Positive and negative carbon mineralization priming effects among a variety of biochar-amended soils

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Abstract

Pyrogenic carbon (biochar) amendment is increasingly discussed as a method to increase soil fertility while sequestering atmospheric carbon (C). However, both increased and decreased C mineralization has been observed following biochar additions to soils. In an effort to better understand the interaction of pyrogenic C and soil organic matter (OM), a range of Florida soils were incubated with a range of laboratory-produced biochars and CO2 evolution was measured over more than one year. More C was released from biochar-amended than from non-amended soils and cumulative mineralized C generally increased with decreasing biomass combustion temperature and from hardwood to grass biochars, similar to the pattern of biochar lability previously determined from separate incubations of biochar alone.

The interactive effects of biochar addition to soil on CO2 evolution (priming) were evaluated by comparing the additive CO2 release expected from separate incubations of soil and biochar with that actually measured from corresponding biochar and soil mixtures. Priming direction (positive or negative for C mineralization stimulation or suppression, respectively) and magnitude varied with soil and biochar type, ranging from −52 to 89% at the end of 1 year. In general, C mineralization was greater than expected (positive priming) for soils combined with biochars produced at low temperatures (250 and 400 °C) and from grasses, particularly during the early incubation stage (first 90 d) and in soils of lower organic C content. It contrast, C mineralization was generally less than expected (negative priming) for soils combined with biochars produced at high temperatures (525 and 650 °C) and from hard woods, particularly during the later incubation stage (250–500 d). Measurements of the stable isotopic signature of respired CO2 indicated that, for grass biochars at least, it was predominantly pyrogenic C mineralization that was stimulated during early incubation and soil C mineralization that was suppressed during later incubation stages. It is hypothesized that the presence of soil OM stimulated the co-mineralization of the more labile components of biochar over the short term. The data strongly suggests, however, that over the long term, biochar–soil interaction will enhance soil C storage via the processes of OM sorption to biochar and physical protection.

Highlights

► For all soils, C mineralization rate increased after biochar amendment, but decreased after a few months. ► During early incubation, soil generally stimulated the release of biochar-C, likely due to co-metabolism. ► During later incubation, biochar generally suppressed the release of soil C, likely due to sorptive protection.

Introduction

Pyrogenic organic matter, or black carbon (BC), the solid residuals of biomass combustion, has recently been recognized to represent a significant portion of sediment and soil organic carbon (SOC), ranging up to 40% but more typically about 10% of SOC (Masiello, 2004). Because of its highly condensed nature and resistance to chemical treatment, BC has generally been regarded as biologically and chemically recalcitrant (e.g. Seiler and Crutzen, 1980, Kuhlbusch, 1998, Skjemstad et al., 2002). While BC is often found to be among the oldest pool or organic matter in soils, with 14C ages ranging to 103 y (Schmidt et al., 2002), some studies have shown BC to be at least partially biotically and chemically reactive (Shneour, 1966, Baldock and Smernik, 2002, Hilscher et al., 2009, Kuzyakov et al., 2009, Zimmerman, 2010). The chemical or ‘combustion’ continuum of black carbon materials, in order of increasing charring temperature from slightly charred biomass to charcoal to soot (Masiello, 2004), likely corresponds to a lability continuum, with BC produced at lower temperatures (<500 °C) and from grasses degrading with shorter C half lives (102–104 y) than those produced at higher temperatures (>500 °C) and from hard woods (105–107 y) (Zimmerman, 2010).

The effect that BC may have on overall carbon cycling when added to a soil or sediment is controversial and not without important and immediate consequences. First, given the expected increase in fire frequency likely to occur with future climate change (IPCC, 2007), an understanding of the effects of BC addition on non-BC soil organic matter (OM) will be needed to model past and future changes in global carbon cycling or climate feedbacks. Second, stimulated by the observation that small plots of anthropogenic Amazon soil, called terra preta, are both extremely enriched in BC and highly fertile, there has been growing call to produce BC from organic wastes which can then be added to soils to enhance fertility and mitigate climate change by sequestering CO2 from the atmosphere (e.g. Glaser et al., 2001, Lehmann et al., 2006). When BC is added to soils (then called biochar), it may be an ecosystem C source or sink, depending upon the nature of the interactions between BC, microbes, and non-BC OM.

‘Priming effects’, changes in the mineralization of native soil OM due to the addition of new substrates, have been observed in many types of laboratory and field studies and recently reviewed by Kuzyakov et al. (2000). Most commonly, it is ‘positive priming’ that is observed, i.e. the accelerated mineralization of a more refractory soil OM components when stimulated by the addition of a labile C source, but results are not always straightforward. For example, soil OM decomposition increased 3- to 5-fold or decreased by up to 30% in the presence of plant residues (Bell et al., 2003, Nottingham et al., 2009) or root exudates (Kuzyakov, 2002, Cheng, 2009). Cellulose additions resulted in a 100% increase in the mineralization of even 2500 y old OM from deep soils layers (Fontaine et al., 2007). Positive priming may be a direct effect of increased production of extracellular enzymes due to the added substrate which ‘co-metabolize’ soil OM, but indirect mechanisms are also possible, such as the stimulation of microbial activity through nitrogen or other nutrient additions or improvement in soils aeration, moisture or structure (Kuzyakov et al., 2000). On the other hand, ‘negative priming’, defined here (and by Kuzyakov et al., 2000) as any retardation in soil OM mineralization due to any treatment such as the addition of a new substrate, may occur due to the divergence of microbes or their enzymes to the more easily available substrate, or to the inhibition of microbial activity because of some change in the soil environment. Mineral adsorptive protection, often discussed as a soil OM preservation mechanism (e.g. Sollins et al., 1996), could be a form of negative priming if the added substrate contains a sorptive component.

Given its porous nature and high affinity for natural organic matter (Kasozi et al., 2010), it could be hypothesized that BC will sequester non-BC soil OM within its pore network, protecting it from degradation both by microbially-produced enzymes and abiotic oxidants. For example, charred biomass of different types had been shown to sorb a number hydrophobic agrochemicals, resulting in their decreased dissipation (Yang and Sheng, 2003, Cao et al., 2009, Spokas et al., 2009). More hydrophilic natural soil OM components have also been shown to sorb to BC, though to lesser extents, depending upon its charring temperature and the molecular size of the sorbate (Kasozi et al., 2010). Other signs of decreased microbial activity have been observed with addition of certain BC types, such as decreased N2O production and CH4 oxidation (Spokas and Reicosky, 2009) and production of the microbial inhibitor, ethylene (Spokas et al., 2010). Alternatively, BC may have a stimulatory effect on soil carbon mineralization. This positive priming could occur if BC acts as a mineralizable C source, and BC amendments may also provide nitrogen, phosphorous and micronutrients (Chan and Xu, 2009) or even a habitat favoring increased microbial heterotrophic activity (Thies and Rillig, 2009).

Positive priming effects on SOC degradation, as well as more labile amended substrates, have also been recorded in the presence of biochar. Wardle et al. (2008) observed greater mass loss from a litterbag containing a mixture of humus and charcoal than would be expected based on mass loss from separate litterbags of humus and charcoal. However, without the presence of soil minerals, the applicability of this finding has been questioned (Lehmann and Sohi, 2008). In another study, Steinbeiss et al. (2009) found an increase in respired CO2 following addition of glucose-derived biochar to one of two soils tested, but no change to either when using a different biochar type. However, this change was only short term (several weeks) and the possibility of CO2 degassing by the biochar alone was not examined. The presence of biochar in soils also enhanced the degradation of more labile C sources such as ryegrass residue (Hilscher et al., 2009) and switchgrass residue (Novak et al., 2010). On the other hand, the addition of glucose had a strong stimulatory effect on the oxidation of BC both in carbon-free sand (Hamer et al., 2004) and in soil (Kuzyakov et al., 2009).

In contrast to these finding, other studies have found no influence, or even a negative priming influence, of BC on OM degradation. For example, in three separate studies, after correcting for the CO2 produced by biochar alone, there was no change in respired CO2 in a biochar-amended versus biochar-absent loamy-sand (South Carolina, USA, Novak et al., 2010), a silty-loam (Minnesota, USA, Spokas et al., 2009) and a German loam and loess (Kuzyakov et al., 2009). Adding to the perplexity, Hilscher et al. (2009) recorded no increase in respired CO2 when a Swiss loam was amended with pine wood-derived biochar but enhanced respiration with added grass-derived biochar. And in another study using sixteen chars and two soil types, about a third increased, a third decreased, and a third had no effect on SOC respiration (Spokas and Reicosky, 2009).

Further supporting the contention that BC amendments will enhance SOC preservation rather than encourage its degradation, terra preta soil are not only enriched in BC, but have also been found to contain greater non-BC amounts of natural OM compared to surrounding native tropical soils which are typically depleted in SOC (Glaser, 2007, Solomon et al., 2007). In addition, terra preta and other BC-containing soils such as those near historical charcoal blast furnace sites exhibit lower soil C respiration rates in incubations than adjacent soils with lower amounts of BC (Cheng et al., 2008b, Liang et al., 2008). Finally, another incubation study of terra preta soils found that, not only was 2–3 times less C mineralized in BC-rich versus adjacent BC-poor soils, but there was about 25% less C mineralized from an added labile carbon source (sugar cane leaves) in the former compared to the latter (Liang et al., 2010).

Clearly, a great deal of confusion exists as to the short and long-term effects that biochar amendment will have on soil C cycling and sequestration. Some of the discrepancy between studies that find a positive versus negative priming effect may lie in the materials used, including soil, biochar or priming substrate type, while others may have to do with the method by which the experiment was conducted, including water saturation, atmosphere, or timeframe over which the experiment was carried out. This study was intended to shed light on the interaction mechanisms between soil and biochar that may lead to variability in priming effects and natural variation in C mineralization by comparing C respiration rates among a variety of well-characterized biochars mixed with a range of soil types under constant laboratory incubation conditions. Modeling of the results and that expected from C mineralization by the soil and biochar alone was carried out to better illustrate the trends in soil–biochar priming that occurred during the experiment and to project them into the future.

Section snippets

Materials and methods

Five soil types were mixed and incubated with biochar produced from five biomass types under four combustion conditions. In addition, each of the soils and each of the biochar types were incubated separately to serve as controls. Carbon degradation was measured periodically as CO2 evolution over the course of 505 days.

Carbon mineralization

Results and discussion of biochar-alone oxidation rate measurement and modeling have been published previously (Zimmerman, 2010). Briefly, biochar-C losses of 3–30 mg C g-biochar−1 y−1 (1.4% on average) were recorded over a year. Abiotic biochar-C release rates were about 50–90% of those found to occur when amended with soil microbes. Biochars made at lower temperatures were found to degrade at faster rates than higher temperature chars, and biochar made from grasses generally degraded faster

Discussion

There are a number of caveats that must be made when interpreting the data. First, the biochar inoculum from a forest soil may have had a different microbial population than the native population in each of the different soils. However, microbial activity in different soil types is often compared, though the microbes present may differ, and it is simply assumed that enough microbial diversity is present so that so that resources will be used to the fullest extent. Second, though each incubation

Conclusion

These experiments suggest possible mechanisms that may explain the seemingly contradictory results of previous works, showing biochar to have a positive priming effect in some cases and a negative one in others. That is, the biochar type, the soil type, and the period over which measurements are made, can strongly influence the direction and magnitude of priming effect recorded. While both positive and negative priming effects were observed in these incubations of biochar and soil, it is

Acknowledgments

We thank Dr. Nick B. Comerford (University of Florida, Soil and Water Science Department) for providing the soils used in this study as well as the acid hydrolysis data, Dr. Herman B. Zimmerman for assistance preparing the incubations and Dr. Jason Curtis (University of Florida, Department of Geological Sciences) for performing stable isotopic analyses. This work was supported by the NSF-Geobiology and Low Temperature Geochemistry Program (EAR#0819706).

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