See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/302558326 Biochar effects on soil nutrient transformations Chapter · January 2015 CITATIONS READS 85 2,516 4 authors, including: Thomas H Deluca M Derek Mackenzie University of Montana University of Alberta 159 PUBLICATIONS 7,815 CITATIONS 44 PUBLICATIONS 1,830 CITATIONS SEE PROFILE SEE PROFILE Davey L Jones University of Western Australia 582 PUBLICATIONS 26,765 CITATIONS SEE PROFILE Some of the authors of this publication are also working on these related projects: 'CINAg': UK-China Virtual Joint Centre for Improved Nitrogen Agronomy View project Soil and Foliar Chemistry Analysis for WBEA’s Terrestrial Environmental Effects Monitoring View project All content following this page was uploaded by M Derek Mackenzie on 06 December 2016. The user has requested enhancement of the downloaded file. 15 Biochar effects on soil nutrient transformations Thomas H. DeLuca, Michael J. Gundale, M. Derek MacKenzie and Davey L. Jones Introduction A key aspect of biochar management is its proposed effect on soil fertility and plant production (Lehmann, 2007). Plant productivity is directly influenced by nutrient availability, which is a product of nutrient transformations in the soil environment (Marschner, 2006). For that reason, there is a great deal of interest in how biochar influences nutrient transformations and availability of those nutrients for plant uptake. And although increasing evidence suggests that biochar addition to soil may enhance plant production in a variety of natural and agricultural environments (Lehmann and Rondon, 2006; Atkinson et al, 2010; Jeffery et al, 2011), the direct influence of biochar additions on soil nutrient cycling are inconsistent and remain somewhat poorly understood. This is partially due to differences in the soils, crops and biochar amendments used in experiments and the predominance of short-term studies in the literature. The purpose of this chapter is to summarize several general mechanisms through Biochar C15.indd 419 which biochar affects nutrient availability to plants and to specifically evaluate the effect biochar has on nutrient cycling and specific transformations within several key nutrient cycles. Our aim is to complement other chapters in this book as well as other reviews that have focused on the chemical and physical properties of biochar (Chapters 5 and 6) (Atkinson et al, 2010; Shrestha et al, 2010), its stability in the soil (Shrestha et al, 2010), its effect on soil biota and plant eco-physiology (Chapters 13 and 14) (Atkinson et al, 2010; Lehmann et al, 2011), its influence on soil properties (Atkinson et al, 2010; Beesley et al, 2011), its impact on trace gas fluxes (Chapter 18) (Jones et al, 2011) and its use in biofuel technology or soil C sequestration (Chapter 10) (Lehmann, 2007; Lee et al, 2010; Macias and Arbestain, 2010). The purpose of this review is to explore what is and is not known about the effect of biochar on soil nutrient transformations, which are likely to have both short- and long-term impacts on plant productivity in forest and 11/3/2014 9:04:29 AM 420 BIOCHAR FOR ENVIRONMENTAL MANAGEMENT agricultural landscapes (Atkinson et al, 2010). We specifically focus on the response of nitrogen (N), phosphorus (P) and sulfur (S) cycles in response to biochar amendment and explore the implications for altered transformations within these cycles on the availability of nutrients to plants and their long term budgets across a range of ecosystems. In this effort we will try to differentiate between short-term and long-term effects of biochar on ecosystem processes. General mechanisms by which biochar influences nutrient turnover and transformations The application of biochar to agricultural and forest soils has been found to increase the bio-availability and uptake of many nutrients to plants (Glaser et al, 2002; Lehmann et al, 2003; Steiner et al, 2007; Jeffery et al, 2011; Nelson et al, 2011). While some mechanisms causing increased nutrient availability have been extensively described and summarized (Atkinson et al, 2010), very little research has been conducted on the influence of biochar on specific nutrient cycling mechanisms. For instance, numerous studies have described high concentrations of available nutrients on the surface of newly created biochar made over a wide range of temperatures and oxidation conditions, and from a range of feedstocks, suggesting that biochars themselves can have fertilization effects over short timescales (Chan and Xu, 2009; Jeffery et al, 2011). As an example, the direct contribution of NH4+ salts from newly formed biochar has been described in numerous studies (see Chapter 7; Gundale and DeLuca, 2006; Chan and Xu, 2009; Spokas et al, 2012). Considerably less attention has been given to the effect of biochar on specific transformations, i.e. indirect alterations, within the N cycle (Lehmann, 2007; Clough and Condron, 2010; Clough et al, 2013), for example biological N-fixation, N-mineralization, nitrification and gaseous N losses (Clough and Condron, 2010). The effects that biochar may have on nutrient transformations has consequences Biochar C15.indd 420 for the long term effect of biochar on plant productivity and on nutrient stocks (i.e. the installation of a positive reinforcing feedback loop, see Figure 15.1) and therefore have important implications for the viability and sustainability of biochar as a C mitigation strategy (Lehmann, 2007; Roberts et al, 2010). In the following section we identify three general mechanisms through which biochar may influence nutrient cycles: (i) Increase in the pool size and turnover of labile organic nutrients; (ii) Alteration of soil physical and chemical properties; and (iii) effects on soil biota. Increase in the pool size and turnover of labile organic nutrients A primary mechanism by which biochar may accelerate nutrient cycling over long time scales is by serving as a short-term source of highly available nutrients, which become incorporated into living biomass and labile soil organic pools (Jeffery et al, 2011). As described above and in detail in Chapter 7, new, unweathered biochar, especially that generated from nutrient-rich material, can be a source of highly available nutrient salts that provide a direct short-term source of nutrition to plants (Chan and Xu, 2009; Atkinson et al, 2010). During the pyrolysis process, heating causes some nutrients to volatilize (e.g. N as nitrogen oxides (NOx)), especially 11/3/2014 9:04:29 AM BIOCHAR EFFECTS ON SOIL NUTRIENT TRANSFORMATIONS Figure 15.1 A conceptual model for the influence of biochar on nutrient (Nr) turnover in the soil environment at the surface of the material, while other nutrients become concentrated in the remaining biochar (Gundale and DeLuca, 2006; Nelson et al, 2011). Feedstock, formation temperature, the time a material is held at a given temperature, oxygen availability and the heating rate directly influence the surface residue chemistry of biochar (Gundale and DeLuca, 2006; Atkinson et al, 2010). Some specific elements are disproportionately lost to the atmosphere, fixed into recalcitrant forms or liberated as soluble oxides during the heating process, affecting the chemical composition of ash residues on the biochar surface (Chan and Xu, 2009). For woodderived biochars, carbon (C) begins to volatilize around 100ºC, N above 200°C, S above Biochar C15.indd 421 421 375 ºC and potassium (K) and P between 700 and 800ºC (Neary et al, 2005), whereas the volatilization of magnesium (Mg), calcium (Ca) and manganese (Mn) only occurs at temperatures above 1000ºC (Neary et al, 1999; Knoepp et al, 2005). These differences in volatilization temperatures among elements cause shifts in the stoichiometry of biochar elemental concentrations, with total S and N concentrations often decreasing relative to other elements due to their lower volatilization temperatures (Knudsen et al, 2004; Trompowsky et al, 2005). Correspondingly, several nutrient salts accumulate on biochar surfaces, with NH4+ and SO4-2 concentrations increasing in low temperature biochars (< 500ºC) (Knudsen et al, 2004; Gundale and DeLuca, 2006) and NO3-, PO4-3, Ca+2, Mg+2 and trace metals increasing, especially in biochars formed at high temperatures (Gundale and DeLuca, 2006; Chan and Xu, 2009; Atkinson et al, 2010; Nelson et al, 2011). Because soils generally contain a relatively large total pool of most nutrients, biochar additions to soil usually provide only a modest contribution to the total soil nutrient capital (Chan et al, 2007). However, only a small fraction of the total soil nutrient capital is usually bio-available, meaning that the addition of nutrient salts in biochar surface residues can constitute a significant increase in the bio-available pool of some nutrients (Gundale and DeLuca, 2006; Yamato et al, 2006; Chan et al, 2007). This short-term input of bio-available nutrients can enhance plant productivity (i.e. total biomass) and improve tissue quality (Kimetu et al, 2008; Jeffery et al, 2011) and therefore influence both the quantity and quality of nutrient-containing plant residues returned to the soil (Major et al, 2010). Plants’ C inputs to the soil occur through root exudation and turnover, and through senescence and death of above-ground tissues. It is well known that the nutrient concentrations of plant litter is a 11/3/2014 9:04:29 AM 422 BIOCHAR FOR ENVIRONMENTAL MANAGEMENT strong control on nutrient mineralization rates (Stevenson and Cole, 1999; Brady and Weil, 2002). Therefore, larger inputs of higher quality plant organic matter to the soil in response to biochar derived nutrients likely result in an increase in the labile nutrient pool size, thereby in theory increasing the total quantity of labile organic nutrients returned back to the soil and available for mineralization (DeLuca et al, 2006; Gundale and DeLuca, 2007; Major et al, 2010). This feedback involving higher plant nutrient uptake, a higher return of labile organic nutrients to the soil and higher nutrient mineralization rates could enhance nutrient availability to plants over longer time scales as implied in Figure 15.1. The persistence of accelerated nutrient turnover between plants and soil is likely dependent on the size of the nutrient pool added from biochar, the frequency of its addition (e.g. single dose, multiple doses or annual), the degree to which nutrient capital is removed from a system during harvesting activities (Jeffery et al, 2011), the degree to which nutrients are fixed into recalcitrant organic or insoluble mineral pools (Hedley et al, 1982), the long-term losses in nutrient capital through leaching or volatilization that occur at a given site (Lehmann et al, 2003; Yanai et al, 2007) and the long-term build-up (or decline) of stable, recalcitrant organomineral complexes beyond the pure biochar. Alteration of soil physical and chemical properties In addition to its direct contribution of available nutrients to the soil, biochar has a variety of physical and chemical properties that influence soil nutrient transformations. For a more detailed review of biochar physical and chemical properties, see Chapters 5 and 6, and Atkinson et al (2010). Biochar is a high surface area (Beesley et al, 2011), highly porous (Keech et al, 2005), variable charge organic Biochar C15.indd 422 material which often contains a surface residue enriched in alkaline metals (Figure 15.2b) (Atkinson et al, 2010). When added to soil, biochar has the potential to alter the physical and chemical properties of soil, which in turn can influence nutrient transformation rates. For instance, biochar has been shown to increase soil water holding capacity, alter gas exchange, increase cation exchange capacity (CEC), increase surface sorption capacity, increase base saturation of acidic mineral soils and alter soil pH (Glaser et al, 2002; Bélanger et al, 2004; Keech et al, 2005; Liang et al, 2006; Atkinson et al, 2010). These biochar properties are highly dependent on the temperature and duration of pyrolysis (Gundale and DeLuca, 2006; Bornermann et al, 2007; Joseph et al, 2007) and the feedstock from which biochar is made (Gundale and DeLuca, 2006; Streubel et al, 2011). Many nutrient transformations are enzyme mediated reactions carried out by soil micro-organisms. Soil micro-organisms require environments with appropriate water potential and redox conditions to carry out their metabolic activities (Alexander, 1991; Briones, 2012). The physical structure of biochar contains a range of pore sizes which are inherited from the feedstock material (Keech et al, 2005) and which can directly influence the water potential and redox environment of soil micro-organisms (Joseph et al, 2010). Micropores, defined by soil scientists as pores with < 30µm diameter (Brady and Weil, 2002), serve as capillary spaces with high surface area to volume ratios and can retain water even when soil moisture is strongly depleted (Kammann et al, 2011), thereby creating moist microsites (Lehmann and Rondon, 2006). Biochar also often contains macropores (>75µm diameter) which can serve as gas exchange channels (Keech et al, 2005), thereby influencing the redox environment for soil biota (Joseph et al, 2010; Lehmann et al, 2011). Organic residues 11/3/2014 9:04:29 AM BIOCHAR EFFECTS ON SOIL NUTRIENT TRANSFORMATIONS decompose much more rapidly under aerobic conditions and therefore biochar may enhance nutrient mineralization in soils with inherently poor gas exchange properties (Gundale and DeLuca, 2006; Asai et al, 2009). Likewise, several specific nutrient transformations require oxygen as an electron acceptor, such as nitrification and S oxidation, which suggests that the physical structure of biochar may increase oxidative transformations in soils with inherently poor gas exchange environments (DeLuca et al, 2006; Asai et al, 2009; Joseph et al, 2010). The highly variable pore size distribution of biochar thus assures the presence of a wide variety of soil micro-sites with contrasting moisture and redox conditions under variable environmental conditions (Joseph et al, 2010). In all biological living systems from microorganisms to plants, gradients and potential-differences (concentrations, redox, Eh, pH) are the prerequisites for material and electron flow, i.e. for metabolism and energy gain. The addition of biochars may thus intensify microbial or root-associated gross nutrient cycling processes by: (i) creating more ‘micro-site opportunities’ with steeper redox, pH or nutrient concentration gradients around or across biochar particles (Briones, 2012; Joseph et al, 2013); and by (ii) creating more such micro-scale metabolism opportunities within the soil matrix. If the ‘biochar micro-site metabolism opportunities’ then meet higher organic (e.g. crop or root residue) inputs, a positive feedback cycle with intensified gross nutrient cycling may result, improving soil fertility in the long run (Figure 15.1). Additional mechanisms through which biochar amendments can alter nutrient transformations is by: (i) Reducing nutrient loss from the soil (Crutchfield et al, 2010; Ding et al, 2010; Prendergast-Miller et al, 2011; Ventura et al, 2013); (ii) Reducing fixation of nutrients into insoluble mineral or recalci- Biochar C15.indd 423 423 trant organic pools (Cui et al, 2011; Nelson et al, 2011); (iii) Reduced gaseous losses of N, be it as NH3, N2 or N2O (Prendergast-Miller et al, 2011; Taghizadeh-Toosi et al, 2012a; Spokas et al, 2012); (iv) By ameliorating other constraints of nutrient cycling e.g. in contaminated soils by its sorptive properties (Figure 15.1). Biochar has been shown to have a transient anion exchange capacity and moderately high CEC that also changes with time in the soil (Brewer et al, 2011). Biochar also can ameliorate soil pH due to its surface ash residue containing alkaline metals, especially in acidic soils (Brewer et al, 2011). Some biochars can harbour relatively high exchange capacity per unit mass (Atkinson et al, 2010), therefore its addition to some soils can increase surface soil exchange capacity. Free nutrient ions can be lost from ecosystems via leaching or runoff, resulting in a decline in soil fertility through time. Biochar can reduce leaching and volatilization losses under some circumstances (PrendergastMiller et al, 2011; Taghizadeh-Toosi et al, 2012a; Spokas et al, 2012; Ventura et al, 2013) and thus increase the total pool of nutrients available to plants or microbes. A variety of studies suggests that biochar can simultaneously reduce nutrient leaching and volatilization losses through its influence on soil pH (Bélanger et al., 2004, Atkinson et al., 2010) and CEC (Crutchfield et al, 2010; Ding et al, 2010); however, the alkaline nature of some biochars may actually increase NH3 volatilization in surface soils amended with biochar (Chen et al, 2013). An additional characteristic of biochar that can influence nutrient cycling is its effect on soil solution C chemistry (Figure 15.1) and turnover (see Chapter 16). While biochar itself has been shown to contain only a minor fraction of bio-available C (Jones et al, 2010; Major et al, 2010), several studies suggest that it serves as a strong sorptive surface for a wide range of C compounds. The high surface area, 11/3/2014 9:04:29 AM 424 BIOCHAR FOR ENVIRONMENTAL MANAGEMENT porous (Figures 15.2 and 15.3) and often hydrophobic nature of biochar directly after production makes it an ideal surface for the sorption of hydrophobic organic compounds (Cornelissen et al, 2004; Keech et al, 2005; Bornermann et al, 2007; Gundale and DeLuca, 2007). Numerous studies have shown a reduction in soluble or free phenolic compounds when activated C is added to soils (DeLuca et al, 2002; Wallstedt et al, 2002; Berglund et al, 2004; Keech et al, 2005; Gundale and DeLuca, 2006; MacKenzie and DeLuca, 2006). Additional studies have demonstrated that char formed during wildfires or burning of agricultural residues also functions to adsorb phenolic and various aromatic and hydrophobic organic compounds (Yaning and Sheng, 2003; Brimmer, 2006; DeLuca et al, 2006; Gundale and DeLuca, 2006; MacKenzie and DeLuca, 2006; Bornermann et al, 2007). Through these sorption reactions, biochar may: (i) reduce the activity of compounds that may be either inhibitory to nutrient transformation specialists, such as nitrifying bacteria (White, 1991; Ward et al, 1997; Paavolainen et al, 1998); (ii) reduce complexation of nutrient-rich molecules such as proteins into tannin-complexes (Kraus et al, 2003; Gundale et al, 2010); or (iii) reduce the concentration of bio-available C in the soil solution that would otherwise enhance the immobilization of inorganic N, P or S (Schimel et al, 1996; Stevenson and Cole, 1999) (Figure 15.1). The interaction of soluble soil C with biochar surfaces is a key mechanism that may influence nutrient availability and transformations, but has received relatively little attention (MacKenzie and DeLuca, 2006; Nelissen et al, 2012). Alteration of microbial communities Biochar additions to soil have the potential to change the biomass, community composition and activity of soil microbes, all of which can Biochar C15.indd 424 Figure 15.2 Electron micrographs of a high sorption (a) and low sorption (b) char collected from forest soils in northern Idaho (Brimmer, 2006). The high sorption char (immature char formed in a recent fire) has open pores that follow trachieds whereas the low sorption char (mature char) has many of the pores occluded with organics influence nutrient mineralization from decomposing plant residues, as well as several specific nutrient transformations. For a complete review of biochar effects on soil microbial communities, see Chapter 13. There are several mechanisms proposed by which biochar can influence soil microbes, including the porous structure of biochar which provides a habitat for microbes (Pietikäinen and Fritze, 1993), its effects on plant growth and associated plant C inputs (Major et al, 2010), its source of trace minerals (Rondon et al, 11/3/2014 9:04:29 AM BIOCHAR EFFECTS ON SOIL NUTRIENT TRANSFORMATIONS 425 Figure 15.3 The pH, electrical conductivity (EC), cation exchange capacity (CEC) and density of biochar produced from Douglas-fir or ponderosa pine wood or bark at 350 or 800°C (from Gundale and DeLuca, 2006). Data meeting the assumptions of normality were compared with one-way ANOVA followed by the Student-Neuman-Kuels post hoc procedure where letters indicate pairwise differences. Non-normal data were compared using the Kruskal-Wallis (K-W) statistic 2007), its sorption of microbial signalling compounds or inhibitory plant phenolic compounds (DeLuca et al, 2006; Ni et al, 2010), as well as its effect on soil physical and chemical properties (described on page 422). Very few studies have attempted to isolate the relative importance of these factors and substantial uncertainty remains regarding the mechanisms through which biochar influences soil microbial community properties (Lehmann et al, 2011). Despite mechanistic uncertainty, several studies have shown that increases in micro- Biochar C15.indd 425 bial biomass appear to occur in response to soil biochar amendments. O’Neill et al (2009) and Liang et al (2010) showed that Amazonian Anthrosol soils rich in pyrogenic C (PyC) contained between one and two orders of magnitude greater microbial biomass than adjacent soils with low PyC concentrations. In short-term studies with biochar amendments, Anderson et al (2011) showed somewhat more modest increases of between 5–14 per cent in the abundance of a variety of microbial taxonomic groups in response to biochar amendment in a temper- 11/3/2014 9:04:29 AM 426 BIOCHAR FOR ENVIRONMENTAL MANAGEMENT ate pasture soil. Pietikäinen et al (2000) also showed that microbial respiration and biomass increased in response to additions of pyrogenic carbonaceous matter (PCM) in boreal soils. However, other studies have shown no significant shift in microbial activity with biochar amendments to soils (Jones et al, 2012). Although soil microbes are the primary driver of organic nutrient mineralization and oxidative or reductive nutrient transformations, these studies suggest that biochar-induced changes in microbial communities likely have consequences for nutrient turnover rates between plants and soil. In addition to observed shifts in microbial biomass in response to biochar, a variety of studies have shown that microbial community composition can be altered by biochar (Anderson et al, 2012; Jones et al, 2012; Ducey et al, 2013), sometimes resulting in increased abundance of functional groups that have key roles in nutrient cycling and plant nutrient acquisition (Lehmann et al, 2011). Mycorrhizal fungi, which play a key role in extracting nutrients from recalcitrant organic or insoluble mineral pools, have been observed to both increase (Saito, 1990; Makoto et al, 2010; Solaiman et al, 2010) and decrease (Warnock et al, 2007; Lehmann et al, 2011) in response to biochar addition to soil. Given the specific functional role of mycorrhizae in nutrient acquisition, changes in mycorrhizal biomass and colonization likely influence the flux of nutrients from unavailable nutrient pools (i.e. recalcitrant organic matter and insoluble minerals, in particular P) into biomass and therefore labile organic pools that actively turn over between plants and soil, although studies identifying the effect of biochar on these fluxes are lacking. In addition to mycorrhizae, several specific nutrient transformations have been shown to either increase or decrease in response to soil biochar amendments and in some cases altered transformation rates have been linked to changes in the abundance of specific soil biota. One of the clearest examples of this is the frequently observed increase of nitrification rates in biochar amended forest soils (DeLuca et al, 2006; Gundale and DeLuca, 2007), which has been linked to larger populations of nitrifying bacteria in biochar pore spaces (Ball et al, 2010; described in further detail below). While an increasing number of studies have described changes in either microbial community composition or changes in nutrient transformation rates in response to biochar amendment (Lehmann et al, 2011), there remain a relatively small number that explicitly link altered nutrient transformation rates to functional changes in the soil microbial community (Ball et al, 2010; Ducey et al, 2013). Influences of biochar on specific nutrient transformations As previously described, there are a range of mechanisms through which biochar can influence the loss of nutrients from forest or agricultural ecosystems, as well as the gross annual turnover between soils and plants. However, plant nutrients differ substantially in many key physical and chemical properties, such as the number of molecular species that exist, the mass and potential energy of Biochar C15.indd 426 those molecular species and the ability of microbes to transform molecular species to acquire energy under given soil conditions (i.e. pH and redox potential). These individualistic properties of different nutrient elements can determine how the cycles of specific elements respond to soil biochar amendments. In the following sections we review the influence of biochar on N, P and S 11/3/2014 9:04:29 AM BIOCHAR EFFECTS ON SOIL NUTRIENT TRANSFORMATIONS 427 cycles. Biochar always contains some quantity of soluble inorganic N and P (see Chapter 7 and Figure 15.4) which can be released rapidly or slowly into the soil; however, in this section we will focus on the influence of biochar on transformations of nutrients in the soil as opposed to nutrient delivery. Nitrogen Nitrogen is the single most limiting plant nutrient in most cold or temperate terrestrial ecosystems (Vitousek and Howarth, 1991) and also most frequently limits agricultural productivity. In soils, the majority of N exists in complex organic forms that must be mineralized (converted from organic N to NH4+ or NO3-) prior to uptake by most agricultural plants (Stevenson and Cole, 1999), although it is increasingly recognized that most plants also take up organic N (Jones et al, 2002; Schimel and Bennett, 2004). Recent studies have demonstrated that the addition of biochar to surface mineral soils may directly influence N transformations. Here we review the evidence for the direct and indirect influences of biochar on ammonification, nitrification, volatilization, denitrification, N2O emission (see also Chapter 17) and N2-fixation, while providing potential mechanisms that may be driving these transformations. Ammonification and nitrification Nitrogen mineralization is the process by which organic N is converted to inorganic forms (primarily NH4+ and NO3-). The conversion of organic-N to NH4+ is generically termed ammonification. This process is driven by a broad consortium of organisms capable of enzymatic denaturation of proteins and the removal of amide groups from organic compounds (e.g., amino acids and amino sugars). Nitrification represents the oxidation of organic N (via heterotrophic organisms) or NH4+-N to NO3- by autotrophic bacteria and Biochar C15.indd 427 Figure 15.4 The soluble PO4-3, NH4+ and NO3- concentration in biochar produced from Douglas-fir or Ponderosa pine wood or bark at 350 or 800ºC (from Gundale and DeLuca, 2006). Data meeting the assumptions of normality were compared with one-way ANOVA followed by the Student-NeumanKuels post hoc procedure where letters indicate pairwise differences. Non-normal data were compared using the Kruskal-Wallis (K-W) statistic archaea as well as certain fungi (Stevenson and Cole, 1999; Leininger et al, 2006). Biochar addition to temperate and boreal forest soils has been found to increase net nitrification 11/3/2014 9:04:30 AM 428 BIOCHAR FOR ENVIRONMENTAL MANAGEMENT rates in soils that otherwise demonstrate little or no net nitrification (Berglund et al, 2004; DeLuca et al, 2006); whereas, there has been little evidence for such an effect in grassland (DeLuca et al, 2006) or agricultural soils (Lehmann et al, 2003; Rondon et al, 2007), which may already accommodate an active nitrifying community. Results from the literature are summarized in Table 15.1, which specifically focuses on ammonification and nitrification resulting from biochar or activated carbon amended soil samples, field plots, or mesocosms, as compared to unamended controls. Several studies in forest ecosystems have aimed to understand the mechanisms underlying increased nitrification following PCM addition. Using forest soils with very low inorganic N concentrations, DeLuca et al (2002) showed that ammonification was enhanced when a labile organic N substrate (i.e. glycine) was added to the soil, indicating that ammonification was substrate limited. In contrast, the large increase in NH4+ that resulted from the glycine addition did not cause soil NO3- concentration to increase, suggesting that nitrification was not substrate limited (DeLuca et al, 2002); rather, nitrification rates exceeded ammonification rates. In the same study, the injection of activated carbon into the organic horizon induced a slight stimulation of nitrification (see Table 15.1), but the injection of glycine with activated carbon consistently stimulated high rates of nitrification, demonstrating that biochar in some way alleviated the factor limiting nitrification (DeLuca et al, 2002; Berglund et al, 2004). Char collected from recently burned forests (DeLuca et al, 2006; MacKenzie and DeLuca, 2006) or generated in laboratories under controlled conditions (Gundale and DeLuca, 2006) were found to stimulate net nitrification in laboratory incubations and in short-term (24hr) nitrifier activity assays. One possible mechanism is that activated car- Biochar C15.indd 428 bon adsorbed organic compounds (and specifically terpenes) that either inhibited net nitrification (White, 1991; Ward et al, 1997; Paavolainen et al, 1998) or caused immobilization of NH4+ (McCarty and Bremner, 1986; Schimel et al, 1996; Ward et al, 1997; Uusitalo et al, 2008). The rapid response of the nitrifier community to biochar additions in soils with low nitrification activity and the lack of a stimulatory effect on actively nitrifying communities suggest that biochar may be adsorbing inhibitory compounds in the soil environment (Zackrisson et al, 1996) that then allows nitrification to proceed. Similarly, fire induces a short-term influence on N availability, but biochar may act to maintain that effect for years to decades after a fire. It is also possible that the presence of biochar in these forest soils enhances the numbers of ammonia oxidizing bacteria by creating conditions conducive to their growth (increased pH, reduced inhibitory compounds, microsites, redox potential, external electron transfer) (Ball et al, 2010). In another study seeking to explain charinduced increased nitrification rates in nutrient poor conifer forests, DeLuca et al (2006) evaluated gross nitrification rates in chartreated and untreated forest soils. Gross nitrification rates in the char-amended forest soils were nearly four times that in the untreated soil, demonstrating the stimulatory effect of char on the nitrifying community rather than reduced immobilization. We also found that sterilized soils treated with biochar also exhibited a modest increase in nitrifier activity (DeLuca, unpublished data) suggesting that the oxide surfaces on biochar may stimulate some quantity of auto-oxidation of NH4+ (DeLuca et al, 2006). Wood ash commonly contains high concentrations of metal oxides including CaO, MgO, Fe2O3, TiO2 and CrO (Koukouzas et al, 2007). Exposure of biochar to solubilized ash may result in the retention of these potentially catalytic oxides on active 11/3/2014 9:04:30 AM Biochar C15.indd 429 11/3/2014 9:04:30 AM Lab Biochar, Ponderosa pine wood Lab Biochar, Ponderosa pine (wood and bark), Douglas-fir (wood and bark) Activated Carbon Activated Carbon Ponderosa pine, Western MT Scots Pine, Sweden Scots Pine, Sweden Wildfire Biochar, Ponderosa pine wood Biochar Type Ponderosa pine, Western MT Forested Ponderosa pine, Western MT Ecosystem Glycine in lab, aerobic incubation, 60 days 0.06 ± 0.02 2.8 ± 0.4 46 ± 6 (µg N g soil -1) 5±1 47 ± 4 (µg N g soil -1) Glycine in lab, aerobic incubation, 14 days 20 ± 13 (µg N cap-1) ‡ 40 ± 5 NA (µg N g soil -1) (NH4)SO4 and H2PO4 in lab, aerobic incubation, 15 days Glycine in Field, resin collected, 30 days 200 ± 100 1350 ± 50 5.5 ± 0.6 YES NH4+ YES NO3- YES NH4+ YES NO3 high 1.89 ± 1.1 NO NH4+ YES NO3- NO NH4+ NO NO3- high 780 ± 302 dfb 16 ± 4 dfb 27 ± 3 YES NH4+ YES NO3- YES NH4+ YES NO3- dfw 11 ± 8 dfw 32 ± 8 low 0.12 ± 0.03 ppb 20 ± 8 ppb 25 ± 6 YES NH4+ YES NO3- YES NO3- NO NH4+ YES NO3- Statistical Difference low§ 410 ± 99 ppw 21 ± 4 70 ± 3 1200 ± 500 NO3- - N ppw † 20 ± 5 NA 700 ± 400 NH4+ - N NH4+ - N NO3- - N Biochar Addition Control 150 ± 200 (µg N cap-1) ‡ Glycine in greenhouse, resin collected, 30 days Nutrient Source and Incubation Berglund et al (2004) DeLuca et al (2002) Gundale and DeLuca (2006) DeLuca et al (2006) MacKenzie and DeLuca (2006) Reference Table 15.1 The effect of biochar (natural biochar, lab-generated biochar, or activated carbon) on nitrogen mineralization, nitrification and immobilization from studies performed in soils of different ecosystems around the world Biochar C15.indd 430 11/3/2014 9:04:30 AM Biochar Type Mineralizable N None, Aerobic 49 days Four feedstocks, Douglas-fir wood, Douglas-fir bark, Switch grass, Digested fibre 5 agronomic soils (S, SiL), Washington Area 30 to 70 (mg N kg-1) 26.8 ± 12.2 0.24 ± 0.08 30.7 ± 12.6 fresh0.63 ± 0.45 old 5.16 ± 3.50 Lower 1.74 ± 0.30 old 3.87 ± 0.76 Mineralizable N 1.05 ± 0.05 43.98 67 days ND fresh 1.42 ± 0.21 78.67 0.6 ± 0.1 25 days 2.25 146 ± 42 - NO3 - N ‡ Ionic resin analysis used approximately 1g mixed bed resin in nylon mesh capsules approximately 25.4mm in diameter † ppw – Ponderosa pine wood; ppb – Ponderosa pine bark; dfw – Douglas-fir wood; dfb – Douglas-fir bark biochar produced at 350ºC § Low biochar application rate of 1,000kg ha-1, high application rate was 10,000kg ha-1 !! Sand (S) and silt loam (SiL) textured soils 15.0 ± 14.2 (mg N kg-1) None, aerobic, 7 days Mixed Harwood Biochar Perennial Rye Eutric Camisol Wales, UK 2.02 ± 0.31 3.70 ± 0.38 (mg N kg-1) None, aerobic, 7 days 4.74 (mg L-1) 49 kg ha-1 UAN (28-0-0), aerobic, 25 days Wheat Residue Biochar 256.85 20 ± 3 (µg N cap-1) ‡ 0.20 ± 0.20 NH4 - N NO3 - N + NH4 - N - Biochar Addition + Control Glycine in Field, resin collected, 75 days Nutrient Source and Incubation Winter Wheat Kandsol Soil Australia Forested continued Scots Pine, Sweden continued Agricultural Corn Production Pecan Shell South Carolina Biochar Ecosystem Table 15.1 continued Novak et al (2010) Reference Significantly lower in most cases Streubel et al (2011) Not Reported Dempster et al (2012) Not Reported Dempster et al (2012) NO NH4+ NO NO3- NO NH4+ YES NO3- YES NH4+ NO NO3- Statistical Difference BIOCHAR EFFECTS ON SOIL NUTRIENT TRANSFORMATIONS surfaces of the biochar (Le Leuch and Bandosz, 2007). These oxide surfaces may in turn effectively adsorb NH4+ or NH3 and potentially catalyse the photo-oxidation of NH4+ (Lee et al, 2005). More work is required to understand these variable mechanisms on nitrification in forest soils. In contrast to forested ecosystems, biochar additions in agricultural systems have yielded mixed results, partially based on the variety of feedstocks tested in agricultural trials. Biochar additions to agricultural soils have been found to reduce, have no effect or in some cases increase net N mineralization (Yoo and Kang, 2010; Streubel et al, 2011; Güereña et al, 2013). Streubel et al (2011) tested 5 different soils from the agronomic regions of Washington state, ranging in texture from sand to silt loam (Table 15.1) and amended with three rates of biochar (9.8, 19.5 and 39.0Mg ha−1), produced from four different feedstocks (Douglas-fir wood and bark, switchgrass stubble and digested fibre). In this study, biochar had no significant effect, or reduced N mineralization regardless of feedstock, for all but the sandy soil amended at the highest quantity of switchgrass biochar, which had significantly higher NH4+ and NO3- production. Contrasting results were reported in alkaline, calcareous agricultural soils amended at a rate of 1–10 per cent switchgrass biochar in a laboratory incubation, wherein biochar applications reduced NH4+ and NO3- accumulation (Ducey et al, 2013). However, when soils are treated with biochar produced from a N-rich feedstock (e.g. swine manure), increases in net N mineralization and net nitrification have been observed in laboratory incubations (Yoo and Kang, 2010). Importantly, barley straw biochar amendments to the same soils had no significant effect on N mineralization. Using molecular analyses (TRFLP and 454 pyrosequencing) microbial response to biochar additions were studied in agricultural Biochar C15.indd 431 431 soils; the presence of Nitrosovibro (NH4+ → NO2-) was found to decrease in the presence of biochar while Nitrobacter (NO2- → NO3-) was observed to increase in the presence of biochar (Anderson et al, 2012). However, these shifts could have little consequence for nitrification rates as molecular analyses have also demonstrated little or no relationship between gene abundance of ammonia oxidizing bacteria and rates of NO3- accumulation (Ducey et al, 2013). Such results emphasize the contrast between the strong positive effects biochar amendment has on forest soils, where little or no net nitrification occurs, compared to absence of effects in agricultural soils, that already exhibit inherently high rates of net nitrification and NO3- accumulation (e.g. over 113mg NO3- -N kg-1 in the control, Ducey et al, 2013) prior to biochar additions. Interestingly, Nelissen et al (2012) reported a significant increase in gross ammonification and nitrification rates in sandy soils amended with maize biochar with the increase in nitrification being attributed to greater substrate availability for autotrophic nitrifying bacteria. The length of time that biochar resides in the soil environment has also been shown to affect N mineralization potential which may be related to its occlusion with organic matter over time as postulated by Zackrisson et al (1996). Dempster et al (2012) found that soils amended with ‘old’ biochar resulted in greater inorganic N accumulation than soils amended with ‘fresh’ biochar in different agronomic soils from both Australia and the UK (Table 15.1). This might have significant implications for management practices that are using biochar to retain inorganic N fertilizer on-site. Regular additions of ‘fresh’ biochar to agricultural systems might be needed to help retain inorganic N fertilizers and this practice may also sequester large amounts of C. In contrast, Novak et al (2010) reported a modest increase in net N mineralization when 11/3/2014 9:04:30 AM 432 BIOCHAR FOR ENVIRONMENTAL MANAGEMENT fresh wood biochar was added to acidic agricultural soils. Biochar additions to agricultural soils of the tropics have been reported to either reduce N availability (Lehmann et al, 2003) or to increase N uptake and export in crops (Steiner et al, 2007; Cornelissen et al, 2012). Reduced N availability may be a result of the high C:N of biochar and thus greater potential for adsorption of NH4+ to biochar which in turn reduces the potential for N leaching losses and sustained higher N fertility over time in surface soils (Steiner et al, 2007). Alternatively, a biochar-induced increase in microbial biomass could result in net immobilization of N as demonstrated in 15 N fertilizer trials on corn fields in New York (Güereña et al, 2013). Several studies have suggested that biochar can adsorb NH4+ from the soil solution (Lehmann et al, 2011; Spokas et al, 2012; Taghizadeh-Toosi et al, 2012a), thus reducing the availability of NH4+ for autotrophic conversion to NO3-; however, this hypothesis has not been adequately tested. Increased sorption of NH4+ could, at least temporarily create localized concentrations for microbial use or plant uptake. Although reduced N2O emissions with biochar additions have been ascribed to increased sorption of NO3- by biochar (van Zwieten et al, 2010), NO3- sorption to wood biochar has also been reported to be insignificant (Jones et al, 2012). In addition to sorption of inorganic N, biochar also has the potential to adsorb organic N compounds (amino acids, peptides, proteins) which could reduce N net mineralization or nitrification, or stimulate N-fixing microbial growth around and within biochar particles, coating them with N-retaining microbes. Moreover, biochar in soil ultimately becomes occluded with organic matter and may aggregate both mineral and organic matter fractions together into physically protected pools (Brodowski et al, 2006), N present in these organic pools would likely remain unavailable Biochar C15.indd 432 for some period of time and be protected against transformation. Immobilization Biochar from wood or other N-poor feedstocks is an N-depleted material with a high C:N ratio; however, biochars generated from N-rich feedstocks can serve as a N source (Lehmann et al, 2006). It has generally been found that some decomposition occurs when fresh biochar is added to soil (Schneour, 1966; Spokas et al, 2009; Jones et al, 2011), although it is also well known that wood biochar is highly recalcitrant (DeLuca and Aplet, 2008). It is therefore uncertain whether biochar amendments provide sufficient bioavailable C to stimulate immobilization (although this argument is often cited). Several studies have demonstrated increased respiration rates with biochar additions to soil and suggested that the biochar was being degraded or that the biochar induced priming of resident soil C or fresh C (Wardle et al, 2008; Spokas et al, 2009; Novak et al, 2010). However, recent studies have shown that increased CO2 evolution, which is usually indicative of increased microbial activity, upon biochar additions was actually partly due to emission of inorganic C (i.e. carbonates) from within the applied biochar (Jones et al, 2011). Low-temperature biochars, in particular, would be more likely to induce net nutrient immobilization, because they contain higher concentrations of bioavailable C and residual bio-oils (Steiner et al, 2007; Nelissen et al, 2012; Clough et al, 2013) or surface functional groups (Liang et al, 2006) that can serve as microbial substrates. Higher temperature biochars, in contrast, contain much higher concentrations of graphene structures which are much more resistant to microbial degradation and less residual volatiles. When biochars do provide a significant concentration of bioavailable C (see Chapter 16), any immobilization stimulated by bio- 11/3/2014 9:04:30 AM BIOCHAR EFFECTS ON SOIL NUTRIENT TRANSFORMATIONS char would likely lead to only short-term reductions in available inorganic N pools that could reduce nitrification and N2O emissions (Chapter 17) (Steiner et al, 2007). Gaseous nitrogen emissions Over the past several years there has been an increasing interest in understanding how biochar influences the gaseous soil N transformations in order to understand ecosystem N budgets and effects of biochar management on greenhouse gas emissions. Much interest has focused on the influence of biochar on N2O flux (i.e., it has a global warming effect per molecule that is 298 times greater than CO2) (Yanai et al, 2007; Spokas et al, 2009; Clough et al, 2010; Cornelissen et al, 2012), because of its importance as a greenhouse gas (Hansen et al, 2005) and ozone-depleting substance (Ravishankara et al, 2009). Several studies have also addressed the influence of biochar applications on denitrification and NH3 volatilization potential to evaluate the influence of biochar on N conservation in agricultural soils (Jones et al, 2012; Taghizadeh-Toosi et al, 2012a). Nitrous oxide emissions from soil are associated with the processes of nitrification and denitrification and this topic is covered in detail in Chapter 17. To date there have been a number of papers devoted to assessing N2O generation (as a greenhouse gas) on biochar-amended agricultural soils, but far less effort geared towards assessing the influence of biochar on denitrification potential. Kammann et al (2012) reported a significant decrease in N2O emissions under ‘denitrification inducing conditions’ following the addition of 50Mg ha-1 of peanut hull biochar to an agricultural Luvisol in Germany. However, when the biochar was added with 50kg N ha-1 as NH4NO3, N2O emissions actually increased with biochar additions (Kammann et al, 2012). The latter results are similar to the findings of Biochar C15.indd 433 433 Jones et al (2012) which demonstrated an increase in denitrification enzyme activity DEA in north Wales where soils had been treated with 50Mg wood biochar ha-1 and 100kg N ha-1 as NH4NO3 two years prior to sampling. Studies have also demonstrated an increase in denitrifying bacterial communities with biochar additions to soil (Anderson et al, 2012; Ducey et al, 2013). As indicated above, biochar applications to agricultural or grassland soils that exhibit high rates of nitrification have generally been found to have no effect or a negative effect on net nitrification rates (DeLuca et al, 2006; Rondon et al, 2007; Dempster et al, 2012; Jones et al, 2012) which would act as to reduce denitrification potential. In contrast, forest soils that otherwise express little or no net nitrification respond to biochar or activated carbon additions by exhibiting an increase in net nitrification and nitrifier activity (Berglund et al, 2004; DeLuca et al, 2006). Further, accumulation of NO3- in soils treated with soluble C-rich biochar would act to increase denitrification potential under anaerobic conditions (McCarty and Bremner, 1992). Hydochar produced under hydrothermal conditions increases soluble C additions and has the potential to increase respiration (Kammann et al, 2012) and denitrification potential. However, application of wood biochar likely results in a long-term net decrease of soluble organic C (see Chapter 16), which would in turn reduce denitrification potential. Several recent studies have also evaluated the influence of biochar on NH3 volatilization (Steiner et al, 2010; Doydora et al, 2011; Jones et al, 2012; Taghizadeh-Toosi et al, 2012a, b; Chen et al, 2013). Ammonia volatilization in agricultural soils is favoured at alkaline pH and when high concentrations of NH4+ are present and is reduced in soils with high CEC (Stevenson and Cole, 1999). Biochar and biochar mixed with ash are 11/3/2014 9:04:30 AM 434 BIOCHAR FOR ENVIRONMENTAL MANAGEMENT known to temporarily increase soil pH (Glaser et al, 2002; Jones et al, 2012), but usually not to a high enough level to increase NH3 volatilization. Taghizadeh-Toosi et al (2012a,b) have shown instead that NH3 is effectively sorbed to the surface of wood biochar, but also demonstrate that it can be desorbed into solution as NH4+ thereby preventing N losses to the atmosphere. Biochar additions to agricultural soils as well as acid forest soils have been found to reduce NH4+ concentrations (Le Leuch and Bandosz, 2007; Taghizadeh-Toosi et al, 2012a) which reduces the potential for NH3 volatilization. Steiner et al (2010) found a clear reduction in NH3 evolution during poultry litter composting when biochar amendment rates were 20 per cent (w/w). Doydora et al (2011) found 50–60 per cent reductions in NH4+ available for volatilization when composting poultry litter was cut 1:1 with biochar prior to incorporation into soil. This finding is supported to some degree by Jones et al (2012) who found a clear capacity of biochar to adsorb NH4+. Furthermore, in field trials the researchers showed a reduction in NH3 volatilization at rates of 50Mg biochar ha-1, but not at 25Mg biochar ha-1 (Jones et al, 2012). In agricultural soils, it appears that biochar generally results in a reduced presence of extractable NH4+, likely as a result of sorption of soluble NH4+ to biochar surfaces. However, the reduced occurrence of NO3formation in agricultural soils treated with biochar suggests that the reduced oxidative pathway may leave more NH4+ present and available for immobilization. Further studies are clearly required to determine the capacity of biochar to reduce volatilization of soil or applied NH4+. Biological nitrogen fixation Biological N2 fixation historically provided the vast majority of N inflow into agroecosys- Biochar C15.indd 434 tems (Galloway et al, 2008). Today it is mandatory in low-input agroecosystems where external N inputs are minimal. A thorough understanding of the influence of biochar on both symbiotic and free-living N2 fixing organisms is needed. The influence of biochar on N2 fixation in leguminous plants was studied with some intensity over half a century ago, as researchers investigated the role of charcoal as a soil amendment. Although char was noted to have positive influence on soil physical properties (Tryon, 1948), there has been no consistent observed influence of biochar on N2 fixing leguminous plants. Table 15.2 provides a summary of results of studies on the influence of PCM applications on nodulation and N2 fixation in leguminous plants. Several of these studies are described in the following section. Vantis and Bond (1950) found that the addition of wood biochar to soils at a rate of 1 per cent (v/v) resulted in a reduction in the number of nodules on clover, but increased the total nodule mass and total N2 fixed in Pisum sativum (L.). However, at higher rates of biochar (greater than 2 per cent) there was no effect or a negative effect of biochar on nodulation (Vantis and Bond, 1950). Turner (1955) found a significant increase in the number of root nodules in clover (Trifolium pratense L.), but only after an initial reduction compared to the control. Their work went on to show that boiled biochar further increased nodulation and suggested that inhibitory compounds can be removed by various forms of pretreatment of biochar (Turner, 1955) (this treatment may have influenced phytohormone-like chemicals, see Chapter 14). Investigation of composts with or without biochar added (5% w/w) as a growth medium suggested that the biochar additions resulted in a significant decrease in nodule number and size (Devonald, 1982), however, there is no discussion on pretreatment of the biochar or its polyaromatic hydrocarbon (PAH) content. 11/3/2014 9:04:30 AM Biochar C15.indd 435 11/3/2014 9:04:30 AM Pisum sativum “ “ “ “ Trifolium pratense P. sativum Medicago sativum Phaseolus vulgaris “ “ Glycine max “ Trifolium repens Trifolium repens Wood biochar 2% Wood biochar 4% Wood biochar 8% Activated carbon 1% Animal biochar 2% Wood biochar 1% –2% ¶ Wood biochar powder 1:1 Wood bark biochar ~ 1% Wood biochar 3% Wood biochar 6% Wood biochar 9% Chicken manure biochar ~ 0.4% Chicken manure biochar ~ 0.8% Wood biochar ~2.5% Wood biochar ~ 5% NA: Not available NS: Not significant at P < 0.05 Response plant Biochar type and rate Neutral Neutral +41% +5% NS + 39% + 25% +70% - 24% NA NS or neutral + 8% + 45% + 37% Growth response -70% NA +190% +100% NA NA NA NA - 39% + 97% -% -% - 31% - 11% + 25% Nodulation + 350% + 250% NA NA NS + 64% + 42% +517% NA NA NA NA NA NA NA Nitrogenase Activity Quilliam et al (2012) Quilliam et al (2012) “ Tagoe et al (2008) “ “ Rondon et al (2007) Nishio and Okano (1991) Devonald (1982) Turner (1955) “ “ “ “ Vantis and Bond (1950) Source Table 15.2 Summary of research findings on the influence of biochar or activated C on growth, nodulation and N2 fixation in leguminous crops. For each study, percentage change in individual variables were calculated relative to an experimental control. All studies are pot trials with the exception of Quilliam which combines field application of biochar with a growth chamber pot trial 436 BIOCHAR FOR ENVIRONMENTAL MANAGEMENT These findings are supported by more recent studies that demonstrate a noted inhibitory effect of activated carbon on nodulation in Lotus corniculatus (L.) (Wurst and van Beersum, 2008). On the other hand, the application of a nutrient-rich biochar (carbonized chicken manure) to silt loam soils in a greenhouse experiment was found to increase nodule number and mass in soybeans (Glycine max L.) and increase total N yield (Tagoe et al, 2008). In a recent field study (Quilliam et al, 2013), high rates of wood biochar were applied to temperate agricultural soils, (total applications of 25, 50 and 100kg biochar ha-1), soils were collected and placed in pots and seeded to clover (T. repens). Clover plants grown in the presence of high rates of biochar were observed to have reduced numbers of nodules, but the mass of nodules was increased as was nitrogenase activity (Quilliam et al, 2013). Rondon et al (2007) tested the effect of adding different amounts of wood (eucalypt) biochar to nodulating and non-nodulating varieties of the common bean, Phaseolus vulgaris, inoculated with Rhizobium strains and measured changes in N uptake using an isotope pool dilution technique. Biochar was found to significantly increase N2 fixation and bean productivity at application rates of 30 or 60g biochar kg-1 compared to a control, but the highest application rate, 90g biochar kg-1 soil reduced bean productivity (Rondon et al, 2007). All biochar treatments increased the percentage of N in bean tissue derived from N2 fixation. The study further indicates that biochar may stimulate N2 fixation as the result of increased availability of trace metals such as nickel (Ni), iron (Fe), boron (B), titanium (Ti) and molybdenum (Mo). The highest rates of biochar application decreased the magnitude of the effect and if taken to the extreme might interfere with N2 fixation. It is possible that lack of consistent effects of biochar on legume performance and nodu- Biochar C15.indd 436 lation is due to differences in nutrient contents of the various biochars and their respective potential to adsorb signalling compounds. There is certainly variation in the nutrient content and sorption capacity of various types of biochar. Nodule formation in leguminous plants is initiated by the release of signalling compounds, often flavonoids (Jain and Nainawatee, 2002). Such polyphenolic compounds are readily sorbed by biochar (Gundale and DeLuca, 2006). This might explain why some studies have shown that activated carbon reduces nodulation, while low sorption P-rich biochars increased nodulation, which is presumably the result of alleviating P-limitation of nodulating bacteria with high P demands, such as Rhizobium spp. (Rondon et al, 2007). Numerous studies have been conducted to evaluate the potential for increasing the activity of free living N2 fixing bacteria in agroecosystems, however, this has only been directly evaluated in a few papers (Table 15.2). One methodological limitation to studying this is that biochar additions to soil likely increase ethylene production (Spokas et al, 2010; see also Chapter 14), which is used as a surrogate for N2 fixation activity in the acetylene reduction assay, the most commonly used technique to estimate nitrogenase activity. It is well understood that excess soluble N in the soil solution reduces N2 fixation rates in free-living N2-fixing bacteria (Kitoh and Shiomi, 1991; DeLuca et al, 1996) and available soil P can stimulate N2 fixation (Chapin et al, 1991). Therefore, it is possible that the activity of free living N2-fixing bacteria could be increased by biochar-induced increases in P solubility (Lehmann et al, 2003; Steiner et al, 2007) and reduced soluble soil N concentrations (due to immobilization or surface adsorption of NH4+). Biochar therefore potentially represents a good carrier or medium for the growth and proliferation of free-living N2-fixing bacteria. Wood and 11/3/2014 9:04:30 AM BIOCHAR EFFECTS ON SOIL NUTRIENT TRANSFORMATIONS cellulose based biochars are low N media, yet serve to sorb soil P (see Chapter 7). Conversely, however, in low inorganic N environments, biochar is known to stimulate net nitrification (e.g., DeLuca et al, 2006) and thus may ultimately down-regulate N2 fixation by free-living N2-fixing bacteria. While many of these mechanisms may influence the activity of free living N2-fixing bacteria, very little work has been done on this topic. Phosphorous Biochar additions to soil have been found to both increase and decrease the availability of soil P (Steiner et al, 2007; Nelson et al, 2011). After N, P tends to be the next major nutrient limiting primary production in most ecosystems, except in the tropics where it is often the primary limitation (subsequently limiting microbial N2 fixation). Unlike N, there is little evidence for the direct uptake of organic P by plants and therefore soil organic matter containing organic P polymers (e.g. phospholipids, DNA, phosphorylated proteins etc.) must be enzymatically broken down outside the cell prior to the uptake of inorganic P (Pi). Inorganic P is most commonly taken up by plants in the HPO4-2 or H2PO4- form. Some low molecular weight organic P can be directly taken up by microbial cells (e.g. adenosine phosphates), however, this pathway is probably small in comparison to the uptake of Pi. In contrast to N, however, the solubility and rate of diffusion of Pi in soils is typically extremely low due to strong sorption to the mineral phase (e.g. on Fe and Al oxyhydroxide surfaces) and its potential to form mineral precipitates (e.g. Ca-P). Although biochar itself can provide a readily available source of P, it may also directly and indirectly influence P behaviour in soil by a range of other mechanisms including: (i) shifts in soil pH; (ii) alteration in enzyme efficiencies; (iii) Biochar C15.indd 437 437 formation of organo-mineral complexes that increase P solubility; (iv) shifts in plant and microbial community structure. Release of P from biochar and impacts on P leaching Most biochars contain an appreciable amount of P and the release of P from biochar has long been recognized (Tryon, 1948). The P contained in biochar feedstocks typically ranges from 0.01–0.1 per cent for wood residues, 0.1–0.4 per cent for crop residues and 0.5–5 per cent for manures and biosolids (Barrelet et al, 2006; Liu et al, 2011; Wang et al, 2012). Within each feedstock, P can be contained in different chemical forms which may affect its subsequent availability after entering the soil. When plant residues are pyrolysed, organic C begins to volatilize at approximately 100°C; whereas, P does not volatilize until approximately 700°C (Knoepp et al, 2005). Combustion or charring of organic materials can greatly enhance P availability from plant tissue by disproportionately volatilizing C and by cleaving organic P bonds, resulting in a residue of soluble P salts associated with the charred material. Pyrolysis leads to the formation of a range of mineral P forms of which complexes with Fe, Al, Ca and Mg predominate. It is likely that biochars derived from biosolids (sewage sludge) will have a high proportion of Fe and Al phosphates which will be less soluble than Ca and Mg phosphates. Biochar therefore contains three pools of P, one which is freely soluble, one which is strongly bound to Fe and Al and one which remains organically bound as a residue of the original feedstock. The proportion of each is dependent on feedstock and pyrolysis conditions (covered in detail in Chapter 6) (Liu et al, 2011), however, a number of studies have shown that a large proportion of the P contained in woodderived biochars is immediately soluble and readily released into soil solution (e.g. 11/3/2014 9:04:30 AM 438 BIOCHAR FOR ENVIRONMENTAL MANAGEMENT Gundale and DeLuca, 2006). Experimental biochar addition rates of 10–50kg biochar ha-1 would result in the addition of 1 to 2500 kg P ha-1 depending on the feedstock of which approximately 5–20 per cent can be assumed to be available depending on feedstock (see Chapter 7). When considering that typical synthetic fertilizers are added at 5 to 50kg P ha-1 there is considerable potential for overapplication with some biochars. However, there has been little evidence for increased leaching of P in laboratory trials (Laird et al, 2010; Borchard et al, 2012a; Schultz and Glaser, 2012). Quilliam et al (2012) described a significant increase in available soil P (0.5M acetic acid extraction) with reapplication of wood biochar (25 and 50Mg biochar ha-1) on top of an existing biochar application of 25 and 50Mg biochar ha-1 (resulting in a 0, 25, 50, 25+25 and 50+50Mg biochar ha-1 experiment) in an agricultural Inceptisol. However, this noted increase in P availability did not translate to an increase in foliar P concentrations in the test crop (Quilliam et al, 2012). Effect of biochar on phosphatase enzymes and P solubilizing bacteria Biochar can induce significant shifts in the size, structure and activity of the soil microbial community (Lehmann et al, 2011). Despite the significant amount of functional redundancy in the microbial population, this may cause changes in rates of P cycling. Biochar has been observed to influence mycorrhizal colonization of plant roots which in turn may alter soil P uptake (Warnock et al, 2007; Lehmann et al, 2011); however, this topic is covered in detail in Chapter 13. Short-term laboratory studies have shown that biochar addition induces an increase in phosphatase activity (Bailey et al, 2010; Yoo and Kang, 2010; Jindo et al, 2012) which would increase the release of P from soil organic matter and organic residues. Other studies, however, have revealed only Biochar C15.indd 438 minor influence on soil phosphatase (Jones et al, 2010). Molecular analyses of soils amended with biochar revealed increased presence of bacteria genes for genera of bacteria that have been observed to produce P solubilizing compounds (Hamdali et al, 2008; Anderson et al, 2012); however, this is indirect evidence for biochar induced enhancement of P solubilizing bacteria and further studies are needed to determine if there is any direct influence on bacterial production of P solubilizing compounds. In addition to directly releasing soluble P, biochar can have a high CEC (Liang et al, 2006). Sorbed Al, Fe or Ca may influence P solubility (see page 439 and Chapter 9). It has been demonstrated that fresh biochar has an abundance of transient anion exchange capacity in the acid pH range (Cheng et al, 2008), which can be in excess of the total CEC of the biochar. These exchange sites have the potential to compete with Al and Fe oxides (e.g. gibbsite and goethite) for sorption of soluble P, similar to that observed for humic and fulvic acid extracts (Sibanda and Young, 1986; Hunt et al, 2007). To date, there is a noted lack of studies evaluating the effect of biochar and variable charge surfaces (short-term anion exchange capacity) on P cycling and availability. As biochar ages, the positive exchange sites on biochar surfaces decline and negative charge sites develop (Cheng et al, 2008). The biochemical basis for the high CEC is not fully understood (see Chapters 5, 6 and 9), but is likely due to the presence of oxidized functional groups (such as carboxyl groups), whose presence is indicated by high surface O/C ratios that form on the surface of charred materials following microbial degradation (Liang et al, 2006; Cheng et al, 2008; Preston and Schmidt, 2006). Phosphorus availability and recycling may be influenced by the biochar CEC over long time scales and in soils that have inherently low exchange capacities. 11/3/2014 9:04:30 AM BIOCHAR EFFECTS ON SOIL NUTRIENT TRANSFORMATIONS By reducing the presence of free Al+3 and Fe+3 near root surfaces, biochar may promote the formation and recycling of labile P fractions. This is also an area of research that deserves greater attention. Complexation A significant component of the P cycle consists of a series of precipitation reactions that influence the solubility of P, ultimately influencing the quantity of P that is available for uptake and actively recycled between plants and microbes. The degree to which these precipitation reactions occur is strongly influenced by soil pH, due to the pH dependent activities of the ions responsible for precipitation (Al3+, Fe3+ and Ca2+) (Stevenson and Cole, 1999). In alkaline soils, P solubility is primarily regulated by its interaction with Ca2+, where a cascading apatite mineral pathway develops. In acid soils, P availability is primarily regulated by its interaction with Al3+ and Fe3+ ions, where highly insoluble Al- and Fe- phosphates form. Biochar may influence precipitation of P into these insoluble pools by altering the pH and thus the strength of ionic P interactions with Al3+, Fe3+ and Ca2+ (Lehmann et al, 2003; Topoliantz et al, 2005) or by sorbing organic molecules that act as chelates of metal ions that otherwise precipitate P (DeLuca, unpublished data, Figure 15.4). The latter pathway may be of particular importance for plant P availability if biochar enhances formation of stabilized organic matter from decomposing organic matter as suggested by some composting studies involving biochar (Dias et al, 2010) (see also Chapter 25), or by altered SOC turnover patterns in Terra Preta (Liang et al, 2010). Numerous studies have demonstrated that biochar can modify soil pH, normally by increasing pH in acidic soils (Mbagwu, 1989; Matsubara et al, 2002; Lehmann et al, 2003). There are few, if any, studies that have demonstrated a reduction in pH with biochar Biochar C15.indd 439 439 addition in alkaline soils, however, the addition of acid biochar to acidic soils has been observed to reduce soil pH (Cheng et al, 2006). An increase in pH associated with adding biochar to acid soils are due to an increased concentration of alkaline metal (Ca2+, Mg2+ and K+) oxides in the biochar and a reduced concentration of soluble soil Al3+ (Steiner et al, 2007). Adding these alkaline metals, both as soluble salts and associated with biochar exchange sites, is likely the single most significant effect of biochar on P solubility in the short term, particularly in acidic soils where subtle changes in pH can result in substantially reduced P precipitation with Al3+ and Fe3+. In contrast, adding biochar (and associated ash residue) to neutral or alkaline soils may have a limited effect on P availability because adding alkaline metals would only exacerbate Ca driven P limitations. In addition to its effect on soil pH, biochar may also influence the bioavailability of P through several other mechanisms associated with P precipitation, such as biocharinduced surface sorption of chelating organic molecules. Biochar is an exceptionally good surface for sorbing polar or non-polar organic molecules across a wide range of molecular mass (Sudhakar and Dikshit, 1999; Schmidt and Noack, 2000; Preston and Schmidt, 2006; Bornermann et al, 2007). Organic molecules involved in chelation of Al3+, Fe3+ and Ca2+ ions will potentially be sorbed to hydrophobic or charged biochar surfaces so that, in the long run, organo-biochar or organo-mineral-biochar complexes begin to form over time that may aid in the retention and exchange of soluble P around aged biochar particles (Briones, 2012; Joseph et al, 2013). However, in the short term, decreased P solubility may result via the following mechanisms. Examples of such chelates include simple organic acids, phenolic acids, amino acids and complex proteins or carbohydrates 11/3/2014 9:04:30 AM 440 BIOCHAR FOR ENVIRONMENTAL MANAGEMENT (Stevenson and Cole, 1999). The sorption of chelates may have a positive or negative influence on P solubility. A clear example of this type of interaction is provided in Figure 15.5. Here, two compounds that have been reported as possible allelopathic compounds released as root exudates from Centaurea species: catechin and 8-hydroxy-quinoline (Vivanco et al, 2004; Callaway and Vivanco, 2007) have also been reported to function as potent metal chelates (Stevenson and Cole, 1999; Shen et al, 2001) that may indirectly increase P solubility. Catechin effectively increased P solubility in an alkaline (pH 8.0) calcareous soil and the 8-hydroxy-quinoline increased P solubility when added to an acidic (pH 5.0) Al-rich soil (Figure 15.5). The addition of biochar to these soils eliminated the presence of soluble chelate in the soil system and in turn eliminated the effect of the chelate on P solubility. This interaction may explain the observed reduction in P sorption by ionic resins with increasing biochar application rates in the presence of actively growing Koleria macrantha (Gundale and DeLuca, 2007). Such indirect effects of biochar on P solubility would vary with soil type and vegetative cover and underscores the complexity of plant-soil interactions. Sulfur To date, there have been few studies that have focused on the influence of biochar soil amendments on soil S transformations. Sulfur plays an extremely important role in the biochemistry of soils and the physiology of plants (Stevenson and Cole, 1999; Marschner, 2006). Sulfur is a component of two amino acids (cysteine and methionine), is required in protein synthesis and is a fundamental component of energy transformations in all living organisms. Sulfur also represents a source of energy for autotrophic organisms and an alternative electron acceptor for oxi- Biochar C15.indd 440 dative decomposition under anaerobic conditions (Stevenson and Cole, 1999). Although biochar produced from high S feedstocks has the potential to release S into the soil solution (Uchimiya et al, 2010), there is little evidence for enhanced oxidation or reduction of soil S with biochar applications. Given the similarities between the S and N cycles (Stevenson and Cole, 1999), there is certainly the potential for biochar to influence S mineralization and oxidation activity in the soil. Although the majority of soil S originates from the geologic parent material, most soil S exists in an organic state and must be mineralized (converted from organic S to SO4-2) prior to plant uptake (Stevenson and Cole, 1999). Organic S exists as either ester sulfate or as carbonbonded S, the latter having to be oxidized to SO4-2 prior to plant uptake. To date, no studies have directly assessed the influence of biochar on transformations of organic S already in agricultural or forest soils (separately from S release from the biochar discussed below). However, numerous studies involving biochar or biochar additions to soils have recorded changes in the soil environment that suggest that biochar additions could change the turnover of soil organic S. One of the few studies that have directly investigated the influence of biochar on S availability was conducted with two soil types, four crop residue amendments and performed in the laboratory in PVC columns (Churka Blum et al, 2013). In this study, S, C and N mineralization was assessed following addition of corn husk biochar to soil compared with fresh residues of corn husks, pea and rape residues. Although C mineralization and N mineralization were notably low with the biochar amendment, the highest rate of S mineralization for all amendments was observed with the corn husk biochar. The authors conclude that the release of S from the residues is likely a function of the S compounds within the residues. The high concentrations of ester S and 11/3/2014 9:04:30 AM BIOCHAR EFFECTS ON SOIL NUTRIENT TRANSFORMATIONS 441 Figure 15.5 Soluble P leached from columns filled with (a) calcareous soil (pH = 8) amended with catechin alone or with biochar or (b) acid Al rich soil (pH = 6) amended with 8-hydroxy quinoline alone or with biochar (DeLuca, unpublished data). Studies were conducted by placing 30g of soil amended with 50mg P kg-1 soil as rock phosphate into replicated 50mL leaching tubes (n = 3). Soils were then treated with nothing (control), chelate, or chelate plus biochar (1% w/w), allowed to incubate for 16 h moist and then leached with 3 successive rinsings of 0.01M CaCl2. Leachates were then analysed for orthophosphate on a segmented flow Auto Analyzer III. Data were subject to ANOVA by using SPSS Biochar C15.indd 441 11/3/2014 9:04:30 AM 442 BIOCHAR FOR ENVIRONMENTAL MANAGEMENT soluble SO4-2 in the biochar amendment combined with the modest increase in biotic activity with the biochar amendment suggests that soluble SO3-2 and SO4-2 readily liberated from the ester S allowed for rapid accumulation of inorganic S in soils treated with biochar (Churka Blum et al, 2013). Biochar additions to acid agricultural soils have been observed to yield a net increase in soil pH (see Chapter 7), potentially as a function of the alkaline oxides applied along with the biochar or potentially as a result of the influence on free Al:Ca ratios in soils amended with biochar (Glaser et al, 2002; Topoliantz et al, 2005). Sulfur mineralization is favoured at slightly acid to neutral pH. Sulfur mineralization rates have been found to increase following fire in pine forest ecosystems (Binkley et al, 1992), much the same as that observed for N (Smithwick et al, 2005). Separating the effect of fire from the effect of the natural addition of char is difficult, but this effect is most likely due to the release of soluble S from litter following partial combustion during fire or heating events at temperatures in excess of 200ºC (Gray and Dighton, 2006). Sulfur oxidation is carried out by both autotrophic (e.g. Thiobacillus spp.) and heterotrophic organisms. Sulfur oxidation by acidophilic Thiobacillus spp. would not be favoured by pH increases induced by the presence of biochar. However, these autotrophic organisms have uniquely high requirements for certain trace elements that are in relatively high concentrations in biochar (see Chapter 13) and are increased in soil when biochar is added (Rondon et al, 2007). Biochar additions to soil that ultimately reduce the surface albedo of mineral soils and result in faster warming of soils in springtime (Meyer et al, 2012) may in turn increase S oxidation or mineralization rates (Stevenson and Cole, 1999). Biochar C15.indd 442 The utility of biochar, activated carbon and graphite in the high temperature, chemical reduction of SO2 to C adsorbed episulfide has been studied intensely (Humeres et al, 2005) to evaluate these materials as scrubbers for removing SO2 from pollution streams. This has limited relevance for soils, except that the very salts demonstrated to enhance catalytic reduction of SO2 in the presence of activated carbon (e.g. Na+ and NO3-) are often present in soils in relatively high concentrations. However, there are no published reports of enhanced SO4-2 reduction in soils in the presence of biochar. Biochar additions to mineral soils may also directly or indirectly affect S sorption reactions and S reduction. However, as with NO3-, non-aged, production-fresh biochar may lack any significant capacity to adsorb SO4-2 (Borchard et al, 2012b). As noted in Chapter 5, biochar improves soil physical properties through increased specific surface area, increased water holding capacity and improved surface drainage. Increased soil aeration through these improvements in soil physical condition would in turn reduce the potential for dissimilatory S reduction (Stevenson and Cole, 1999). Sulfur is readily adsorbed to mineral surfaces in the soil environment and particularly to exposed Fe and Al oxides. Once Fe and Al have been sorbed to biochar surfaces, SO4-2 may interact with the exposed metal oxides. Conversely, organic matter additions to soil have been shown to reduce the extent of SO4-2 sorption in acid forest soils (Johnson, 1984), therefore biochar amendments could act to increase solution concentrations of S in acidic iron-rich soils. The lack of studies devoted to the evaluation of S transformations following biochar addition to soils calls for additional research in this area. 11/3/2014 9:04:30 AM BIOCHAR EFFECTS ON SOIL NUTRIENT TRANSFORMATIONS 443 Future research directions The application of biochar to agricultural soils has the potential to greatly improve soil physical, chemical and biological conditions. In this chapter we reviewed biochar as a modifier of soil nutrient transformations and discussed the known and potential mechanisms that drive these modifications. Biochar additions to soils may directly or indirectly alter nutrient cycling. Biochar applications may increase NH4+ retention in soil and have often been observed to increase N uptake by crop plants; however, there is little evidence for an increase in N availability following crop harvest. It is important to note that biochar has few negative impacts on soil nutrient cycling. The observed increases in net nitrification in forest soils occur at a level that would have minimal influence on net N leaching and N2O emissions. Although biochar additions could increase net ammonification observations have not been consistent. While P solubility appears to generally increase with biochar additions, this may be primarily a result of direct P addition with the applied biochar than altered P cycling. There is a distinct need for studies directed at explaining mechanisms for increased P uptake with biochar additions to agricultural soils. It is possible that biochar additions to soils stimulate mycorrhizal colonization, which may increase P uptake, but when applied with P-rich materials, this effect may be lost. There is a great need for additional studies that elucidate the effect of biochar on soil nutrient transformations, in the short term directly after application as well as in the long term, e.g. in aged PyC-rich soils. 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