil via both biotic and abiotic processes [54]. It is known that weathering of minerals in rocks proceeds through microorganisms that ‘mine’ specific mineral phases for cations or anions, which then become more available to plants [58,59]. Rates of reac-tion depend on the nature of the crystal structure as well as other environmental factors. Fungi and bacte-ria can symbiotically form biofilms to enhance mineral

weathering rates [60]. Breakdown of minerals leads to formation of nanoparticles [61], and occurs preferen-tially at cleavage planes, dislocations and other defects in the mineral structure [62]. Nanoparticles can also form through precipitation where there is a high concentration of sparingly soluble dissolved cations and anions. Pre-cipitation of nanoparticles in conjunction with organic matter helps to stabilize the carbon. Nanoparticles have also been seen to adhere to cell walls of microorganisms where they may provide protection from predators [59]. Fe nanoparticles can participate in biotic and abiotic redox reactions, where they can be important as electron acceptors in carbon oxidation [63].

Notably, the redox properties of nanoparticles can be different from those of large particles due to specific quantum effects. Semiconductor nanoparticles exhibit molecular-like redox behavior with size-dependent redox potentials [61]. The surfaces of nanoparticle semiconduc-tors have modified local electronic structures, which can facilitate the creation of mobile electrons, or hole charge carriers, which can result in modification of Lewis acid or base characteristics [61]. These under-coordinated sites tend to be highly reactive. Since biochars produced at temperatures below 600°C are semiconductors consist-ing of heterogeneous mineral and organic phases that slowly degrade in soil, they may exhibit a number of properties similar to those of synthetic nanoparticles [64].

Both biotic and abiotic corrosion mechanisms can be responsible for microbially mediated transformations between soluble and insoluble metal species [59]. Micron-scale electrochemical corrosion cells can develop when biofilms with a range of microorganism colonies form on mineral surfaces on biochars [59]. As redox reactions take place, micron scale pits are formed and a series of phases develop (Figure 2). Areas become anodic when metals lose electrons and go into solution, resulting in the flow of electrons to areas that are aerobic. Microbial exudates (exopolymers and organic acids) can increase reaction rates both by forming complexes with metals and by lowering pH. Certain bacteria can even generate sulfu-ric acid by means of oxidizing sulfur compounds [65]. These same processes may be responsible for some of the changes that occur to biochar in the soil, such as release of soluble pyrogenic condensed aromatic structures [52]. These structures are extensively substituted with oxygen-containing functional groups, indicating both oxidation and dissolution of the charcoal black carbon [66]. There is abundant spectroscopic evidence that natural weathering or oxidative depolymerization of soil charcoal results in the formation of soil humic substances [66].

A growing body of literature suggests that some bio-chars have a greater impact on crop yields as they age in soil [1,67]. Joseph and colleagues carried out detailed examinations of biochars that had been in the soil from



6 months to 3 years, and much older deposits containing agglomerates having a small percentage of biochar along with other forms of organic

matter [27,28,68,69]. Biochar particles were found to have reacted with minerals, organic matter and microorgan-isms during their aging in the soil. Key findings from their comparisons of aged biochar particles to fresh bio-char particles include:

� The content of oxygen on the surface was higher. A wide range of functional groups were detected including COOH, C=O and C-O;

� There was an increase in amino-acid N and a decrease in N-C. Some of the N was associated with a high Fe phase, suggesting that the organic N may have been associated with microbes;

� Na, K, P and Cl disappeared, and Ca was significantly reduced. In contrast, Al, Si, Fe, Mn and Ti increased on surfaces and in the pores of the aged biochar;

� Newly formed Ca/P rich phases together with Al/Si/Fe phases were detected in the pores of the aged biochar. Some of these phases had dimensions smaller than 50 nm;

� Fe(II) and Fe(III) were associated with S at surfaces of biochar pores;

� There was an increase in the concentration of radicals in the aged biochar as measured using electron spin resonance spectroscopy;

� The structure and distribution of the various phases that formed on the surfaces of the aged biochars were heterogeneous;

� Mesopores and macropores formed at mineral–organic interfaces during aging.

In addition to these chemical changes, complex micro-bial communities become established on the surfaces and in the pores of biochar in soil [70,71]. Analysis of microbial communities by sequencing of the 16S rRNA gene indicated a high abundance of non-nodularizing N fixating bacteria not only in the soil [70], but also on the surfaces of the biochar [72]. Biofilms were detected on the surfaces of biochar particles after being in soil 4 months, and they appeared to preferentially form on mineral phases with a significant content of Fe, S, Al and Si, as well as C, Ca, K, P, Mn and Ti [72]. Much more research is required to understand the interaction between mineral phases in the biochar and the abun-dance of specific microorganisms on the surfaces and in the pores of biochars.

Altogether, these many aging-related changes to micro- and nano-structures of biochar are related to complex physical and chemical processes that occur in soil during wetting and drying cycles, including altera-tions in solution Eh and pH, development of microbial communities on initially sterile biochar, interactions of biochar particles with roots and root hairs and their exu-dates, and more. These environmental factors result in a cascade of secondary chemical and biological reactions. Net changes will be influenced also by the particular soil and biochar types. Plant roots, in particular root hairs, can strongly affect these processes, as the release of acidic exudates in biochar pores can cause changes in the Eh and pH in microsites. This will result in increased dissolution of cations, which in turn can increase uptake by microorganisms and plants. Such findings related to overall kinetics and energetics of weathering of miner-als in the presence of microbial communities have been reported [58,59].



Table 1. Summary of field trial results†.

Treatment (t ha-1) Chemical fertilizer Wheat straw biochar composite fertilizer

Saleable grain yield 8.21 ± 0.75bB 11.44 ± 1.12aA Biomass yield 34.47 ± 5.41aA 41.44 ± 3.36aA†Values with different lower case letters in the same row are significantly different (p < 0.05), while those with different upper case letters are very significantly different (p < 0.01).

Table 2. Changes in nitrogen uptake in root, shoot and grains under different fertilizer treatments†.

Treatment N content (g·kg-1) N uptake (kg·ha-1)

N uptake by grain/N uptake by shootRoot Shoot Grain Shoot Grain

Chemical fertilizer

9.32 ± 1.29aA

8.45 ± 0.54aA

15.18 ± 1.29aA

53.85 ± 9.60aA

124.67 ± 11.43aA

2.34 ± 0.24bB

Wheat straw biochar composite fertilizer

6.61 ± 0.74bA

6.66 ± 0.18bB

13.43 ± 0.29aA

48.51 ± 3.83aA

153.56 ± 15.02aA

3.17 ± 0.17aA

†Values with different lower case letters in the same column are significantly different (p < 0.05), while those with different upper case letters are very significantly different (p < 0.01).

Table 3. Indices of rice nitrogen-use efficiency under different fertilizer treatments†.

Treatment Total N applied(kg·ha-1)

NPFP (kg·N kg-1)

HIG(kg·kg-1)

NHI(kg·kg-1)

NGPE(kg·kg-1)

CF 210 39bB 0.24bA 0.70bA 46bBWSF 168 68aA 0.28aA 0.76aA 56aA†Values with different lower case letters in the same column are significantly different (p < 0.05), while those with different upper case letters are very significantly different (p < 0.01). CF: Chemical fertilizer (16–16–16, N:P2O5:K2O in 100 g); HIG: Harvest index of grain (= rice yield [kg ha-1]/aboveground biomass production [kg ha-1]); NGPE: Grain production efficiency of N (= rice yield [kg ha-1]/total N in rice plants [kg ha-1]); NHI: Harvest index of nitrogen (= total N of ears [kg ha-1]/total N in rice plants [kg ha-1]); NPFP: Productivity of nitrogen (= rice yield[kg ha-1]/total N input [kg N ha-1]); WSF: Wheat straw biochar–fertilizer composite composed of wheat straw biochar (~25%), bentonite (~5%), urea CO(NH2)2, KCl and monoammonium phosphate (NH4H2PO3) to give a N:P2O5:K2O ratio by weight of 18:9:10 in 100 g.

Key term

Eh: Reduction potential, measured in volts or millivolts.

Redox reactions that occur on the surface of bio-char, or as a result of release of redox active compounds and elements from the biochar, can provide metabolic energy for prokaryotes [61]. Moreover, the concentra-tion of electron donors (e.g., organic C) and acceptors (e.g., O

2 and NO

3) and microbial population dynam-

ics potentially influence mineral colloidal stability in soils via biogeochemical pathways. As noted by Gadd, formation of biofilms with a variety of microorgan-isms that weather the minerals in biochar will increase reaction rates significantly [59]. More importantly, the loss of minerals at the carbon–mineral interface can lead to an increase in surface area, formation of pores and development of charged surfaces. Studies on bio-char-based microbial fuel cells have highlighted the role of microorganisms in both oxidation and reduc-tion reactions and the shuttling of electrons to and from the carbon surfaces [73]. Electron and proton

f low have many important impacts on processes in the rhizosphere.

Gilbert and Banfield noted that magnetic nanopar-ticles could be formed through biological-mediated organic/inorganic interactions [61]. Joseph et al., using electrochemical impedance spectroscopy, reported that currents could be induced in fresh and aged biochars (including black carbon-containing particles from Terra Preta soils) with a significant content of magnetic Fe oxide particles [38]. Sarafik et al. reviewed the magnetic properties of activated carbon and biochars having mag-netic Fe oxide particles both in the pores and on the surface [74]. They found that the effectiveness of acti-vated carbon as a catalyst for a range of organic and inorganic reactions and as an adsorbent increased with the addition of Fe nanoparticles. Magnetic fields can play important roles in nutrient cycling and soil reme-diation [75]. It is not inconceivable that biochars with a



A Wheatstraw biochar

1696

1575

C=O & COOR

C=C

C-O1372

1032872

34433343 3203

N-H

Wheatstraw biochar + NPKB

1658O=C(NR2)2 1615

1591

1444

C=C

1032

872 781

C-O

3443 3342

3203

N-H

UreaC

1681

C=O& NH2

NH2

1627

1600

1463

1153

C-N

2924

2853

N-H & PO-H

Ammonium phosphateD1460

NH2

1202

P=PP-O

1076 1054956

NH2, NH4, NO3

4000 3000 2000

Wavenumber (cm-1)

1500 1000 500

A

O

H2N NH2

Figure 3. Stack plot of Fourier transform infrared spectroscopy absorbance spectra. (A) Wheatstraw biochar, (B) wheatstraw biochar–fertilizer composite (indicated in figure as wheatstraw biochar plus NPK), (C) pure urea and (D) ammonium phosphate dibasic. Spectra (C) and (D) are taken from the Thermo Fisher Library of standard Fourier transform infrared spectroscopy spectra [101].

high content of magnetic Fe oxide nanophases could result in an increase in magnetotactic bacteria in soil [76]. Bazylinski and Blakemore noted that magnetosomes can play a major role in denitrification [77]. This is a promis-ing area that requires careful research to determine the effects of the addition of magnetic particles on nutrient cycling, changes in microbial populations, removal of toxic substances and changes in fluxes of GHGs.

Replacing or enhancing NPK CFs with biochar-based fertilizers

� Hypothesis formulationTo develop biochar products that are both active at low application rates and cost-effective to produce, a clear understanding of the principles governing biochar efficacy is needed. According to our view, based on the literature reviewed above, effective biochars need

to have high concentrations of functional groups that capture nutrient elements, and nanophase mineral mat-ter and labile organic compounds that catalyze a range of biotic and abiotic reactions, which reduce the energy expended by the plant to take up nutrients, improve plant resistance to stress, stabilize soil organic matter and increase plant growth-promoting microbes that solubilize locked up nutrients and fix N. To under-take such an endeavor, the techniques and materials developed by industries and researchers that produce activated carbon, catalysis nanomaterials and microbial fuel cells need to be harnessed. The activated carbon industry has developed a range of techniques that either involve pretreatment of the biomass or post-treatment of the carbon matrix to enhance its properties. These include deposition of magnetically responsive nanopar-ticles [74], functionalization and increase in surface area



A

Wavenumber (cm-1)

4000 3000 2000 1500 1000

3339 3196

Wheatstraw biochar + NPKA

N-H

1617 1592

1446

C=C NH2

1652O=C-(NR2)2

1034

13161409

1114

1446

NH2

1642O=C-(NR2)2

B Polyacrylamide3179

3327

C-H2923

N-H

1598

NH2O

n

500

Figure 4. Stack plot of Fourier transform infrared spectroscopy absorbance spectra. (A) Biochar–fertilizer composite and (B) polyacrlylamide. Taken from the Thermo Fisher Library of standard Fourier transform infrared spectroscopy spectra [101].

through reaction of the biomass or the carbon with KOH or H

3PO

4 [78,79], or ammonization and treatment

with strong acids [80]. Chemicals and minerals can then be bound to the biochar surface in such a way that the rate of release of specific macro- and micro-nutrients can be controlled.

The following is a series of working hypotheses about the governing principles:

� The type and concentration of mineral phases (metal oxides, carbonates, sulfates/sulfides, phosphates and chlorides) in biochar have at least the same importance in its efficacy as a soil amendment as the organic matrix, if not more so. The smaller the mineral phases at biochar surfaces (in particular, less than 100 nm), the more effective they are at catalyzing reactions involved in nutrient cycling and adsorption of organic and inorganic compounds. Moreover, the smaller the phases, the more available will be the nutrients for growth of beneficial microorganisms and uptake by plant roots;

� Hydrophilic water-soluble organic molecules in biochars are more likely to form and adhere at mineral surfaces, mineral–carbon interfaces and carbon-surface oxygenated functional groups than at carbon matrix surfaces. Insoluble (hydrophobic) organic molecules are more likely to undergo adsorption interactions with the condensed aromatic surfaces of the carbon matrix and to condense in pores;

� When biochars are added to soil, both abiotic and biotic reactions preferentially take place at air or water mineral–organic phase interfaces or where metal atoms are ionically bound in the organic matrix;

� There will be a change in both Eh and pH of the soil immediately around biochar particles. The magnitude of these changes is a function of the soil water content, the concentration and the solubility of the mineral phases and LOM on the surfaces of the biochar, and the quantity of water in the biochar pores;

� A unique community of microorganisms will develop preferentially at the mineral–organic interfaces on the surfaces and in the pores of each individual biochar particle. The nature of this community will be affected by the composition of both organic and mineral phases and their relative proportion, the biochar pore structure (interconnectivity, size), development of aerobic and anaerobic microsites, and the presence of root hairs in the pores or at surfaces. This unique community plays a key role in the gas transfer and redox reactions of gases, metals, cations and anions, and organic species both on the surface of the biochar and in macropores having a diameter greater than 1 µm;

� The ability of biochar to promote plant development is related to the complex electrochemical environment that develops in response to the varied chemical and microbial reactions occurring in the presence of these varied nanomineral and organic phases.

Much work is still required to validate these hypotheses.

� Case studyResults of preliminary field trials carried out by Nanjing Agricultural University (Jiangsu, China) with a biochar–clay–CF composite are provided to illustrate the improve-ments in crop response that may be achieved by post-pyrol-ysis treatment of biochar with CFs. The original biochar and the biochar–fertilizer complex were examined to char-acterize the changes in their micro- and nano-structure that may have contributed to the improved crop response.

Table 4. High-resolution x-ray photoelectron spectroscopy analysis of carbon and nitrogen on wheatstraw biochar and biochar–fertilizer composite.

Region scans (C1s & N1s)

Structure Wheat straw biochar

Biochar–fertilizer composite

Beam energy (eV)

Atomic percent (%)

Beam energy (eV)

Atomic percent (%)

C1s A C-C/C-H 285.1 75.2 285.0 33.3C1s B C-O 286.6 14.2 286.6 18.2C1s C C=O 288.1 5.3 288.0 4.9C1s D O=C-O or

O=C-N289.5 3.6 289.2 7.0

C1s E O=C-N-C*(=O)NH2 291.0 12.2N1s A Quaternary or

N-C-COOH401.1 1.5 401.2 16.9

N1s B NO groups 402.8 5.6N1s C NH2 groups 399.2 0.3 399.7 1.8Atomic percentage values have been scaled to 100%.



O

H2N NH2

NH2

O

R

R

OH+ H+,- NH3,- CO2

O

OH

NH

R

R

O

O

O

NH

R

R

O

O

Figure 5. A possible mechanism for the reaction of wheat straw biochar with urea. A possible reaction pathway that could occur between (A) urea and (B) the anhydride groups expected on wheatstraw biochar. (C) Carboxy urea derivatives and (D) the consequent ring closure product are consistent with the spectroscopic data.

Biochar was produced from wheat straw (wheat straw biochar; WSB) by the San Li New Energy Com-pany (Henan, China) in a gasifier at approximately 460–500°C. This WSB was field tested at application rates of 20 and 40 tonnes ha-1 [81–83]. Results of those field trials showed increases in yields of maize of 15% and of rice of 5% at application rates of 40 tonnes bio-char ha-1. The field trials also found that decreasing the amount of chemical N in the form of urea/monoam-monium phosphate by 50% and adding 20 tonne ha-1 biochar also increased yields over an equivalent reduc-tion in the CF. Interviews carried out with farmers

indicated that, at a cost of WSB at approximately $250 tonnes, use of 20 tonnes ha-1 of biochar would result in loss of income.

Based on published research on the activating of biomass and biochars with compounds containing N, P and K, researchers at Nanjing Agricultural University hypothesized that combin-ing standard CFs and clay minerals with WSB would result in greater yields of grain with lower application rates of N. The composite biochar–clay–CF (WSB composite fertilizer; WSF) contained WSB (~25%), ben-tonite (~5%), urea CO(NH

2)2, KCl

and monoammonium phosphate to give a N:P

2O

5:K

2O ratio by weight

of 18:9:10 in 100 g of fertilizer. These ingredients were blended and allowed to react together without mixing in sealed containers under ambient conditions over a period of 4 weeks before incorporating into the soil with the seed. The control treatment was standard farmer practice of CF with the total nutrient content of 48% (N:P

2O

5:K

2O = 16:16:16).

Different levels of total input of N were planned for the biochar–fertil-izer composite treatment and control treatment (WSF = 168 kg ha-1 and CF 210 kg ha-1) on the basis of the previous trials using WSB. Initial application rates of both fertilizers were 450 kg ha-1 with an additional 51 kg ha-1 urea. A top dressing of urea was applied in the late tillering stage and heading stage at the rate of 60 kg ha-1 in the WSF treatment and 75 kg ha-1 in the CF treatment. Details of the trial methodology and

soil properties are provided in the Supplementary Data. Results of the WSF versus CF trial are provided in

Tables 1–3. Statistically significant increases in grain yield were found in the WSF treatment. Productiv-ity of N, harvest index of grain, harvest index of N and grain production efficiency were also significantly higher.

To determine possible reasons for the significant improvement in grain yield and N use efficiency indi-ces (Tables 1 & 3), despite lower N application with WSF, an examination of the micro- and nano-structure of the WSB and WSF was undertaken using FTIR, x-ray



180 160 140 120 100 80 60

13C MAS NMR at 7 Tesla (ppm)

O

=

NCN

A

B

C

D

E

C=OCOO

C-O

aromatic C-H

aromatic C

Figure 6. 13C nuclear magnetic resonance spectra of wheat straw biochar. (A, B & C) without and (D & E) with fertilizer treatment. (A) Acquired with direct polarization with a Hahn echo and decoupling throughout, while (B) was acquired with the decoupling turned off during the Hahn echo. (C) Is the difference between (A) and (B). (D) Acquired with 13C(1H) cross polarization with magic angle spinning for sensitivity enhancement, while (E) was acquired with direct polarization and a Hahn echo before detection. MAS: Magic angle spinning; NMR: Nuclear magnetic resonance.

photoelectron spectroscopy (XPS), scanning electron microscopy and TEM. Detailed methods using this equipment are given by Zhang and colleagues [83–85].

Figure 3 is a set of infrared spectra demonstrating the influence of fertilizer additives on WSB. Figure 3A is pure WSB and Figure 3B shows the same WSB combined to make the biochar composite fertilizer, WSF. The spectral differences can only be attributed to chemi-cal reaction with one or all of the additives. The WSB in Figure 3A shows a strong peak at 1575 cm-1 that can be assigned to aromatic ring stretching (signified by C=C), and a shoulder at approximately 1696 cm-1 that can be assigned to C=O stretching in ketone and car-boxylate derivatives. In Figure 3B, new peaks appear that are not found in the untreated WSB. The new peaks can also be compared with spectra of the four addi-tives; peak positions do not match those found in pure

urea Figure 3C (especially two distinct absorption peaks at 1682 cm-1 and 1465 cm-1), ammonium phosphate Figure 3D, or bentonite clay (not shown) and potassium chloride (an infrared silent material). The presence of unique peaks in Figure 3B confirms that a reaction has occurred between the WSB and the additives. Of the four additives, an acid-catalyzed nucleophilic addition of ammonia (derived from decomposition of urea) to carboxylate derivatives acid is the most likely reaction pathway based on the available materials.

A comparison of the WSF FTIR spectrum against a library of FTIR spectra reveals a striking similarity of parts of the spectrum to that of polyacrylamide. Figure 4 shows the infrared spectrum of WSF (Figure 4A) with a standard polyacrylamide spectrum (Figure 4B). Similarities are seen in the hydrogen-bonded N-H stretching region and the carbonyl stretching region at



COKClSiMgPS

60

80

100C

ou

nts

0

20

40

100Distance (µm)

20 30 40 50

100 µm

100 µm 10 µm

Figure 7. Scanning electron microscopy images of a wheatstraw biochar particle. (A) Electron backscattered image (FEI NanoSEM operating at 15 kV) with (B) energy dispersive x-ray spectroscopy (EDS) elemental maps for C, Si, K and Cl (a Bruker silicon drift detector EDS system had been interfaced). (C) Higher magnification backscattered electron image of a wheatstraw biochar particle showing submicron mineral phases on the surface; (D) EDS line scan taken across the region indicated by the arrow in (C).

1642–1652 cm-1, which can be attributed to the primary amide group found on chains of polyacrylamide. The formation of primary amide groups on the biochar is easily rationalized by the availability of ammonia in the mixture from ammonium phosphate and ammo-nia liberated by acid-catalyzed urea hydrolysis. Clearly, a proportion of the urea is decomposed to ammonia, which is available to react with carboxylate derivatives on the biochar to form primary amides, since the infra-red no longer shows significant peaks expected from the urea molecule.

Aside from decomposition to ammonia, urea might also be expected to react with carboxylic acid anhy-drides likely to be present on the WSB to form car-boxyurea adducts (Figure 5C) that could cyclize to a maleimide (Figure 5D). Reactions between anhydrides and urea are common industrial processes, although they require heating to be commercially viable; for example, in the reaction of urea with phthalic anhy-dride to synthesize the pigment phthalocyanine. Any reaction that has occurred between urea and groups on the biochar has occurred at room temperature, perhaps in the presence of microorganisms, so the scheme state in Figure 5 is speculative, although the duration available for reaction was significant (4 weeks) and the struc-tures are consistent with the infrared and photoelectron spectroscopic data.

The interpretation of the infrared ana lysis is sup-ported by the XPS results shown in Table 4. As expected, a significant increase in the proportion of N 1s photoelectrons is observed from the addition of urea to form organic bound NH

2 (399.7 eV) and

ammonium phosphate (401.2 eV). Less easily assigned is a higher energy peak at 402.8 eV that is typical of NO groups. This may be nitrate present in the ben-tonite clay, or formed from an oxidative process on the inorganic N. This assignment is supported by the broad infrared peak at 1444 cm-1, as nitrate would be expected to absorb at 1420–1330 cm-1 [86]. A strik-ing result in the C 1s spectrum (Supplementary Data & Supplementary Figure 1) is a 12.2 atomic percentage peak at 291 eV, 6 eV higher than the C 1s found in saturated hydrocarbons. The chemical environment associated with such a high C 1s binding energy is normally associated with carbon bound to highly elec-tronegative f luorine groups. However, only 1.5 atomic percentage of the sample was found to contain fluorine (Supplementary Data & Supplementary Table 2), so a more likely origin of this peak is a carbonyl group bound to N and/or O, with adjacent carbonyl groups inducing a secondary chemical shift. The structure in Figure 5C could satisfy this condition, although no exact example of an XPS spectrum of this structure was found in the literature [87,88].



1µm

50nm

a b

1µm

50nm

1µm

50nm

1µm1µm1µm

50nm50nm50nm

a bA B

(i)

keV1 2 3 4 50

100

200

300

400

500

600

700

800

900

1000

Co

un

ts

0

FeK

esc

CaK

b

CaK

aK

Kb

KK

a

ClK

bC

lKa

SK

bS

Ka

PK

a

SiK

a

AlK

a

MgK

a

CuL

aC

uLl

FeL

aF

eLl

OK

a

1 µm

50 nm

CK

a

Figure 8. Transmission electron microscopy images of a wheatstraw biochar particle. (A) Bright field transmission electron microscopy (Joel JEM -1200, Tokyo, Japan) with energy dispersive x-ray spectroscopy spectra (Oxford ISIS, Oxford, UK) image of a wheatstraw biochar particle. Inset image is a higher resolution image of the nanophase structure of the particle from area A. (B) An energy dispersive x-ray spectroscopy spectra from area (i) indicating that the mineral phases in the carbon lattice contain K, Mg, Si and S.

Solid state (13C, 31P and 15N) nuclear magnetic reso-nance (NMR) experiments were carried out on Bruker AVANCE III 300 MHz spectrometer operating at a field of 7 Tesla with a 4 mm double resonance wide-bore magic angle spinning probehead. Details of the experiments can be found in the Supplementary Data. The directly polarized, quantitative 13C NMR of the WSB showed a high degree of aromatic condensation (Figure 6 and Supplementary Data). In the case of the biochar–fertilizer composite (WSF), the situation was altered significantly. The bulk conductivity of the mate-rial was reduced so that cross-polarization from 1H was possible, as can be seen in Figure 6D. Although the pri-mary aromatic peak for the treated biochar is identical

to that of the untreated biochar, an additional sharp peak at approximately 163 in the cross polarization with magic angle spinning spectrum is observed. This peak can be attributed to the presence of urea. The directly polarized 13C NMR spectrum of the fertilizer treated biochar (Figure 6E) shows an additional sharp peak at approximately 158 ppm. Although the nature of this additional peak is not clear, at this point we hypothesize that it may be due to urea molecules with high mobility due to the presence of residual water in the char.

In order to further detect the state of the fertilizers co-added to the biochar, 15N and 31P NMR spectra of the fertilizer-treated biochar were measured and com-pared with the neat as received fertilizer as shown in



A B

CKCOClCaSiS

Mg

100

80

60

40

20

0

Distance (µm) 6420

300 nm 1 µm

Co

un

ts

Figure 9. Transmission electron microscopy images of a wheatstraw biochar particle. (A) Bright field transmission electron microscopy image of a section of a wheatstraw biochar particle. (B) Scanning transmission electron microscope image together with an energy dispersive x-ray spectroscopy elemental line scan (Phillips CM 200 transmission electron microscopy with Bruker energy dispersive x-ray spectroscopy detector). (C) Concentration profile along the region marked with an arrow in (B).

Supplementary Figure 2. In the case of the 15N NMR, the ammonium dihydrogen phosphate yields a sharp sig-nal (Supplementary Figure 2B) as expected of a crystalline ammonium salt. In comparison, the 15N NMR signals from the biochar–fertilizer composite, WSF, are both broadened and have a significantly reduced intensity. This change can be explained by the lower concentra-tion of the N fertilizers in the WSF and due to a change in the physical characteristics of these fertilizers. In par-ticular, the amine peak of the diammonium phosphate in WSF has shifted downfield to 5 ppm in addition to being significantly broadened. Part of this broadening could be due to the very small amount of Fe in the sample.

Additionally, there are two peaks visible at approximately 60 ppm, which are assigned to urea in different environ-ments. The 31P NMR shows similar changes as can be seen in Supplementary Figures 2C & 2D. The 31P NMR sig-nals of the fertilizer in the biochar are reduced in intensity and significantly broadened as compared with the neat ammonium dihydrogen phosphate. In all cases, these broadenings and shifts would be consistent with an inti-mate interaction between the biochar and the fertilizers, which prevents the recrystallization of the fertilizer spe-cies into well-ordered phases. It is important to note that is would be unlikely to detect 15N and 13C NMR signals from urea had the urea recrystallized into its native state.



AA(i)

A

B

C

Ca

K

Cl

S

P

Si

Al

Mg

NaF

N

Ca

S

K

O

C

keV1 2 3 4

Co

un

ts

2

4

6

8

10

12

0

Figure 10. Scanning electron microscopy images of a wheat straw biochar–fertilizer composite particle. (A) Area (i) shows that a range of mineral phases have entered the pores of the wheat straw biochar–fertilizer composite. (B) An energy dispersive x-ray spectroscopy spectrum of the entire area indicating that minerals rich in N, P and K are present. (C) Shows there has been considerable reactions occurring in the composite that produced complex morphologies.

This is because the spin lattice relaxation for both 13C and 15N species in crystalline urea are of the order of several hours, while even that of the 1H species is over 1 h long. As a result, under the conditions of our measurement, it is highly unlikely to observe signals of urea in its native crystalline habit. However, the presence of both the 15N and 13C signals of urea in WSF is an indication that it does not form its usual crystalline phase. One of the pos-sible interactions in this case could be hydrogen bonding between the amide groups of the urea and the aromatic CO groups of the biochar in the WSF composite. These results are consistent with those of the XPS and FTIR ana lysis.

A secondary electron image of the coarse structure of an original biochar WSB particle is shown in Figures 7A & 7B, where it is seen that the particle retains its cellulosic struc-ture and the surface contains elongated pores. A series

of energy dispersive x-ray spectroscopy (EDS) elemental x-ray maps indicate there are areas rich in clay and silica on the particle surface, along with minerals that are rich in K and Cl. Figure 7B reveals phases on the WSB carbon surface, some of which are submicron in scale and contain P, Mg and S.

The ana lysis of WSB particles using TEM shows heterogeneity at both the micrometer and nanometer scale (Figures 8 & 9). Both micrographs show that the WSB particle consists of many different phases and that the pore structure is diverse with long cylindri-cal macropores and mesopores, as well as many min-eral interfaces. The EDS line scan ana lysis (Figure 9C) indicates that within a predominately KCl phase there exist other phases that are high in C, Ca, Si and S. The phases next to this have high concentrations of K and Ca indicating that there could be calcium and



C

BA

400 nm

200 nm

100 nm

Figure 11. Transmission electron microscopy bright field images of a wheat straw biochar–fertilizer composite particle. (A) The interface between a mineral-rich phase and an amorphous carbon phase, (B) an image of the porous interface between the two phases and (C) crystalline particles within a carbon matrix.

potassium carbonate. Some of the calcium in high-ash biomass chars also may be bound to oxygen as ionic metal phenoxides, which are quite thermally stable (more so than phenol itself ) [89]. K may also be present as ionic metal phenoxides or as intercalated K. Based on their study of pyrolysis and combustion of pine and switchgrass, Wornat et al. postulated that Mg and Ca in biochars could occur as ion-exchanged metals asso-ciated with oxygen-containing functional groups [89]. The other possibility is that complex silica structures (such as feldspathoids) are formed during pyrolysis of Si-rich biomass. It is also probable that part of the silica comes from soil that is covering the biomass before it is pyrolysed.

The micro-structure of the biochar-fertilizer complex, WSF, was substantially different from that of the parent WSB. The secondary electron image (Figure 10A) indi-cates that a range of minerals have entered the pores of the WSB. Figure 10B is an EDS of the whole area indi-cating that minerals high in N, P and K are present at the micron level. Figure 10C indicates that there has been considerable reaction between the WSB and the clay and the other chemicals to produce some unusual structures.

Higher resolution examination of the structure of the WSF using TEM reveals there has been a change in the composition and structure of the phases from those in the original WSB. Figure 11 is a representative area of one particle. It can been seen that there is a large



KP

Si

AlNa

O

C

CaK

PSi

AlMgNa

F

O

CaK

P

SiAl

MgF

O

Inte

nsi

ty

C

keV1 2 3 4

Inte

nsi

ty

keV1 2 3 4 5

Inte

nsi

ty

5

C

keV1 2 3 4 5

200 nm

Figure 12. Transmission electron microscopy bright field images of a wheat straw biochar–fertilizer composite particle with energy-dispersive x-ray spectroscopy spectra from a range of different mineral phases adjacent to an amorphous carbon phase. The location from where each spectra was recorded is indicated by arrows. A carbon-based phase that exhibits a crystalline structure, marked X, is visible.

concentration of pores with diameters less than 20 nm at the interface between a mineral phase rich in P and K and a carbon-rich phase. Figure 12 shows the diversity of compositions within the area of high mineral content. Further work is required to unambiguously identify this phase.

It is apparent that in WSF the clay and chemicals have reacted with the biochar matrix and that there has also been a migration of soluble cations and anions into the biochar pores. We suggest that these changes resulted in different rates of nutrient availability and, hence, nutrient uptake by the plant.

Future perspectiveBased on all that has been presented above, we offer the following perspectives for developing low-dose, high-efficiency biochar–fertilizer products. An optimal enhanced biochar is envisioned to have an inner core of porous carbon (biochar) that is resistant to mineraliza-tion, with nanosized mineral phases rich in macro- and micro-nutrients coating the pores and external surfaces of the carbon. Such biochar complexes can be developed in a number of different ways, for example:

� A clay and mineral and/or chemical mixture is applied to biochar when it comes from the pyrolysis unit. Organic molecules from wood smoke, the reaction of biochar with KOH [20,27] or other sources (e.g., humics from lignite or peat [90]) that have proven to enhance germination rates, disease resistance or nutrient uptake are added. The mixture is formed using a binder into a uniform product for use in standard fertilizer applicators. This would build on advances of the WSF described in this paper;

� Nanophase organic compounds and/or minerals are chemically bound to a biochar, which has been previously activated either by an acid or a base [27,78];

� A biochar is produced from biomass that has been soaked in a nutrient- and clay-rich solution. The biomass is dried and then pyrolyzed. The firing temperature is regulated to control the release rate of these minerals and labile organic component of the particle. This approach follows the work of Joseph et al. in characterizing biochars that were produced by Vietnamese farmers [91];

� A biochar is produced from biomass that was reacted with phosphoric acid and then mixed with nutrients and clay, and fired to a temperature that maximizes the functionality and surface area of both the carbon and the mineral matrix. This biochar is added to composting organic matter and then pelletized after the composting process is completed;

� A biologically active biochar product may be produced by composting or fermenting biochar together with manures/urine and ashes [92]. The product can also be inoculated with beneficial microorganisms.

Such biochar-based fertilizers will be purpose-devel-oped, taking into consideration soil type and fertility sta-tus, crop, climate, available biochar feedstock and more. The biochar-based fertilizers will be applied at low doses on a conventional schedule of fertilizer application with the same farm instruments that exist today for this pur-pose. Over time, the accumulated biochar will sequester ever-increasing amounts of carbon, ensuring the carbon negative vision of the pyrolysis/biochar scheme.

The current governing concept of biochar use involv-ing large, one-time doses of ‘one size fits all’ biochar to soils around the world to improve fertility and seques-ter carbon is not tenable under current constraints in many areas of either developed or developing coun-tries [93]. Thus, we foresee that the small niche market occupied today by biochar will continue well into the future, unless significant advances are made in develop-ing high-potency, low-rate, biochar-based fertilizers that can perform better than NPK fertilizers at lower costs, and additionally have added value in the form of carbon credits. At present, China is the only country where com-mercial production of these combined fertilizers is taking place, currently at a scale in excess of 40,000 tonnes per year. Utilizing advances in the development of activated carbons, nano-scale carbon-based composite materials and biomolecular engineering could transform biochar from a niche product produced by a small number of high-input enterprises to a mainstream business relevant to extensive agriculture.

Supplementary dataTo view the supplementary data that accompany this paper please visit the journal website at: www.future-science.com/doi/full/10.4155/CMT.13.23

AcknowledgementsWe gratefully acknowledge the efforts of the Comissioning Editor of Carbon Management (R Williamson) and the reviewers, and express our appreciation for their input which helped us to substantially improve this work. S Joseph would like to acknowledge the assistance given by the electron microscope unit of the University of Newcastle (Callaghan, Australia), and to thank B Gong for his assistance in carrying out the x-ray photoelectron spectroscopy analyses of the samples.

Financial & competing interests disclosureG Pan holds two patents related to the production of an enhanced biochar for the removal of heavy metals and has applied for a patent for a biochar NPK fertilizer. S Joseph holds a patent on an enhanced biochar. ER Graber would like to acknowledge financial support from



the Bi-National Israel–Italy Cooperation (grant: Improving Agricultural Productivity Through Sustainable Soil Management). The authors have no other relevant affiliations or financial involvement with any organization or entity with a financial interest in or financial

conflict with the subject matter or materials discussed in the manuscript apart from those disclosed.

No writing assistance was utilized in the production of this manuscript.

Executive summary

� Surfaces of biochar can be functionalized by micro- and nano-phase mineral matter during pyrolysis or after pyrolysis. � The presence of minerals during biomass pyrolysis increases the content of labile organic compounds in biochar. � Nanophase minerals, functional groups at carbon surfaces and labile organic compounds are fundamental for biochar efficacy. � High-mineral content biochars catalyze biotic and abiotic reactions in soil, behaving as microgalvanic cells where organic and inorganic

compounds are oxidized and reduced. � Labile organic compounds released from biochar reduce and chelate important plant micronutrients. � Specialized microbial communities colonize specific biochar phases, resulting in highly spatially variable communities and community

dynamics. � Suggestions for developing low-dose, high-potency biochar–mineral blends are given.

ReferencesPapers of special note have been highlighted as:n of interestnn of considerable interest

1 Kimetu JM, Lehmann J, Ngoze SO et al. Reversibility of soil productivity decline with organic matter of differing quality along a degradation gradient. Ecosystems 11(5), 726–739 (2008).

2 Vaccari FP, Baronti S, Lugato E et al. Biochar as a strategy to sequester carbon and increase yield in durum wheat. Eur. J. Agron. 34(4), 231–238 (2011).

3 Yamato M, Okimori Y, Wibowo IF, Anshori S, Ogawa M. Effects of the application of charred bark of Acacia mangium on the yield of maize, cowpea and peanut, and soil chemical properties in South Sumatra, Indonesia. Soil Sci. Plant Nutr. 52(4), 489–495 (2006).

4 Elad Y, Cytryn E, Harel YM, Lew B, Graber ER. The biochar effect: plant resistance to biotic stresses. Phytopathol. Mediterr. 50(3), 335–349 (2011).

nn Reviews the role of biochar and its labile organic compounds in promoting plant resistance to pathogen attack.

5 Elad Y, Rav-David D, Harel YM et al. Induction of systemic resistance in plants by biochar, a soil-applied carbon sequestering agent. Phytopathology 100(9), 913–921 (2010).

6 Graber ER, Elad Y. Biochar impact on plant resistance to disease. In: Biochar and Soil Biota. Ladygina N, Rineau F (Eds). CRC Press, Boca Raton, FL, USA (2013).

7 Harel YM, Elad Y, Rav-David D et al. Biochar mediates systemic response of strawberry to foliar fungal pathogens. Plant Soil 357, 245–257 (2012).

8 Chen YX, Huang XD, Han ZY et al. Effects of bamboo charcoal and bamboo vinegar on

nitrogen conservation and heavy metals immobility during pig manure composting. Chemosphere 78(9), 1177–1181 (2010).

9 Uchimiya M, Lima IM, Klasson KT, Chang SC, Wartelle LH, Rodgers JE. Immobilization of heavy metal ions (Cu-II, Cd-II, Ni-II, and Pb-II) by broiler litter-derived biochars in water and soil. J. Agric. Food Chem. 58(9), 5538–5544 (2010).

10 Cheng CH, Lehmann J, Thies JE, Burton SD. Stability of black carbon in soils across a climatic gradient. J. Geophys. Res. Biogeosci. 113, G02027 (2008).

11 Kuzyakov Y, Subbotina I, Chen HQ, Bogomolova I, Xu XL. Black carbon decomposition and incorporation into soil microbial biomass estimated by C-14 labeling. Soil Biol. Biochem. 41(2), 210–219 (2009).

12 Zimmerman AR. Abiotic and microbial oxidation of laboratory-produced black carbon (biochar). Environ. Sci. Technol. 44(4), 1295–1301 (2010).

13 Jeffery S, Verheijen FGA, van der Velde M, Bastos AC. A quantitative review of the effects of biochar application to soils on crop productivity using meta-analysis. Agric. Ecosyst. Environ. 144(1), 175–187 (2011).

14 Joseph S. Socioeconomic assessment and implementation of small scale biochar projects. In: Biochar for Environmental Management: Science and Technology. Lehmann J, Joseph S (Eds). Earthscan Publications, London, UK, 359–371 (2009).

15 Torres-Rojas D, Lehmann J, Hobbs P, Joseph S, Neufeldt H. Biomass availability, energy consumption and biochar production in rural households of western Kenya. Biomass Bioenergy 35(8), 3537 (2011).

16 Blackwell P, Krull E, Butler G, Herbert A, Solaiman ZM. Effect of banded biochar on

dryland wheat production and fertiliser use in south-western Australia: an agronomic and economic perspective. Soil Res. 48(7), 531–545 (2010).

17 Dias BO, Silva CA, Higashikawa FS, Roig A, Sanchez-Monedero MA. Use of biochar as bulking agent for the composting of poultry manure: effect on organic matter degradation and humification. Bioresour. Technol. 101(4), 1239–1246 (2010).

18 Steiner C, Das KC, Melear N, Lakly D. Reducing nitrogen loss during poultry litter composting using biochar. J. Environ. Qual. 39(4), 1236–1242 (2010).

19 Hua L, Wu WX, Liu YX, McBride M, Chen YX. Reduction of nitrogen loss and Cu and Zn mobility during sludge composting with bamboo charcoal amendment. Environ. Sci. Pollut. Res. 16(1), 1–9 (2009).

20 Lin Y, Munroe P, Joseph S et al. Chemical and structural analysis of enhanced biochars: thermally treated mixtures of biochar, chicken litter, clay and minerals. Chemosphere 91(1), 35–40 (2013).

21 Day D, Evans RJ, Lee JW, Reicosky D. Valuable and stable co-product from fossil fuel exhaust scrubbing. In: American Chemical Society, Division of Fuel Chemistry. American Chemical Society, Washington, DC, USA, 352–355 (2004).

22 Amonette JE, Joseph S. Characteristics of biochar: microchemical properties. In: Biochar for Environmental Management: Science and Technology. Lehmann J, Joseph S (Eds). Earthscan, London, UK, 33–52 (2009).

23 Demirbas A. Carbonization ranking of selected biomass for charcoal, liquid and gaseous products. Energy Convers. Manag. 42(10), 1229–1238 (2001).



n Provides a wealth of data on the yields of different products from the pyrolysis of biomass.

24 Novak JM, Lima IM, Xing B et al. Characterization of designer biochar produced at different temperatures and their effects on a loamy sand. Ann. Environ. Sci. 3, 195–206 (2009).

25 Gaskin JW, Steiner C, Harris K, Das KC, Bibens B. Effect of low-temperature pyrolysis conditions on biochar for agricultural use. Trans. ASABE 51(6), 2061–2069 (2008).

26 Kloss S, Zehetner F, Dellantonio A et al. Characterization of slow pyrolysis biochars: effects of feedstocks and pyrolysis temperature on biochar properties. J. Environ. Qual. 41(4), 990–1000 (2012).

27 Lin Y, Munroe P, Joseph S, Kimber S, Van Zwieten L. Nanoscale organo-mineral reactions of biochars in ferrosol: an investigation using microscopy. Plant Soil 357(1–2), 369–380 (2012).

28 Solomon D, Lehmann J, Wang J et al. Micro- and nano-environments of C sequestration in soil: a multi-elemental STXM-NEXAFS assessment of black C and organomineral associations. Sci. Total Environ. 438, 372–388 (2012).

29 Yang HP, Yan R, Chen HP, Lee DH, Zheng CG. Characteristics of hemicellulose, cellulose and lignin pyrolysis. Fuel 86(12–13), 1781–1788 (2007).

30 Gray MR, Corcoran WH, Gavalas GR. Pyrolysis of a wood-derived material – effects of moisture and ash content. Ind. Eng. Chem. Proc. Des. Dev. 24(3), 646–651 (1985).

31 Giuntoli J, Arvelakis S, Spliethoff H, de Jong W, Verkooijen AHM. Quantitative and kinetic thermogravimetric fourier transform infrared (TG–FTIR) study of pyrolysis of agricultural residues: influence of different pretreatments. Energy Fuels 23, 5695–5706 (2009).

32 Xu MZ, Sheng CD. Influences of the heat-treatment temperature and inorganic matter on combustion characteristics of cornstalk biochars. Energy Fuels 26(1), 209–218 (2012).

33 Keiluweit M, Nico PS, Johnson MG, Kleber M. Dynamic molecular structure of plant biomass-derived black carbon (biochar). Environ. Sci. Technol. 44(4), 1247–1253 (2010).

34 Harvey OR, Herbert BE, Kuo LJ, Louchouarn P. Generalized two-dimensional perturbation correlation infrared spectroscopy reveals mechanisms for the development of surface charge and

recalcitrance in plant-derived biochars. Environ. Sci. Technol. 46(19), 10641–10650 (2012).

35 Heller-Kallai L. The nature of clay volatiles and condensates and the effect on their environment. J. Therm. Anal. 50(1–2), 145–156 (1997).

n Highlights the role of clay volatiles in assisting both with the thermal decomposition of the biomass and the functionalizing of biochar surfaces through the release of strong acids such as hydrofluoric acid.

36 Chen BL, Chen ZM, Lv S. A novel magnetic biochar efficiently sorbs organic pollutants and phosphate. Bioresour. Technol. 102(2), 716–723 (2011).

37 Hamilton SM. Electrochemical mass-transport in overburden: a new model to account for the formation of selective leach geochemical anomalies in glacial terrain. J. Geochem. Explor. 63(3), 155–172 (1998).

n Details the effect of graphitic deposits on movement of cations and anions in soils. It shows that electronic conductors such as graphite in bedrock can provide a ‘short-circuit’ route across the redox field between reducing agents abundant at depth and oxidizing agents abundant in shallower areas.

38 Joseph SD, Donne S, Camps-Arbestain M et al. Does biochar and BMC lower the energy required for plants to take up nutrients by changing the redox potential and the concentration gradients of nutrients in the rhizosphere. Presented at: 3rd International Biochar Initiative Conference. Rio de Janeiro, Brazil, 12–15 September 2010.

39 Petter FA, Madari BE. Biochar: agronomic and environmental potential in Brazilian savannah soils. Rev. Bras. Eng. Agríc. Ambient. 16(7) (2012).

40 Wulff J. The Structure and Properties of Materials. Wiley, Hoboken, NJ, USA (1964).

41 Meyer M, Campaignolle X, Coeuille F, Shanahan MER. Processes on anticorrosion properties of thick polymer coatings for steel pipelines. In: Corrosion 2004, Research Topical Symposium: Corrosion Modeling for Assessing the Condition of Oil and Gas Pipelines. King F, Beavers J (Eds). NACE, Houston, TX, USA, 93–146 (2004).

42 Graber ER, Meller-Harel Y, Kolton M et al. Biochar impact on development and productivity of pepper and tomato grown in fertigated soilless media. Plant Soil 337, 481–496 (2010).

43 Kolton M, Harel YM, Pasternak Z, Graber ER, Elad Y, Cytryn E. Impact of biochar application to soil on the root-associated bacterial community structure of fully developed greenhouse pepper plants. Appl. Environ. Microbiol. 77, 4924–4930 (2011).

44 Singh BP, Hatton BJ, Singh B, Cowie AL, Kathuria A. Influence of biochars on nitrous oxide emission and nitrogen leaching from two contrasting soils. J. Environ. Qual. 39(4), 1224–1235 (2010).

45 Spokas KA, Koskinen WC, Baker JM, Reicosky DC. Impacts of woodchip biochar additions on greenhouse gas production and sorption/degradation of two herbicides in a Minnesota soil. Chemosphere 77(4), 574–581 (2009).

46 Taghizadeh-Toosi A, Clough TJ, Condron LM, Sherlock RR, Anderson CR, Craigie RA. Biochar incorporation into pasture soil suppresses in situ nitrous oxide emissions from ruminant urine patches. J. Environ. Qual. 40(2), 468–476 (2011).

47 Yanai Y, Toyota K, Okazaki M. Effects of charcoal addition on N

2O emissions from soil

resulting from rewetting air-dried soil in short-term laboratory experiments. Soil Sci. Plant Nutr. 53(2), 181–188 (2007).

48 Light ME, Burger BV, Van Staden J. Formation of a seed germination promoter from carbohydrates and amino acids. J. Agric. Food Chem. 53(15), 5936–5942 (2005).

49 Lin Y, Munroe P, Joseph S, Henderson R, Ziolkowski A. Water extractable organic carbon in untreated and chemical treated biochars. Chemosphere 87(2), 151–157 (2011).

50 Graber ER, Tsechansky L, Lew B, Cohen E. Reducing capacity of water extracts of biochars and their solubilization of soil Mn and Fe. Eur. J. Soil Sci. (2013) (Accepted).

nn Analyzes the redox potential of the water-soluble component of labile organic molecules on both high- and low-temperature biochars. Low highest treatment temperature biochars were found to be more redox active than extracts of high highest treatment temperature biochars. Phenolic compounds were responsible for the main part of the reducing capacity.

51 Lovley DR, Fraga JL, Blunt-Harris EL, Hayes LA, Phillips EJP, Coates JD. Humic substances as a mediator for microbially catalyzed metal reduction. Acta Hydrochim. Hydrobiol. 26(3), 152–157 (1998).

52 Abiven S, Hengartner P, Schneider MPW, Singh N, Schmidt MWI. Pyrogenic carbon soluble fraction is larger and more aromatic in



aged charcoal than in fresh charcoal. Soil Biol. Biochem. 43(7), 1615–1617 (2011).

53 Hockaday WC, Grannas AM, Kim S, Hatcher PG. The transformation and mobility of charcoal in a fire-impacted watershed. Geochim. Cosmochim. Acta 71, 3432–3445 (2007).

54 Silber A, Levkovitch I, Graber ER. pH-dependent mineral release and surface properties of cornstraw biochar: agronomic implications. Environ. Sci. Technol. 44, 9318–9323 (2010).

55 Chen Y, Clapp CE, Magen H. Mechanisms of plant growth stimulation by humic substances: the role of organo–iron complexes. Soil Sci. Plant Nutr. 50(7), 1089–1095 (2004).

56 Pohlman AA, McColl JG. Kinetics of metal dissolution from forest soils by soluble organic acids. J. Environ. Qual. 15(1), 86–92 (1986).

57 Pohlman AA, McColl JG. Organic oxidation and manganese and aluminum mobilization in forest soils. Soil Sci. Soc. Am. J. 53(3), 686–690 (1989).

58 Bonneville S, Morgan DJ, Schmalenberger A et al. Tree-mycorrhiza symbiosis accelerate mineral weathering: evidences from nanometer-scale elemental f luxes at the hypha-mineral interface. Geochim. Cosmochim. Acta 75(22), 6988–7005 (2011).

59 Gadd GM. Metals, minerals and microbes: geomicrobiology and bioremediation. Microbiology 156(3), 609–643 (2010).

60 Ehrlich HL, Newman DK. Geomicrobiology (5th Edition). CRC Press/Taylor and Francis, Boca Raton, FL, USA (2009).

61 Gilbert B, Banfield JF. Molecular-scale processes involving nanoparticulate minerals in biogeochemical systems. In: Molecular Geomicrobiology. Banfield JE, CerviniSilva J, Nealson KH (Eds). Mineralogical Society of America, Chantilly, VA, USA, 109–155 (2005).

62 Luttge A, Conrad PG. Direct observation of microbial inhibition of calcite dissolution. Appl. Environ. Microbiol. 70(3), 1627–1632 (2004).

63 Zhang GX, Dong HL, Jiang HC et al. Biomineralization associated with microbial reduction of Fe3+ and oxidation of Fe2+ in solid minerals. Am. Mineral. 94(7), 1049–1058 (2009).

64 Ishihara S. Recent trend of advanced carbon materials from wood charcoals. Mokuzai Gakkaishi 42(8), 717–723 (1996).

65 Waksman SA, Joffe JS. Microorganisms concerned in the oxidation of sulfur in the soil ii. Thiobacillus thiooxidans, a new sulfur-

oxidizing organism isolated from the soil. J. Bacteriol. 7(2), 239–256 (1922).

66 Hockaday WC, Grannas AM, Kim S, Hatcher PG. Direct molecular evidence for the degradation and mobility of black carbon in soils from ultrahigh-resolution mass spectral analysis of dissolved organic matter from a fire-impacted forest soil. Org. Geochem. 37(4), 501–510 (2006).

67 Major J, Rondon M, Molina D, Riha SJ, Lehmann J. Maize yield and nutrition during 4 years after biochar application to a Colombian savanna oxisol. Plant Soil 333(1–2), 117–128 (2010).

68 Joseph SD, Camps-Arbestain M, Lin Y et al. An investigation into the reactions of biochar in soil. Austral. J. Soil Res. 48(6–7), 501–515 (2010).

nn Details the very complex set of interactions and reactions that occur between biochar and soil solids, dissolved organic matter, minerals and microorganisms.

69 Chia CH, Munroe P, Joseph S, Lin Y. Microscopic characterisation of synthetic Terra Preta. Austral. J. Soil Res. 48(6–7), 593–605 (2010).

n Demonstrates that minerals and clay react with biomass when heated to low temperature to form organo–mineral complexes with characteristics that differ from those of a pyrolyzed biomass.

70 Anderson CR, Condron LM, Clough TJ et al. Biochar induced soil microbial community change: implications for biogeochemical cycling of carbon, nitrogen and phosphorus. Pedobiologia 54(5–6), 309–320 (2011).

71 Lehmann J, Rillig MC, Thies J, Masiello CA, Hockaday WC, Crowley D. Biochar effects on soil biota – a review. Soil Biol. Biochem. 43(9), 1812–1836 (2011).

nn Comprehensive review of the effects that biochar can have in terms of enhancing microbial growth in soils.

72 Joseph S, Van Zwieten L, Kimber S et al. Developing biochars that can be applied at low application rates; field results. Presented at: Asia Pacific Biochar Conference Kyoto. Kyoto, Japan, 15–18 September 2011.

73 Lovley DR. Electromicrobiology. Annu. Rev. Microbiol. 66, 391–409 (2012).

74 Safarik I, Horska K, Pospiskova K, Safarikova M. Magnetically responsive activated carbons for bio – and environmental applications. Int. Rev. Chem. Eng. 4(3), 346–352 (2012).

75 Kovacs PE, Valentine RL, Alvarez PJJ. The effect of static magnetic fields on biological

systems: implications for enhanced biodegradation. Crit. Rev. Environ. Sci. Technol. 27(4), 319–382 (1997).

76 Fassbinder JW, Stanjek H, Vali H. Occurrence of magnetic bacteria in soil. Nature 343(6254), 161–163 (1990).

77 Bazylinski DA, Blakemore R. Denitrification and assimilatory nitrate reduction in Aquaspirillum magnetotacticum. Appl. Environ. Microbiol. 46(5), 1118–1124 (1983).

78 Jibril B, Houache O, Al-Maamari R, Al-Rashidi B. Effects of H

3PO

4 and KOH in

carbonization of lignocellulosic material. J. Anal. Appl. Pyrolysis 83, 151–156 (2008).

79 Gu Z, Wang X. Carbon materials from high ash bio-char: a nanostructure similar to activated graphene. Am. Trans. Eng. Appl. Sci. 2(1), 15–34 (2013).

80 Shen W, Li Z, Liu Y. Surface chemical functional groups modification of porous carbon. Recent Pat. Chem. Eng. 1, 27–40 (2008).

81 Zhang AF, Bian R, Pang G et al. Effects of biochar amendment on soil quality, crop yield and greenhouse gas emission in a Chinese rice paddy: a field study of 2 consecutive rice growing cycles. Field Crops Res. 127, 153–160 (2012).

82 Zhang AF, Cui L, Pang G et al. Effect of biochar amendment on yield and methane and nitrous oxide emissions from a rice paddy from Tai Lake plain, China. Agric. Ecosys. Environ. 139, 469–475 (2010).

83 Zhang AF, Liu YM, Pan GX et al. 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(1–2), 263–275 (2012).

84 Pan GX, Zhang AF, Zou JW. Biochar from agro-byproducts used as amendment to croplands: an option for low carbon agriculture. J. Ecol. Rural Environ. 26(4), 394–400 (2010).

85 Zhang AF, Zheng YM, Liu JL, Pan GX. An approach to the measurement for carbon sequestration and mitigation of straw biochar amendment. J. Agro-Environ. Sci. 30(9), 1811 (2011).

86 Rao CNR. Chemical Applications of Infrared Spectroscopy. Academic Press, New York, NY, USA (1963).

87 Beamson G, Briggs D. High Resolution XPS of Organic Polymers. Wiley, New York, NY, USA (1992).

88 Moulder JF, Stickle WF, Sobol PE, Bomben KD. Handbook of X-Ray Photoelectron



Spectroscopy. PerkinElmer Corporation, Waltham, MA, USA (1992).

89 Wornat MJ, Hurt RH, Yang NYC, Headley TJ. Structural and compositional transformations of biomass chars during combustion. Combust. Flame 100(1–2), 133–145 (1995).

90 Wu W, Yang M, Liu Y, Dong D, Feng Q, Zhou M. Application of biochar in rice productivity and nitrogen run-off control. Presented at: International Workshop on Production and Application of Biochar in China’s Agriculture. Nanjing, China, 20–23 September 2011.

91 Joseph S, van Zwieten L, Chia CH et al. ‘Designing’ of biochar for specific

applications to soils; a technology in its infancy. In: Biochar and Soil Biota. Ladygina N, Rineau F (Eds). CRC Press, Boca Raton, FL, USA (2013).

92 Fischer D, Glaser B. Synergisms between compost and biochar for sustainable soil amelioration. In: Management of Organic Waste. Kumar S, Bharti A (Eds). InTech, Rijeka, Croatia, 167–198 (2012).

n Highlights the increases in crop yields that can be acheived by adding small quantities of both biochar, minerals and urine to biomass to produce compost.

93 Woolf D, Amonette JE, Street-Perrott FA, Lehmann J, Joseph S. Sustainable biochar to

mitigate global climate change. Nat. Commun. 1(5), 56 (2010).

n Provides the potential for biochar to sequester carbon from a range of biomass feedstocks from different regions in the world.

� Website101 Thermo Fisher Scientific. A guide to raw

material analysis using Fourier transform near-infrared spectroscopy. www.thermo.com.cn/Resources/201211/141413246.pdf



www.thermo.com.cn/Resources/201211/141413246.pdf

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Shifting paradigms: development of high-efficiency biochar fertilizers based on nano-structures and soluble components

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