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GCB Bioenergy (2013) 5, 202–214, doi: 10.1111/gcbb.12037

Biochar and its effects on plant productivity and nutrient cycling: a meta-analysis L O R I A . B I E D E R M A N and W . S T A N L E Y H A R P O L E Department of Ecology, Evolution, and Organismal Biology, Iowa State University, 251 Bessey Hall, Ames, IA, 50011, USA

Abstract Biochar is a carbon-rich coproduct resulting from pyrolyzing biomass. When applied to the soil it resists decomposition, effectively sequestering the applied carbon and mitigating anthropogenic CO2 emissions. Other promoted benefits of biochar application to soil include increased plant productivity and reduced nutrient leaching. However, the effects of biochar are variable and it remains unclear if recent enthusiasm can be justified. We evaluate ecosystem responses to biochar application with a meta-analysis of 371 independent studies culled from 114 published manuscripts. We find that despite variability introduced by soil and climate, the addition of biochar to soils resulted, on average, in increased aboveground productivity, crop yield, soil microbial biomass, rhizobia nodulation, plant K tissue concentration, soil phosphorus (P), soil potassium (K), total soil nitrogen (N), and total soil carbon (C) compared with control conditions. Soil pH also tended to increase, becoming less acidic, following the addition of biochar. Variables that showed no significant mean response to biochar included belowground productivity, the ratio of aboveground : belowground biomass, mycorrhizal colonization of roots, plant tissue N, and soil P concentration, and soil inorganic N. Additional analyses found no detectable relationship between the amount of biochar added and aboveground productivity. Our results provide the first quantitative review of the effects of biochar on multiple ecosystem functions and the central tendencies suggest that biochar holds promise in being a win-win-win solution to energy, carbon storage, and ecosystem function. However, biochar’s impacts on a fourth component, the downstream nontarget environments, remain unknown and present a critical research gap. Keywords: carbon sequestration, charcoal, pH, plant productivity, soil nutrients, soil organisms

Received 7 September 2012 and accepted 11 October 2012

Introduction Atmospheric CO2 concentration is nearly 400 ppm and continues to rise due to human activities, with consequences to global climate, human health (Lafferty, 2009; Anderson et al., 2012), agriculture (Auffhammer et al., 2012), and biodiversity (Bakkenes et al., 2002; Bellard et al., 2012). Among the many proposed solutions to mitigate this increase in atmospheric carbon is to enhance long-term sequestration of carbon through the application of biochar to the soil (Marris, 2006; Lehmann, 2007b). Biochar is a carbon-rich coproduct resulting from pyrolyzing biomass under high-temperature, low oxygen conditions for biofuel production (Lehmann, 2007a; Laird et al., 2009) and although it is similar to other charcoals, biochar is defined by its intentional application to the soil for environmental applications (Lehmann & Joseph, 2009). It contains highly condensed aromatic structures that resist decomposition in soil and thus can effectively sequester a portion of the applied carbon for Correspondence: Lori A. Biederman, tel. 515-509-6346, fax (515)-204-1337, e-mail: [email protected]

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decades to centuries (Lehmann et al., 2006; Novak et al., 2010; although see Wardle et al., 2008). One analysis estimates that widespread use of biochar could mitigate up to 12% of current anthropogenic CO2 emissions (Woolf et al., 2010). In addition to biochar’s potential to sequester recently fixed atmospheric carbon, its porous structure, high surface area, and affinity for charged particles (Keech et al., 2005) interact with physical and biological components of the soil (Glaser et al., 2002; Steiner et al., 2008a) and can have cascading effects throughout the ecosystem (Hammes & Schmidt, 2009). Recent reviews have highlighted the benefits of adding biochar to agricultural soils (Glaser et al., 2002; Marris, 2006; Lehmann, 2007b; Warnock et al., 2007). These benefits include the promotion of plant growth (Chan et al., 2008; Asai et al., 2009; Major et al., 2009; Graber et al., 2010; Hossain et al., 2010), the improvement of soil water-holding capacity (Laird et al., 2010b), diminishing disease incidence in crops (Matsubara et al., 2002; Elad et al., 2010; Elmer & Pignatello, 2011), limiting the bioavailability of heavy metals (Park et al., 2011), reducing soil N2O emission (Kammann et al., 2011; Taghizadeh-Toosi et al., 2011), © 2012 Blackwell Publishing Ltd

B I O C H A R A N D E C O S Y S T E M S : A M E T A - A N A L Y S I S 203 and reducing of nutrient leaching loss, which in turn can reduce fertilizer needs (Liang et al., 2006; Laird et al., 2010a). Because biochar is a coproduct of bioenergy production and can contribute to carbon sequestration goals, while also simultaneously increasing yield and reducing fertilizer use, biochar has been touted as a ‘win-win-win’ solution to meeting global environmental challenges (Laird, 2008). There is, however, considerable variation in plant and soil responses to biochar that cannot be evaluated in a single study and may be lost in the overall message of a literature review. Source material and pyrolysis conditions introduce significant variation in the structure, nutrient content, pH, and phenolic content of the biochar products (Novak et al., 2009a). Interactions with climate, soil type (texture, chemistry, hydrology) (Tryon, 1948; van Zwieten et al., 2010a), and fertilization status (van Zwieten et al., 2010b; Haefele et al., 2011) can also contribute to uncertainty in how biochar interacts with organisms. There are also many concerns about the production of biochar and the release of this novel material into the environment. In addition to apprehensions about food prices and potential land-use changes due to its manufacture and transport (Hill et al., 2006; Stoms et al., 2012), it remains unclear if there will be negative externalities associated with the widespread application of biochar. Specifically, there has been limited research on the impacts to nonagricultural species, such as soil organisms and perennial plants that inhabit field margins or other nontarget ecosystems, especially aquatic systems. Effective implementation of biochar as a climate-mitigating tool would require the application of vast quantities of biochar into the environment; exposure of nontarget terrestrial and aquatic systems to biochar is likely as wind and water can translocate up to 53% of applied biochar material during application (Major et al., 2009) and biochar materials preferentially erode from the soil (Rumpel et al., 2006). Because many reports on the benefits of biochar draw on the results of relatively few studies, a quantitative understanding of its potential impacts to ecosystems is needed prior to its adoption as a major climate mitigation tool. We performed a comprehensive meta-analysis of published studies that tested the effects of biochar on one or more ecosystem functions including plant productivity, nutrient uptake, soil properties, and on ecosystem services, such as crop yield. Our primary question was to ask whether the central tendencies in the published empirical literature supported the often-enthusiastic claims of previous reports (Marris, 2006; Lehmann, 2007a; Kleiner, 2009). Furthermore, because the effects of biochar have been described as analogous to effects of fertilization, we compared the effect of biochar vs. © 2012 Blackwell Publishing Ltd, GCB Bioenergy, 5, 202–214

fertilizer and evaluated synergistic interactions (Glaser et al., 2002; Chan et al., 2008; Lau et al., 2008). The potential effects of accidental biochar exposure on nonagricultural species were assessed by comparing the responses of annual and perennial plant species and evaluating the effect of biochar on soil organisms. Finally, because biochar as a product can be chemically highly variable, we examined the ability of particular biochar characteristics arising from feedstock and production methodologies to influence plant growth to inform best use practices.

Materials and methods Literature search We conducted an exhaustive literature search in Web of Science (thomsonreuters.com) and Google Scholar (scholar.google. com) databases using the keywords ‘biochar’, ‘char’, ‘black carbon’, ‘charcoal’, and ‘agchar’ (most recent search, June 25, 2012). The literature cited sections of published literature reviews (e.g., Glaser et al., 2002; Atkinson et al., 2010; Spokas et al., 2011) were consulted for additional sources. For each identified article, we evaluated the title and abstract to determine if it contained original data and measured the responses of interest (plant growth, soil nutrients, and soil organisms). Those articles that met these criteria were examined in detail. Although biochar specifically refers to pyrolyzed biomass that is intentionally applied to the soil for environmental applications (Lehmann & Joseph, 2009), we included charcoal derived from hydrothermal carbonization (Rilling et al., 2010). We excluded studies that examined the response to wildfire deposition and historical charcoal applications, such as those found in ‘Terra Preta’ soils, because the exact nature and quantity of amendment material cannot be known. Those studies that included soil contaminants, tested alleopathic interference, averaged responses among different trials, or did not contain appropriate controls were also excluded. This process identified 114 published articles.

Data extraction Data from ecosystem variables that were measured in more than five studies were extracted from the identified articles, including plant production and nutrient content, soil organism composition, and nutrient availability. Data concerning gas fluxes and process rates were outside the scope of this analysis. Within each article, data were divided into ‘experiments’ based on differences in soil, biochar material, and/or plant species, resulting in 371 independent experiments (Supplemental table 1). Different application rates of biochar and supplemental nutrient addition (inorganic and organic) were considered variables within an experiment. During data extraction, we selected treatments and experimental conditions that were most representative of normal field conditions. For example, if soil organisms were manipulated within an experiment only data from nonsterilized soils were

204 L . A . B I E D E R M A N & W . S . H A R P O L E used. Other decision rules included extracting only the final data of repeated measurements and nutrient data from the uppermost soil layer. We also had to manipulate data presented to allow for comparisons. In 43% the experiments, the biochar application rate was presented as mass per area, these data were converted to percent volume, assuming a soil bulk density of 1.5 g cm 3 unless otherwise provided. pH values measured with CaCl2 were made comparable with pH measured with distilled water using the formula pHH2O = 1.65 + (0.86*pH-[CaCl2]) (Augusto et al., 2008). Productivity data from plants grown in a mixed-species community were summed. The ratio of aboveground-to-belowground tissue and total biomass were also calculated in those cases where both above- and belowground data were reported. We also obtained auxiliary information whenever possible, including experimental setting, study length, fertilizer type, soil nutrients and pH, biochar composition, feedstock source, pyrolysis conditions, and activation status. The target organisms’ functional group was noted and if it is plant, we recorded its life span. We used the natural log-transformed response ratio as a measure of effect size (Hedges et al., 1999; Lajeunesse & Forbes, 2003): RRX = ln (T/C), where T is the measured value of the response variable to treatment X [biochar (B), fertilizer (F), or both (BF)] and C is the value in the untreated soils – the control. For those studies where fertilizer was added to both the control and biochar treatments, the response ratio was modified RRX = ln (BF/F). We used RRBFC and RRBFF to distinguish between the true factorial conditions and those where all treatments receive fertilizer, respectively. With the exception of the analysis of biochar rate (described below), we calculated the mean response to material application prior to calculating RRX when studies included multiple biochar (n = 20) or fertilizer application rates. To ensure that our results were not affected by this decision, we calculated a response ratio using the maximum response and compared it with the mean response scenario and they were not significantly different. The effect of biochar application rate on aboveground productivity was calculated in a manner similar to RRB, but in this case the response to biochar was calculated for each reported biochar application rate, rather than averaged over all application amounts. The slope of each of the response surfaces was determined.

Analysis All statistical analyses and graphical presentation were performed in R 2.12.2 and the ggplot2 package (Wickham, 1999; R Development Core Team, 2011). Because the data distributions tended to be slightly skewed, we used nonparametric tests. To determine if biochar significantly affected ecosystem variables, we used Wilcoxon signed rank tests to compare the mean RRB with zero. We used paired Wilcoxon signed rank tests to compare the effect size of biochar with that of fertilizer (RRB vs. RRF). To determine if there was a superadditive effect of applying both biochar and fertilizer we used two tests to determine if: First, for factorial application studies we calculated a test statistic (θ) from the original data [θ = ln ((biochar/control) + (fertilizer/control))] that represents the potential additive effect of adding both materials. We compared θ with RRBFC, or the

observed effect of adding both biochar and fertilizer, using a one-sided Wilcoxon rank sum test. Second, for those cases where fertilizer was applied to both control and biochar conditions, we used a Wilcoxon signed rank test to determine if RRBFF was different from zero. We compared biochar’s effect on annual and perennial plants by comparing productivity responses (RRB) using Wilcoxon rank sum tests. Our ability to assess how site conditions interact with biochar was limited by the lack of consistent reporting of biochar chemistry and soil characteristics among studies and it was only possible to analyze those variables with more than 100 studies: aboveground productivity and pH. The mean RRB for biochars of different source materials were compared with ANOVA, and the effects of latitude, pyrolysis temperature, and C : N ratio were determined using regression. We used robust standard errors for regressions using pH to correct for heteroskedastity. Many literature reviews of biochar effects, such as Lehman et al. (2011), Atkinson et al. (2010), and Spokas et al. (2011), include activated charcoal within their broader definition of biochar. We compared the response ratios (RRB) of our biochar data with response ratios from studies that used activated charcoals (Ridenour & Callaway, 2001; Kulmatiski & Beard, 2006; Chan et al., 2008; Lau et al., 2008; Weißhuhn et al., 2009; Wurst et al., 2010; Hale et al., 2011; Hass et al., 2012; Rajkovich et al., 2012), and used Wilcoxon rank sum tests to determine if the responses of these two products are similar (Supplemental table 2). To evaluate the potential of bias introduced from unpublished data we estimated the hypothetical number of unreported zero effect studies needed to produce a nonsignificant overall effect (Rosenthal, 1979; Harpole et al., 2007). This ‘fail k )2 – 2.706]. safe’ number is calculated as X = (k/2.706) [k(Z Where k is the number of studies that measured the variable of  k is the mean of the normalized standard deviainterest, and Z tions of the k studies. We excluded studies that did not report the significance of their data. A conservative estimate of  = 1.645 can be used for studies with significant effects Z  = 0 for studies reporting nonsignificant (P < 0.05) and Z responses to biochar (Supplementary table 3).

Results The addition of biochar to soils resulted in increased aboveground productivity (P < 0.01), crop yield (P 0). Also, on average, soil pH increased, or became less acidic, with biochar addition (P < 0.001). Those variables that showed no significant mean effect of biochar included belowground productivity, aboveground : belowground biomass ratio, percent mycorrhizal colonization of roots, plant tissue N and P concentration, and soil inorganic N. The effect size of aboveground productivity did not change as biochar application rate increased (Fig. 2). © 2012 Blackwell Publishing Ltd, GCB Bioenergy, 5, 202–214

B I O C H A R A N D E C O S Y S T E M S : A M E T A - A N A L Y S I S 205

Aboveground

**

n = 67

Belowground

ns n = 28

Above:below ratio

ns n = 21

Yield

**

n = 30

SMB

**

n = 16

Rhizobia nodules

*

n=6

% mycorrhizae col.

ns n = 23

Tissue N conc.

ns n = 25

Tissue P conc.

ns n = 21

Tissue K conc.

*

n = 12

Soil inorganic N

ns n = 33

Soil P

*** n = 53

Soil K

*** n = 31 *** n = 146

pH

*** n = 39

Total N

*** n = 26

Total C –0.5

0.0

0.5

1.0

1.5

RRB Fig. 1 The relative effect size (mean  CI) of biochar treatments (RRB) on a range of ecosystem variables. Significance of Wilcoxon signed rank tests: *P < 0.05, **P < 0.01, ***P < 0.001.

However, the variation around the mean response at each application rate, as measured by standard error, increased with application rates greater than 0.5%. In the 20 studies that reported multiple biochar application rates the overall mean (CI) response slope was 0.002  0.181, indicating no clear relationship between productivity and biochar application rate. Of those 20 studies, 8 had negative slopes (< 0.02), meaning the addition of more biochar reduced productivity, 10 had positive slopes (>0.02) meaning increasing biochar application increased productivity, and 2 studies had flat slopes ( 0.02 to 0.02) suggesting no effect of increasing biochar application rate. The average effect size of fertilization was significantly greater than that of biochar addition for aboveground productivity (P < 0.01), yield (P < 0.05), and soil P (P < 0.01) when compared with control conditions (Table 1 and Fig. 1). Biochar addition, however, was more effective than fertilization at increasing plant tissue P (P < 0.05) and K (P < 0.05) concentration. For all variables except soil total C (P < 0.001), the addition of both biochar and fertilizer (RRBFC) was not significantly © 2012 Blackwell Publishing Ltd, GCB Bioenergy, 5, 202–214

different than the additive expectation ( ). In those studies where fertilizer was added to all treatments (RRBFF), aboveground productivity (P < 0.01), crop yield (P < 0.001), plant tissue K concentration (P < 0.01), pH (P < 0.005), and soil total C (P < 0.01) increased significantly with biochar. Belowground biomass in perennial plants did not change in biochar treatments, which was significantly (P < 0.01) different than the belowground response by annual plants (Fig. 3). This difference contributed to a significantly smaller total productivity for perennial plants in biochar-treated soils (P < 0.001). Perennial and annual plants did not differ in aboveground productivity and the ratio of aboveground : belowground tissue in response to biochar. Aboveground productivity RRB varied significantly with latitude (adj. R2 = 0.095, P < 0.01); the effect size of biochar was more positive in the tropical regions than in temperate zones (Fig. 4). There was also a significant effect (P < 0.01) of feedstock source of the biochar material on aboveground productivity: grass- and manureorigin biochars increased productivity compared with control conditions (Fig. 5a) and forb-origin biochar reduced productivity, although there were limited data for this class of biochar. The C : N ratio of the biochar source had no predictable effect on productivity (adj. R2 = 0, P = 0.96) (Fig. 5b). Higher pyrolysis temperature biochars produced greater effects (adj. R2 = 0.076, P < 0.05) (Fig. 5c) and the pH of the biochar product significantly influenced aboveground productivity (adj. R2 = 0.172, P < 0.01), with alkaline biochars having a more pronounced positive effect than acidic biochars (Fig. 5d). The change in soil pH following the application of biochar is a function of both the initial soil pH (adj. R2 = 0.069, P < 0.01) and the pH of the biochar (adj. R2 = 0.139, P < 0.001). Acidic soils showed a greater positive response to biochar than alkaline soils. The effect of biochar on soil pH was greater for alkaline biochars. Both biochar and activated charcoal affected the ecosystem variables similarly. The average length of the studies analyzed was 113.4 days and the longest study was 3 years. For most variables, the number of hypothetical studies necessary to overturn the results of the meta-analysis was sufficiently large that our results are unlikely to be biased by unreported null responses (Supplemental table 3). For example, at least 1172 unreported nullresponse studies would be needed to cause the overall mean effect of biochar on aboveground productivity to be nonsignificant. For SMB, rhizobia nodules, and tissue nutrient concentration, however, the number of hypothetical unreported nonsignificant studies that would cause an overall nonsignificant mean effect would be less than 25.

2

Standard error

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RRB aboveground

1

0

1

2 0.02%

4

0.14%

2

1%

7.4%

54.6%

0

2

4

biochar application rate, ln Fig. 2 The relative effect size (mean  CI) of biochar treatments (RRB) for aboveground productivity at different log-transformed biochar application rates (equivalent percent application rates on the inside of x axis). Colors represent different experiments. Experiments with multiple application rates (n = 20) are connected with solid lines. Inset: the standard errors for the mean rates for studies with multiple application rates.

Discussion In our meta-analysis of 371 independent experiments we find that despite variability introduced by soil type, climate, and production methods, the average effect of biochar on various ecosystem properties was neutral to positive. This is consistent with previous reviews reporting the beneficial aspects of this product (Lehmann et al., 2006; Atkinson et al., 2010). Most importantly for agricultural systems, aboveground production and yield were increased in biochar-treated soils. Biochar has been shown to promote plant productivity and yield though several mechanisms. Physical conditions change with biochar; its dark color alters thermal dynamics and facilitates rapid germination, allowing more time for growth compared with controls (Genesio et al., 2012). Biochar can also improve soil water-holding capacity (Laird et al., 2010b), facilitating biomass gain (Kammann et al., 2011). Plant growth can also be affected by biochar-induced changes in soil nutrient conditions, particularly the cycling of P and K (Dempster et al., 2012a,b; Taghizadeh-Toosi et al., 2012). In this analysis, we found that plant tissue K concentration and soil P and K increased following biochar application (Fig. 1). These nutrients may be directly introduced to the soil through labile organic compounds associated with biochar and become available as these compounds weather (Topoliantz & Ponge, 2005; Yamato et al., 2006; Rajkovich et al., 2012). This effect, however, depends on the pro-

duction variables of the biochar (Hass et al., 2012), and is short lived, as the nutrients are used by plants and/or are leached from the soil (Steiner et al., 2007; Major et al., 2010). Long-term effects of biochar on nutrients occur through complex physiochemical reactions with soil particles (Spokas et al., 2011). One such reaction that affects P is biochar-induced increases in soil alkalinity (liming). In acidic soils phosphorus can be adsorbed onto iron oxides, which makes it unavailable to plants. Liming agents reduce the concentration of iron and aluminum in the soil solution and the previously bound phosphorus then becomes available (Cui et al., 2011). Liming also reduces the mobility of toxic elements, such as Al and Cd (Ritchey & Snuffer, 2002; Hass et al., 2012). Changes in plant productivity with biochar pH support this mechanism; alkaline biochars are more effective at increasing biomass than acidic biochars (Fig. 5d). Biochar was also most effective at changing soil pH in acidic soils, which would be particularly beneficial in low latitudes (Fig. 4) where soils are acidic and agriculture is limited by P availability (Steiner et al., 2008b). Another way biochar may affect soil nutrients is through the reduction in leaching losses (Laird et al., 2010a). Biochar’s porous structure, large surface area, and negative surface charge (Bird et al., 2008; Cheng et al., 2008; Downie et al., 2009; Novak et al., 2009a) increase the soil’s cation exchange capacity and allow for the retention of nutrients, such as K (Liang et al., 2006; Major et al., 2011). Biochar can also slow cation © 2012 Blackwell Publishing Ltd, GCB Bioenergy, 5, 202–214

B I O C H A R A N D E C O S Y S T E M S : A M E T A - A N A L Y S I S 207 Table 1 The mean (CI) effect size for the fertilizer (RRF) and fertilizer plus biochar treatments (RRBFC and RRBFF). Bold values of RRF were significantly different than the effect size of RRB. Bold values of RRBFC indicate a significant difference than θ, a test statistic that represents the potential additive effect of biochar and fertilizer. For those cases where fertilizer was applied to both the control and biochar treatment (RRBFF), bold values indicate a significant difference from zero

1.18 0.92 0.89

0.05  0.25

0.21  0.14

0.78

0.35  0.16 0.05  0.52 Insufficient data 0.22  0.18

        

0.84 0.76 0.76 1.06 2.16 1.15 0.76 0.89 0.93

0.06 0.09 0.08 0.00 0.21 0.51 0.08 0.13 0.94

0.25 0.05 0.04 3.83 1.43 0.23 0.002 0.04 0.11

        

0.17 0.07 0.08 1.03 0.73 0.2 0.03 0.08 0.08

0.23 0.08 0.39 0.55 1.66 0.66 0.11 0.33 1.27

0.17 0.15 0.25 1.16 0.73 0.37 0.04 0.12 0.27

        

0.16 0.12 0.08 0.19 0.41 0.33 0.03 0.16 0.51

loss by inducing a shift in soil water nutrient transport from bypass to matrix flow (Laird et al., 2010a). Nutrients, such as P, can be adsorbed to biochar’s surface, which slows leaching (Laird et al., 2010a; Beck et al., 2011). The analysis of application rate provided little insight into how biochar maybe best applied; there was no obvious threshold or trend with increasing application rates (Fig. 2). Variability in plant response, however, increased at with application rates (Fig. 2 inset). Other studies have found application thresholds, beyond which growth was reduced: Rajkovich et al. (2012) found a general application threshold of 2% (26 t ha 1); Kammann et al. (2011) found that quinoa growth was retarded at 100–200 t ha 1 (6.7–13.3%); and Baronti et al. (2010) observed a threshold of 10 t ha 1 (0.7%) for durum wheat.

1.5 1.0

n = 51 n = 16

n = 14 n = 14

n = 11 n = 10

n = 15 n = 10

Aboveground ns

Belowground

Above:below ns

Total biomass

**

***

Fig. 3 The relative effect size (mean  CI) of biochar treatments (RRB) for annual and perennial plant productivity. Significance of Wilcoxon signed rank tests: *P < 0.05, **P < 0.01, ***P < 0.001.

2

0.83  0.37 0.48  0.62 0.55  0.33

1

0.69  0.35 0.31  0.45 0.21  0.1

0

0.18  0.1 0.23  0.18 0.03  0.18

–1

1.22 1.48 0.95

0.5

0.96  0.29 1.38  1.4 0.56  0.69

0.0

0.65  0.23 0.64  0.74 0.41  0.7

−0.5

Aboveground Belowground Above : below ratio Yield SMB Rhizobia nodules % Mycorrhizae col. Tissue N conc. Tissue P conc. Tissue K conc. Soil inorganic N Soil P Soil K pH Soil total N Soil total C

−1.0

RRBFF

RRB − aboveground

h

Perennials

RRB

RRBFC

RRF

Annuals

Biochar–fertilizer interactions Although biochar altered the soil nutrient environment and promoted plant growth, it is effects are not equivalent to that of fertilizer, as fertilizer alone was more effective for improving plant productivity and soil P (Table 1). Furthermore, unlike in the fertilizer treat© 2012 Blackwell Publishing Ltd, GCB Bioenergy, 5, 202–214

0

10

20

30

40

50

Degree latitude Fig. 4 The relative effect size of biochar treatments (RRB) for aboveground productivity as a function of latitude. (Adj. R2 = 0.079, P < 0.01).

208 L . A . B I E D E R M A N & W . S . H A R P O L E

Fig. 5 The relative effect size of biochar treatments (RRB) for aboveground productivity as a function of (a) source material (P < 0.01), (b) pyrolysis temperature (Adj. R2 = 0, P = 0.9), (c) biochar pH (Adj. R2 = 0.059, P < 0.05), and (d) C : N ratio (Adj. R2 = 0.172, P < 0.01).

ments, plant allocation patterns did not change in biochar treatments. Plants typically respond to improved nutrient conditions by reducing the allocation of tissue belowground (Brouwer, 1962; Poorter & Nagel, 2000), and a lack of change following biochar exposure suggests that it is not similarly alleviating belowground competition for nutrients. In contrast, biochar amendments were better than fertilizer at increasing plant P and K tissue concentrations. As explained above, biochar can improve the availability of these nutrients through soil liming and by reducing leaching losses. Despite the differential effects of these materials, however, there was limited evidence of a superadditive or synergistic effect when both biochar and fertilizer are applied. Our analysis finds that biochar’s effects on N are limited, as both soil available N and the concentration of N in plant tissues were unaffected by its application. Furthermore, aboveground productivity did not change with the nitrogen content of the biochar, as measured by C : N ratio. This contradicts studies that find complex interactions between fertilizer, biochar, and the N cycle (DeLuca et al., 2006; Laird et al., 2010a; Taghi-

zadeh-Toosi et al., 2012). Soil type and existing soil N status are strong controls on soil N cycling and because this meta-analysis generalizes across a wide range of soils these effects may be masked. There were, however, increases in total soil N, presumably because the N within the structure of the biochar material contributed to this pool, but is unavailable to plants and microbes.

Effects on perennial species and soil organisms Belowground, annual plants responded positively to biochar, whereas perennial species (including native and naturalized grasses and forbs, forage crops, and sugar cane) had no response and the difference between these two life forms was significant (Fig. 3). Rather than producing differences in tissue allocation, biochar affects overall plant productivity; increasing it for annual plants and with limited effect on perennials. There was also considerable variability in plant response, especially for annual plants belowground. Numerous volatile and biologically active compounds, such as ethylene, butyric acids, benzoic acid, quinones, and 2-phenoxyethanol, are introduced into the soil with © 2012 Blackwell Publishing Ltd, GCB Bioenergy, 5, 202–214

B I O C H A R A N D E C O S Y S T E M S : A M E T A - A N A L Y S I S 209 biochar amendment (Graber et al., 2010; Spokas et al., 2010) and depending on concentration, these compounds may promote growth, or produce toxic effects (Keely & Pizzorno, 1986; Elad et al., 2010; Meller Harel et al., 2012). Differences in allocation and phenology, such as higher growth rates in annual species (Pitelka, 1977), may contribute to functional group sensitivity to these compounds. Documented changes following historical charcoal applications (not included in the analysis) underscore biochar’s potential effect on plant community composition (Chidumayo, 1988). For example, annual weed cover and legume density was increased, and perennial sprouting reduced, on Terra Preta soils compared with adjacent nonaffected areas (Major et al., 2005). Plant species composition is also affected by the alkaline soils and altered calcium concentrations found in former charcoal production areas (Mikan & Abrams, 1995; Young et al., 1996). Biochar has variable effects on plant-associated soil microbes. Root nodulation by rhizobia generally increased (Fig. 1), presumably because conditions associated with efficient N-fixation, such as slightly alkaline soil and access to P, have improved (Graham, 1981; Rondon et al., 2007; Lehman et al., 2011). In contrast, biochar did not significantly alter root colonization by mycorrhizal fungi, although the wide confidence intervals suggest that there is considerable variability. Biochar changes the plant’s nutrient environment, increasing P availability for example, and this may reduce plant dependence on mycorrhizae (Raznikiewicz et al., 1994). Biochar could also affect the adsorption and desorption of signaling compounds that would otherwise promote root–fungi connections (Akiyama et al., 2005; Warnock et al., 2007). Biochar application increased total soil C, thus it contributes to the sequestration of carbon at least in the short term (3 years) (Fig. 1). Although much of this carbon sequestration is due to the inert portions of the biochar material, there was also an increase in SMB, another soil carbon pool. Biochar can contribute to SMB through various mechanisms. It augments the availability of micropore habitat providing refugia for soil microbes from larger fauna, thus increasing microbe population size (Zackrisson et al., 1996; Pietik€ainen et al., 2000). Labile organic compounds, a by-product of the production process, are introduced to the soil with biochar and decompose readily. Microbial food resources are also enhanced by the retention of native dissolved organic matter on the charged surface of biochar (Steiner et al., 2008a; Deenik et al., 2010) and through biocharinduced increases in plant productivity (Graber et al., 2010; Jones et al., 2012). It is also possible that biochar addition could increase microbe populations by ‘priming’ the decomposition of native soil carbon, leading to © 2012 Blackwell Publishing Ltd, GCB Bioenergy, 5, 202–214

a net loss of carbon to the atmosphere (Wardle et al., 2008; Rogovska et al., 2011). Recent studies, however, have found priming to be negligible in soils that are unaffected by phenolic compounds (Bell & Worrall, 2011; Jones et al., 2011; Zimmerman et al., 2011).

Biochar characteristics The net ability of biochar to enhance ecosystem services depends, in part, on the specific qualities of the biochar and site conditions (Haefele et al., 2011). Within the literature surveyed there was little uniformity on the production methods of biochar; materials were created in a range of pyrolyzers from highly sophisticated industrial equipment to primitive earthen mounds. Temperature conditions also varied, and there was no precise definition of terminology, such as the time and temperature conditions of ‘fast’ or ‘slow’ pyrolysis processes (Mohan et al., 2006). Furthermore, the reporting of production (feedstock source, time and temperature of pyrolysis, kiln type) variables and the resulting qualities (pH, C : N ratio, and nutrient content) of the biochars was inconsistent and there were few data available to correlate with the variables of interest. Because pyrolysis conditions affect the behavior of biochar in the soil (Bruun et al., 2012), the lack of data limits our ability to understand biochar’s interaction with soil and its organisms (Spokas et al., 2011). There was considerable variation in how feedstock source influences aboveground productivity (Fig. 5); biochars from grass and manure/sewage increased aboveground productivity. This was unexpected given the reputation of grass- and manure-sourced biochars for producing unpredictable effects due to high concentrations of silicates (Lehman et al., 2011). We also found that biochars produced at higher temperatures were more effective at promoting aboveground productivity. High-temperature biochars tend to be alkaline (Bagreev et al., 2001; Novak et al., 2009b) and contain less biologically active volatile compounds (Gundale & DeLuca, 2006; Hale et al., 2012) that can otherwise limit plant growth. High-temperature biochars are also more resistant to decomposition and would, therefore, be better candidates to fulfill the C sequestration function (Novak et al., 2010; Harvey et al., 2012).

Future research needs and environmental concerns We found that the addition of biochar generally improves, or at least does not harm, many aspects of the ecosystem and its functioning, including plant productivity and soil nutrient content. This is consistent with the findings of other nonquantitative reviews (Glaser et al., 2002; Marris, 2006; Lehmann, 2007b;

210 L . A . B I E D E R M A N & W . S . H A R P O L E Warnock et al., 2007). However, to achieve meaningful goals for carbon sequestration, such as 12% of current anthropogenic CO2 emissions (Woolf et al., 2010), large quantities of biochar would have to be applied to a significant portion of the earth’s arable land. Because of the ability of applied biochar to be transported by wind and water, nontarget organisms will be affected by this activity, but there are limited data available for biochar’s effects on nonagricultural species, including native plant communities, aquatic systems, and soil organisms. For example, only 16 studies have tested biochar effects on perennial plants and relatively few studies are needed to overturn the positive findings for rhizobia and SMB. Changes in community composition following biochar application are also very limited and the different responses by annual and perennial plants demonstrate that we still do not understand the mechanism by which it interacts with organisms. Perennial plants and soil creatures perform many critical ecosystem services, such as erosion prevention and pest predation, in agricultural systems. It is imperative that we understand how biochar interacts with all aspects of the environment prior to its widespread application.

Acknowledgments

Beck DA, Johnson GR, Spolek GA (2011) Amending greenroof soil with biochar to affect runoff water quantity and quality. Environmental Pollution, 159, 2111–2118. Beesley L, Moreno-Jimenez E, Gomez-Eyles JL (2010) Effects of biochar and greenwaste compost amendments on mobility, bioavailability and toxicity of inorganic and organic contaminants in a multi-element polluted soil. Environmental Pollution, 158, 2282–2287. Bell MJ, Worrall F (2011) Charcoal addition to soils in NE England: a carbon sink with environmental co-benefits? Science of the Total Environment, 409, 1704–1714. Bellard C, Bertelsmeier C, Leadley P, Thuiller W, Courchamp F (2012) Impacts of climate change on the future of biodiversity. Ecology Letters, 15, 365–377. Berglund M, DeLuca H, Zackrisson O (2004) Activated carbon amendments to soil alters nitrification rates in scots pine forests. Soil Biology and Biochemistry, 36, 2067 –2073. Bird MI, Ascough PL, Young IM, Wood CV, Scott AC (2008) X-ray microtomographic imaging of charcoal. Journal of Archaeological Science, 35, 2698–2706. Birk JJ, Steiner C, Teixiera WC, Zech W, Glaser B (2009) Microbial response to charcoal amendments and fertilization of a highly weathered tropical soil. In: Amazonian Dark Earths: Wim Sombroek’s Vision (eds Woods WI, Teixeira WJ, Lehmann J, Steiner C, WinklerPrins AMGA, Rebellato L), pp. 309–324. Springer Science + Business Media, Berlin. Blackwell P, Krull E, Butler G, Herbert A, Solaiman Z (2010) Effect of banded biochar on dryland wheat production and fertiliser use in south-western Australia: an agronomic and economic perspective. Australian Journal of Soil Research, 48, 531–545. Bolster CH, Abit SM (2012) Biochar pyrolyzed at two temperatures effects Escherichia coli transport through a sandy soil. Journal of Environmental Quality, 41, 124–133. Brockhoff SR, Christians NE, Killorn RJ, Horton R, Davis DD (2010) Physical and mineral-nutrition properties of sand-based turfgrass root zones amended with biochar. Agronomy Journal, 102, 1627–1631. Brouwer R (1962) Nutritive influences on the distribution of dry matter in the plant. Journal of Agricultural Science, 10, 399–408. Bruun W, M€ uller-St€ over D, Ambus P, Hauggaard-Nielsen H (2011) Application of biochar to soil and N2O emissions: potential effects of blending fast-pyrolysis biochar with anaerobically digested slurry. European Journal of Soil Science, 62, 581–589. Bruun EW, Ambus P, Egsgaard H, Hauggaard-Nielsen H (2012) Effects of slow and fast pyrolysis biochar on soil C and N turnover dynamics. Soil Biology and Bio-

We wish to thank the Leopold Center for Sustainable Agriculture for funding this project, Joseph Garrison, Erich Sneller, and Emily Zimmerman for assistance, and Dean Adams and David Laird for technical advice.

chemistry, 46, 73–79. Chan KY, Van Zwieten L, Meszaros I, Downie A, Joseph S (2007) Agronomic values of greenwaste biochar as a soil amendment. Australian Journal of Soil Research, 45, 629–634. Chan KY, van Zwieten L, Meszaros , I , Downie A, Joseph S (2008) Using poultry litter biochars as oil amendments. Australian Journal of Soil Research, 46, 437–444.

References

Chen Y, Shinogi Y, Taira M (2010) Influence of biochar use on sugarcane growth, soil parameters, and ground water quality. Australian Journal of Soil Research, 48, 526–530. Cheng C-H, Lehmann J, Engelhard MH (2008) Natural oxidation of black carbon in soils: changes in molecular form and surface charge along a climosequence. Geochimica et Cosmochimica Acta, 72, 1598–1610. Cheng Y, Cai Z-C, Chang SX, Wang J, Zhang J-B (2012) Wheat straw and its biochar have contrasting effects on inorganic N retention and N2O production in a culti-

Ahmad M, Soo Lee S, Yang JE, Ro HM, Han Lee Y, Sik Ok Y (2012) Effects of soil dilution and amendments (mussel shell, cow bone, and biochar) on pb availability and phytotoxicity in military shooting range soil. Ecotoxicology and Environmental Safety, 79, 225–231. Akiyama K, Matsuzaki K-I, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature, 435, 824–827. Anderson LK, Hercogova J, Wollina U, Davis MDP (2012) Climate change and skin disease: a review of the English-language literature. International Journal of Dermatology, 51, 656–661. Asai H, Samson BK, Stephan HM et al. (2009) Biochar amendment techniques for upland rice production in northern Laos. Field Crops Research, 111, 81–84. Atkinson CJ, Fitzgerald JD, Hipps NA (2010) Potential mechanisms for achieving agricultural benefits from biochar application to temperate soils: a review. Plant and Soil, 337, 1–18. Auffhammer M, Ramanathan V, Vincent JR (2012) Climate change, the monsoon, and rice yield in India. Climatic Change, 111, 411–424. Augusto L, Bakker MR, Meredieu C (2008) Wood ash applications to temperate forest ecosystems – potential benefits and drawbacks. Plant and Soil, 306, 181– 198. Bagreev A, Bandosza TJ, Locke DC (2001) Pore structure and surface chemistry of adsorbents obtained by pyrolysis of sewage sludge-derived fertilizer. Carbon, 39, 1971–1979. Bakkenes M, Alkemade JMR, Ihle F, Leemans R, Latour JB (2002) Assessing effects of forecasted climate change on the diversity and distribution of European higher plants for 2050. Global Change Biology, 8, 390–407. Baronti S, Alberti G, Vedove GD et al. (2010) The biochar option to improve plant yields: first results from some field and pot experiments in Italy. Italian Journal of Agriculture, 5, 3–11.

vated black chernozem. Biology and Fertility of Soils, 48, 941–946. Chidumayo E (1988) Effects of wood carbonization on soil and initial development of seedlings in miombo woodland, Zambia. Forest Ecology and Management, 70, 3553–3557. Choi D, Makoto K, Quoreshi AM, Qu L (2009) Seed germination and seedling physiology of Larix kaempferi and Pinus densiflora in seedbeds with charcoal and elevated CO2. Landscape and Ecological Engineering, 5, 107–113. Clay SA, Malo DD (2012) The influence of biochar production on herbicide sorption characteristics. In: Herbicides – Properties, Synthesis and Control of Weeds (eds Hasaneen MNAE-G), pp. 59–74. InTech. Available at: http://www.intechopen. com/books/herbicides-properties-synthesis-and-control-of-weeds/the-influenceof-biochar-production-on-herbicide-sorption-characteristics (accessed 18 January 2012). Clough J, Bertram E, Ray L, Condron M, O’Callaghan M, Sherlock R, Wells S (2010) Unweathered wood biochar impact on nitrous oxide emissions from a bovine-urine-amended pasture soil. Soil Science Society of America Journal, 74, 852–860. Cui H-J, Wang MK, Fu M-K, Ci E (2011) Enhancing phosphorus availability in phosphorus-fertilized zones by reducing phosphate adsorbed on ferrihydrite using rice straw-derived biochar. Journal Soils Sediments, 11, 1135–1141. Deal C, Brewer CE, Brown RC, Okure MA, Amoding A (2012) Comparison of kilnderived and gasifier-derived biochars as soil amendments in the humid tropics. Biomass and Bioenergy, 37, 161–168.

© 2012 Blackwell Publishing Ltd, GCB Bioenergy, 5, 202–214

B I O C H A R A N D E C O S Y S T E M S : A M E T A - A N A L Y S I S 211 Deenik JL, McClellan T, Uehara G, Antal MJ, Campbell S (2010) Charcoal volatile matter content influences plant growth and soil nitrogen transformations. Soil Sci-

tration potential of engineered black carbons (biochars). Environmental Science and Technology, 46, 1415–1421.

ence Society of America Journal, 74, 1259–1270. Deenik J, Diarra A, Uehara G, Campbell S, Samiyoshi Y, Antal MJ (2011) Charcoal ash and volatile matter effects on soil properties and plant growth in an acid ultisol. Soil Science, 176, 336–345. DeLuca TH, MacKenzie MD, Gundale MJ, Holben WE (2006) Wildfire-produced charcoal directly influences nitrogen cycling in ponderosa pine forests. Soil Science Society of America Journal, 70, 448–453.

Hass A, Gonzalez JM, Lima IM, Godwin HW, Halvorson JJ, Boyer DG (2012) Chicken manure biochar as liming and nutrient source for acid Appalachian soil. Journal of Environmental Quality, 41, 1096–1106. Hedges LV, Gurevitch J, Curtis PS (1999) The meta-analysis of response ratios in experimental ecology. Ecology, 80, 1150–1156. Hill J, Nelson E, Tilman D, Polasky S, Tiffany D (2006) Environmental, economic, and energetic costs and benefits of biodiesel and ethanol biofuels. PNAS, 103,

Dempster N, Gleeson B, Solaiman M, Jones L, Murphy V (2012a) Decreased soil microbial biomass and nitrogen mineralisation with eucalyptus biochar addition to a coarse textured soil. Plant and Soil, 354, 311–324. Dempster N, Jones L, Murphy V (2012b) Organic nitrogen mineralisation in two contrasting agro-ecosystems is unchanged by biochar addition. Soil Biology and Biochemistry, 48, 47–50.

11206–11210. Hoshi T (2001) Growth promotion of tea trees by putting bamboo charcoal in the soil. In: Proceedings of 2001 International Conference on O-cha (tea) Culture and Science Tokyo, Japan pp. 147–150. World Green Tea Association, Tokyo, Japan. Hossain MK, Strezov V, Chan KY, Nelson PF (2010) Agronomic properties of wastewater sludge biochar and bioavailability of metals in production of cherry tomato

Downie A, Crosky A, Munroe P (2009) Physical properties of biochar. In: Biochar for Environmental Management (eds Lehmann J, Joseph S), pp 13–29. Earthscan, London. Doydora SA, Cabrera ML, Das KC, Gaskin JW, Sonon LS, Miller WP (2011) Release of nitrogen and phosphorus from poultry litter amended with acidified biochar. International Journal of Environmental Research and Public Health, 8, 1491– 1502. Durenkamp M, Luo Y, Brookes C (2010) Impact of black carbon addition to soil on

(Lycopersicon esculentum). Chemosphere, 78, 1167–1171. Ishii T, Kadoya K (1994) Effects of charcoal as a soil conditioner on citrus growth and vesicular-arbuscular mycorrhizal development. Journal of the Japanese Society of Horticultural Science, 63, 529–535. Islami T, Curitno B, Basuki N, Suryanto A (2011) Maize yield and associated soil quality changes in cassava + maize intercropping system after 3 years of biochar application. Journal of Agriculture Food Technology, 1, 112–115.

the determination of soil microbial biomass by fumigation extraction. Soil Biology and Biochemistry, 42, 2026–2029. Elad Y, David DR, Harel YM, Borenshtein M, Kalifa HB, Silber A, Graber ER (2010) Induction of systemic resistance in plants by biochar, a soil-applied carbon sequestering agent. Disease Control and Pest Management, 100, 913–921. Elmer WH, Pignatello J (2011) Effect of biochar amendments on mycorrhizal associa-

Iswaran V, Jauhri KS, Sen A (1980) Effect of charcoal, coal and peat on the yield of moong, soybean and pea. Soil Biology and Biochemistry, 12, 191–192. Jia J, Li B, Chen Z, Xie Z, Xiong Z (2012) Effects of biochar application on vegetable production and emissions of N2O and CH4. Soil Science and Plant Nutrition, 58, 1–7. Jindo K, Suto K, Matsumoto K, Garcıa C, Sonoki T, Sanchez-Monedero MA (2012) Chemical and biochemical characterisation of biochar-blended composts pre-

tions and Fusarium crown and root rot of Asparagus in replant soils. Plant Disease, 95, 960–966. Ezawa T, Yamamoto K, Yoshida S (2002) Enhancement of the effectiveness of indigenous arbuscular mycorrhizal fungi by inorganic soil amendments. Soil Science and Plant Nutrition, 48, 897–900. Gaskin JW, Speir RA, Harris K, Das C, Lee RD, Morris LA, Fisher DS (2010) Effect of peanut hull and pine chip biochar on soil nutrients, corn nutrient status, and

pared from poultry manure. Bioresource Technology, 110, 396–404. Jones L, Murphy V, Khalid M, Ahmad W, Edwards-Jones G, DeLuca H (2011) Shortterm biochar-induced increase in soil CO2 release is both biotically and abiotically mediated. Soil Biology and Biochemistry, 43, 1723–1731. Jones L, Rousk J, Edwards-Jones G, DeLuca H, Murphy V (2012) Biochar-mediated changes in soil quality and plant growth in a three-year field trial. Soil Biology and Biochemistry, 45, 113–124.

yield. Agronomy Journal, 102, 623–633. Genesio L, Miglietta F, Lugato E, Baronti S, Pieri M, Vaccari FP (2012) Surface albedo following biochar application in durum wheat. Environmental Resource Letters, 7, doi: 10.1088/1748-9326/7/1/014025. Glaser B, Lehmann J, Zech W (2002) Ameliorating physical and chemical properties of highly weathered soils in the tropics with bio-char – a review. Biology and Fer-

Kammann CI, Linsel S, G€ oßling JW, Koyro HW (2011) Influence of biochar on drought tolerance of Chenopodium quinoa willd. and on soil–plant relations. Plant and Soil, 345, 195–210. Keech O, Carcaillet C, Nilsson MC (2005) Adsorption of alleopathic compounds by wood-derived charcoal; the role of wood porosity. Plant and Soil, 272, 291–300. Keely SC, Pizzorno M (1986) Charred wood stimulated germination of two fire-fol-

tility of Soils, 35, 219–230. Graber ER, Meller-Harel Y, Kolton M et al. (2010) Biochar impact on development and productivity of pepper and tomato grown in fertigated soilless media. Plant and Soil, 337, 481–496. Graham PH (1981) Some problems of nodulation and symbiotic nitrogen fixation in Phaseolus vulgaris L.: a review. Field Crops Research, 4, 93–112. Gundale MJ, DeLuca TH (2006) Temperature and source material influence ecologi-

lowing herbs of the California chaparral and the role of hemicellulose. American Journal of Botany, 73, 1289–1297. Kimetu JM, Lehmann J, Ngoze SO et al. (2008) Reversibility of soil productivity decline with organic matter of differing quality along a degradation gradient. Ecosystems, 11, 726–739. Kleiner K (2009) Bright prospect of biochar. Nature Reports Climate Change, 3, 72–74. Knowles OA, Robinson BH, Contangelo A, Clucas L (2011) Biochar for the mitiga-

cal attributes of ponderosa pine and Douglas-fir charcoal. Forest Ecology and Management, 231, 86–93. Gundale MJ, DeLuca TH (2007) Charcoal effects on soil solution chemistry and growth of Koeleria macrantha in the ponderosa pine/Douglas-fir ecosystem. Biology and Fertility of Soils, 43, 303–311. Haefele M, Konboon Y, Wongboon W, Amarante S, Maarifat A, Pfeiffer M, Knobl-

tion of nitrate leaching from soil amended with biosolids. The Science of the Total Environment, 409, 3206–3210. Kolb SE, Fermanich KJ, Dornbush ME (2009) Effect of charcoal quantity on microbial biomass and activity in temperate soils. Soil Science Society of America Journal, 73, 1173–1182. Kulmatiski A, Beard KH (2006) Activated carbon as a restoration tool: potential for

auch C (2011) Effects and fate of biochar from rice residues in rice-based systems. Field Crops Research, 121, 430–440. Hale SE, Hanley K, Lehmann J, Zimmerman AR, Cornelissen G (2011) Effects of chemical, biological, and physical aging as well as soil addition on the sorption of pyrene to activated carbon and biochar. Environmental Science and Technology, 45, 10445–10453. Hale SE, Lehmann J, Rutherford D et al. (2012) Quantifying the total bioavailable

control of invasive plants in abandoned agricultural fields. Restoration Ecology, 14, 251–257. Lafferty KD (2009) The ecology of climate change and infectious diseases. Ecology, 90, 888–900. Laird DA (2008) The Charcoal Vision: a win-win-win scenario for simultaneously producing bioenergy, permanently sequestering carbon, while improving soil and water quality. Agronomy Journal, 100, 178–181.

polycyclic aromatic hydrocarbons and dioxins in biochars. Environmental Science and Technology, 46, 2830–2838. Hammes K, Schmidt MWI (2009) Changes of biochar in soil. In: Biochar for Environmental Management (eds Lehmann J, Joseph S), pp 169–182. Earthscan, London. Harpole WS, Goldstein L, Aicher RJ (2007) Resource limitation. In: Ecology and Man-

Laird DA, Brown RC, Amonette JE, Lehmann J (2009) Review of the pyrolysis platform for co-producing bio-oil and biochar. Biofuels, Bioproducts and Biorefining, 3, 547–562. Laird D, Fleming P, Wang B, Horton R, Karlen D (2010a) Biochar impact on nutrient leaching from a Midwestern agricultural soil. Geoderma, 158, 436–442. Laird DA, Fleming P, Davis DD, Horton R, Wang B, Karlen DL (2010b) Impact of

agement of California Grassland (eds Stromberg M, Corbin J, D’Antonio C), pp 119– 127. University of California Press, Berkeley. Harvey OR, Kuo , L-J , Zimmerman AR, Louchouarn P, Amonette JE, Herbert BE (2012) An index-based approach to assessing recalcitrance and soil carbon seques-

biochar amendments on the quality of a typical Midwestern agricultural soil. Geoderma, 158, 443–449. Lajeunesse MJ, Forbes MR (2003) Variable reporting and quantitative reviews: a comparison of three meta-analytical techniques. Ecology Letters, 6, 448–454.

© 2012 Blackwell Publishing Ltd, GCB Bioenergy, 5, 202–214

212 L . A . B I E D E R M A N & W . S . H A R P O L E Lau JA, Puliafico KP, Kopshever JA et al. (2008) Inference of allelopathy is complicated by effects of activated carbon on plant growth. New Phytologist, 178, 412–423.

Nag SK, Kookana R, Smith L, Krull E, Macdonald LM, Gill G (2011) Poor efficacy of herbicides in biochar-amended soils as affected by their chemistry and mode of

Lehman J, Rillig MC, Thies J, Masiello CA, Hockaday WC, Crowley D (2011) Biochar effects on soil biota – a review. Soil Biology and Biochemistry, 43, 1912–1836. Lehmann J (2007a) A handful of carbon. Nature, 447, 143–144. Lehmann J (2007b) Bioenergy in the Black. Frontiers in Ecology, 5, 381–387. Lehmann J, Joseph S (2009) Biochar for environmental management: an introduction. In: Biochar for Environmental Management (eds Lehmann J, Joseph S), pp 1–12. Earthscan, London.

action. Chemosphere, 84, 1572–1577. Nelson NO, Agudelo SC, Yian W, Gan J (2011) Nitrogen and phosphorus availability in biochar-amended soils. Soil Science, 176, 218–226. Nigussie A, Kissi E, Misganaw M, Ambaw G (2012) Effect of biochar application on soil properties and nutrient uptake of lettuces (Lactuca sativa) grown in chromium polluted soils. American-Eurasian Journal of Agriculture and Environmental Science, 12, 369–376.

Lehmann J, Pereira da Silva J, Steiner C, Nehls T, Zech W, Glaser B (2003) Nutrient availability and leaching in an archaeological anthrosol and a ferralsol of the central Amazon basin: fertilizer, manure and charcoal amendments. Plant and Soil, 249, 343–357. Lehmann J, Gaunt J, Rondon M (2006) Biochar sequestration in terrestrial ecosystems – a review. Mitigation and Adaption Strategies for Global Change, 11, 395–419.

Nishio M, Okano S (1991) Stimulation of the growth of alfalfa and infection of roots with indigenous vesicular-arbuscular mycorrhizal fungi by the application of charcoal. Bulletin of the National Grassland Research Institute, 45, 61–71. Noguera D, Rond on M, Laossi K-R, Hoyos V, Lavelle P, Cruz de Carvalho MH, Barot S (2010) Contrasted effect of biochar and earthworms on rice growth and resource allocation in different soils. Soil Biology & Biochemistry, 42, 1017–1027.

Lentz D, Ippolito A (2012) Biochar and manure affect calcareous soil and corn silage nutrient concentrations and uptake. Journal of Environmental Quality, 41, 1033– 1043. Liang B, Lehmann J, Solomon D et al. (2006) Black carbon increases cation exchange capacity in soils. Soil Science Society of America Journal, 70, 1719–1730. Liu Y, Yang M, Wu Y, Wang H, Chen Y, Wu W (2011) Reducing CH4 and CO2 emissions from waterlogged paddy soil with biochar. Journal of Soils and Sediments, 11,

Norguera D, Barot S, Laossi KR, Cardoso J, Lavelle P, Cruz de Carvalho MH (2012) Biochar but not earthworms enhances rice growth through increased protein turnover. Soil Biology and Biochemistry, 52, 13–20. Novak JM, Lima I, Xing B et al. (2009a) Characterization of designer biochar produced at different temperatures and their effects on a loamy sand. Annals of Environmental Science, 3, 195–206. Novak JM, Busscher WJ, Laird DL, Ahmedna M, Watts DW, Niandou MAS (2009b)

930–939. Liu J, Schulz H, Brandl S, Miehtke H, Huwe B, Glaser B (2012a) Short-term effect of biochar and compost on soil fertility and water status of a dystric cambisol in NE Germany under field conditions. Journal of Plant Nutrition and Soil Science, 175, 698–707. Liu X-Y, Qu J-J, Li L-Q, Zhang A-F, Jufeng Z, Zheng JW, Pan G-X (2012b) Can bio-

Impact of biochar amendment on fertility of a southeastern coastal plain soil. Soil Science, 174, 105–112. Novak M, Busscher J, Watts W, Laird D, Ahmedna A, Niandou AS (2010) Short-term CO2 mineralization after additions of biochar and switchgrass to a typic kandiudult. Geoderma, 154, 281–288. Park JH, Choppala GK, Bolan NS, Chung JW, Chuasavathi T (2011) Biochar reduces

char amendment be an ecological engineering technology to depress N2O emission in rice paddies? A cross-site field experiment from south China. Ecological Engineering, 42, 168–173. Magrini-Bair KA, Czernik S, Pilath HM, Evans RJ, Maness PC, Leventhal J (2009) Biomass derived, carbon sequestering, designed fertilizers. Annals of Environmental Science, 3, 217–225. Major JA, DiTommaso A, Lehmann J, Falc~ao NPS (2005) Weed dynamics of Amazo-

the bioavailability and phytotoxicity of heavy metals. Plant and Soil, 348, 439–451. Paz-Ferreiro J, Gasc o G, Gutierrez B, Mendez A (2012) Soil biochemical activities and the geometric mean of enzyme activities after application of sewage sludge and sewage sludge biochar to soil. Biology and Fertility of Soils, 48, 511–517. Peng X, Ye L, Wang H, Zhou H, Sun B (2011) Temperature- and duration-dependent rice straw-derived biochar: characteristics and its effects on soil properties of an ultisol in southern China. Soil and Tillage Research, 112, 159–166.

nian Dark Earth and adjacent soils of Brazil. Agriculture, Ecosystems and Environment, 111, 1–12. Major J, Lehmann J, Rondon M, Goodale C (2009) Fate of soil-applied black carbon: downward migration, leaching and soil respiration. Global Change Biology, 16, 1366–1379. Major J, Rondon M, Molina D, Riha SJ, Lehmann J (2010) Maize yield and nutrition

Pietik€ainen J, Kiikkil€a O, Fritze H (2000) Charcoal as a habitat for microbes and its effect on the microbial community of the underlying humus. Oikos, 89, 231–242. Pitelka LF (1977) Energy allocation in annual and perennial lupines (Lupinus: leguminosae). Ecology, 58, 1055–1065. Poorter H, Nagel O (2000) The role of biomass allocation in the growth response of plants to different levels of light, CO2, nutrients and water: a quantitative review.

during 4 years after biochar application to a Colombian savanna oxisol. Plant and Soil, 333, 117–128. Major JA, Rondon M, Molina D, Riha SJ, Lehmann J (2011) Nutrient leaching in a Columbian savanna oxisol amended with biochar. Journal of Environmental Quality, 41, 1076–1086. Makoto K, Tamai Y, Kim S, Koike T (2010) Buried charcoal layer and ectomycorrhizae cooperatively promote the growth of Larix gmelinii seedlings. Plant and Soil,

Australian Journal of Plant Physiology, 27, 595–607. Prendergast-Miller MT, Duvall M, Sohi SP (2011) Localisation of nitrate in the rhizosphere of biochar-amended soils. Soil Biology & Biochemistry, 43, 2243–2246. R Development Core Team (2011) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-070, URL. Available at: http://www.R-project.org/ (accessed 1 February 2012) Rajkovich S, Enders A, Hanley K, Hyland C, Zimmerman AR, Lehmann J (2012)

327, 143–152. Mankasingh U, Choi PC, Ragnarsdottir V (2011) Biochar application in a tropical, agricultural region: a plot scale study in Tamil Nadu, India. Applied Geochemistry, 26, S218–S221. Marchetti R, Castelli F, Orsi A, Sghedoni L, Bochicchio D (2012) Biochar from swine manure solids: influence on carbon sequestration and Olsen phosphorus and

Corn growth and nitrogen nutrition after additions of biochars with varying properties to a temperate soil. Biology and Fertility of Soils, 48, 271–284. Raznikiewicz H, Carlgren K, Maartensson A (1994) Impact of phosphorus fertilization and liming on the presence of arbuscular mycorrhizal spores in a Swedish long-term field experiment. Swedish Journal of Agricultural Research, 24, 157–164. Ridenour WM, Callaway RM (2001) The relative importance of allelopathy in interfer-

mineral nitrogen dynamics in soil with and without digestate incorporation. Italian Journal of Agronomy, 7, 189–195. Marris E (2006) Black is the new green. Nature, 442, 624–626. Matsubara Y, Hasegawa N, Fukui H (2002) Incidence of fusarium root rot in asparagus seedlings infected with arbuscular mycorrhizal fungus as affected by several soil amendments. Journal of Japanese Society of Horticultural Science, 71, 370–374.

ence: the effects of an invasive weed on a native bunchgrass. Oecologia, 126, 444–450. Rilling MC, Wagner M, Salem M et al. (2010) Material derived from hydrothermal carbonization: effects on plant growth and arbuscular mycorrhiza. Applied Soil Ecology, 45, 238–242. Ritchey KD, Snuffer JD (2002) Limestone, gypsum, and magnesium oxide influence restoration of an abandoned Appalachian pasture. Agronomy Journal, 94, 830–839. Robertson SJ, Rutherford M, Lopez-Gutierrez JC, Massicotte HB (2012) Biochar

Meller Harel Y, Elad Y, Borenshtein M, Graber ER (2012) Biochar-induced systemic response of strawberry to foliar fungal pathogens. Plant and Soil, 350, 245–257. Mendez A, Gomez A, Paz-Ferreiro J (2012) Effects of sewage sludge biochar on plant metal availability after application to a Mediterranean soil. Chemosphere, 89, 1354– 1359. Mikan CJ, Abrams MD (1995) Altered forest composition and soil properties of his-

enhances seedling growth and alters root symbioses and properties of sub-boreal forest soils. Canadian Journal of Soil Science, 92, 329–340. Rodriguez L, Salazar P, Preston TR (2009) Effect of biochar and biodigester effluent on growth of maize in acid soils. Livestock Research for Rural Development, 21, 1–11. Rodriguez L, Salazar P, Preston TR (2011) Effect of a culture of “native” microorganisms, biochar and biodigester effluent on the growth of maize in acid soils.

toric charcoal hearths in southeastern Pennsylvania. Canadian Journal of Forestry, 25, 687–696. Mohan D, Pittman CU, Steele PH (2006) Pyrolysis of wood/biomass for bio-oil: a critical review. Energy & Fuels, 20, 848–889.

Livestock Research for Rural Development, 23, 1–7. Rogovska N, Laird D, Cruse R, Fleming P, Parkin T, Meek D (2011) Impact of biochar on manure carbon stabilization and greenhouse gas emissions. Soil Science Society of America Journal, 75, 871–879.

© 2012 Blackwell Publishing Ltd, GCB Bioenergy, 5, 202–214

B I O C H A R A N D E C O S Y S T E M S : A M E T A - A N A L Y S I S 213 Rondon MA, Lehmann J, Ramırez J, Hurtado M (2007) Biological nitrogen fixation by common beans (Phaseolus vulgaris L.) increases with bio-char additions. Biol-

Tryon EH (1948) Effect of charcoal on certain physical, chemical, and biological properties of forest soils. Ecological Monographs, 18, 81–115.

ogy and Fertility of Soils, 43, 699–708. Rosenthal R (1979) The “file drawer” problem and tolerance for null results. Psychological Bulletin, 86, 638–641. Rumpel C, Chaplot V, Planchon O, Bernadoe J, Valentin C, Mariotti A (2006) Preferential erosion of black carbon on steep slopes with slash and burn agriculture. Catena, 65, 30–40. Saranya K, Kumutha K, Krishnan PS (2011) Influence of biochar and Azospirillum

Uzoma C, Inoue M, Andry H, Fujimaki H, Zahoor A, Nishihara E (2011) Effect of cow manure biochar on maize productivity under sandy soil condition. Soil Use and Management, 27, 205–212. Vaccari P, Baronti S, Lugato E, Genesio L, Castaldi S, Fornasier F, Miglietta (2011) Biochar as a strategy to sequester carbon and increase yield in durum wheat. European Journal of Agronomy, 34, 231–238. Wardle DA, Nilsson M-C, Zackrisson (2008) Fire derived charcoal causes loss of for-

application on the growth of maize. Madras Agricultural Journal, 98, 158–164. Schomberg HH, Gaskin JW, Harris K et al. (2012) Influence of biochar on nitrogen fractions in a coastal plain soil. Journal of Environmental Quality, 41, 1087–1095. Schulz H, Glaser B (2012) Effects of biochar compared to organic and inorganic fertilizers on soil quality and plant growth in a greenhouse experiment. Journal of Plant Nutrition and Soil Science, 175, 410–422.

est humus. Science, 320, 629–621. Warnock DD, Lehmann J, Kuyper TW, Rilling MC (2007) Mycorrhizal responses to biochar in soil – concepts and mechanisms. Plant and Soil, 300, 9–20. Warnock DD, Mummey DL, McBride B, Major J, Lehmann J, Rillig MC (2010) Influences of non-herbaceous biochar on arbuscular mycorrhizal fungal abundances in roots and soils: results from growth-chamber and field experiments. Applied Soil

Shenhagavalli S, Mahimairaja S (2012) Characterization and effect of biochar on nitrogen and carbon dynamics in soil. International Journal of Advanced Biological Research, 2, 249–255. Sokchea H, Preston TR (2011) Growth of maize in acid soil amended with biochar, derived from gasifier reactor and gasifier stove, with or without organic fertilizer biodigester effluent. Livestock Research for Rural Development, 23, 1–7. Solaiman ZM, Sarcheshmehpour M, Abbot LK, Blackwell P (2010a) Effect of biochar

Ecology, 46, 450–456. Weißhuhn K, Prati , D (2009) Activated carbon may have undesired side effects for testing allelopathy in invasive plants. Basic and Applied Ecology, 10, 500–507. Wickham H (1999) Ggplot; Elegant Graphics for Data Analysis. Springer Science + Business Media, Dordrecht, Germany. Widowati , Utomo WH (2012) The effect of biochar on the growth and N fertilizer requirement of maize (Zea mays L.) in green house experiment. Journal of Agricul-

on arbuscular mycorrhizal colonisation, growth, P nutrition and leaf gas exchange of wheat and clover influenced by different water regimes. In: 19th World Congress of Soil Science, Soil Solutions for a Changing World pp 33–52. International Union of Soil Scientists, Madison, WI. Solaiman K, Blackwell P, Abbot LK, Storer P (2010b) Infectivity and effectiveness of five endomycorrhizal fungi: competition with indigenous fungi in field soils. Aus-

tural Science, 4, 255–262. Widowati , Utomo WH, Soehono LA, Shi D-Z, Guritno B (2011) Effect of biochar on the release and loss of nitrogen from urea fertilization. Journal of Agricultural Food Technology, 1, 127–132. Woolf D, Amonette , JE , Street-Perrot FA, Lehmann J, Joseph , S (2010) Sustainable biochar to mitigate global climate change. Nature Communications, 1, 1–9.

tralian Journal of Soil Research, 48, 546–554. Spokas KA, Baker JM, Reicosky DC (2010) Ethylene: potential key for biochar amendment impacts. Plant and Soil, 333, 443–452. Spokas KA, Cantrell KB, Novak JM et al. (2011) Biochar: synthesis of its agronomic impact beyond carbon sequestration. Journal of Environmental Quality, 41, 973–989. Steiner C, Teixeira WG, Lehmann J, Nehls T, Mac^edo JLV, Blum WEH, Zech W (2007) Long term effects of manure, charcoal and mineral fertilization on crop

Wurst S, Vender V, Rillig MC (2010) Testing for allelopathic effects in plant competition: does activated carbon disrupt plant symbioses? Plant Ecology, 211, 19–26. Yamato M, Okimori Y, Wibowo IF, Anshori S, Ogawa M (2006) Effects of the application of charred bark of Acacia mangium on the yield of maize, cowpea and peanut, and soil chemical properties in south Sumatra, Indonesia. Soil Science and Plant Nutrition, 52, 489–495. Yin DW, Meng J, Zheng GP, Zhong XM, Yu L, Gao JP, Chen WF (2012) Effects of

production and fertility on a highly weathered central Amazonian upland soil. Plant and Soil, 291, 275–290. Steiner C, Das KC, Garcia M, F€ orster B, Zech W (2008a) Charcoal and smoke extract stimulate the soil microbial community in a highly weathered xanthic ferralsol. Pedobiologia, 51, 359–366. Steiner C, Glaser B, Geraldes Teixeira W, Lehmann J, Blum WE, Zech W (2008b)

biochar on acid black soil nutrient, soybean root and yield. Advanced Materials Research, 524–527, 2278–2289. Young MJ, Johnson JE, Abrams MD (1996) Vegetative and edaphic characteristics on relic charcoal hearths in the Appalachian mountains. Vegetatio, 125, 43–50. Yu L, Tang J, Zhang R, Wu Q, Gong M (2012) Effects of biochar application on soil methane emission at different soil moisture levels. Biology and Fertility of Soils, 48, 1–10.

Nitrogen retention and plant uptake on a highly weathered central Amazonian ferralsol amended with compost and charcoal. Journal of Plant Nutrition and Soil Science, 171, 893–899. Stoms DM, Davis FW, Jenner MW, Nogeire TM, Kaffka SR (2012) Modeling wildlife and other trade-offs with biofuel crop production. GCB Bioenergy, 4, 330–341. Streubel D, Collins P, Garcia-Perez M, Tarara J, Granatstein D, Kruger E (2011) Influence of contrasting biochar types on five soils at increasing rates of application.

Yuan , H , Xu K (2010) The amelioration effects of low temperature biochar generated from nine crop residues on an acidic ultisol. Soil Use and Management, 27, 110–115. Yuan JH, Xu , RK , Li J-Y (2011a) Amendment of acid soils with crop residues and biochars. Pedosphere, 21, 302–308. Yuan J-H, Xu R-K, Qian W, Wang R-H (2011b) Comparison of the ameliorating effects on an acidic ultisol between four crop straws and their biochars. Journal of Soils and Sediments, 11, 741–750.

Soil Science Society of America Journal, 75, 1402–1413. Sun DQ, Jun M, Zhang WM et al. (2012) Implication of temporal dynamics of microbial abundance and nutrients to soil fertility under biochar application – field experiments conducted in a brown soil cultivated with soybean, north China. Advanced Materials Research, 518-523, 38, 4–394. Taghizadeh-Toosi A, Clough TJ, Condron LM, Sherlock RR, Anderson CR, Craigie RA

Zackrisson O, Nilsson MC, Wardle DA (1996) Key ecological function of charcoal from wildfire in the boreal forest. Oikos, 77, 10–19. Zhang A, Cui L, Pan G et al. (2010) Effect of biochar amendment on yield and methane and nitrous oxide emissions from a rice paddy from Tai Lake plain, China. Agriculture, Ecosystems and Environment, 139, 469–475. Zhang A, Bian R, Pan G et al. (2012a) Effects of biochar amendment on soil quality,

(2011) Biochar incorporation into pasture soil suppresses in situ nitrous oxide emissions from ruminant urine patches. Journal of Environment Quality, 40, 468–475. Taghizadeh-Toosi A, Clough TJ, Sherlock RR, Condron LM (2012) Biochar adsorbed ammonia is bioavailable. Plant and Soil, 350, 57–69. Tagoe SO, Horiuchi T, Matsui T (2008a) Effects of carbonized and dried chicken manures on the growth, yield, and N content of soybean. Plant and Soil, 306, 211– 220.

crop yield and greenhouse gas emission in a Chinese rice paddy: a field study of 2 consecutive rice growing cycles. Field Crops Research, 127, 153–160. Zhang A, Liu Y, Pan G, Hussain Q, Li L, Zheng J, Zhang X (2012b) Effect of biochar amendment on maize yield and greenhouse gas emissions from a soil organic carbon poor calcareous loamy soil from central China plain. Plant and Soil, 351, 263–275. Zimmerman AR, Gao B, Ahn M-Y (2011) Positive and negative carbon mineralization priming effects among a variety of biochar-amended soils. Soil Biology and

Tagoe SO, Horiuchi T, Matsui T (2008b) Preliminary evaluation of the effects of carbonized chicken manure, refuse derived fuel and K fertilizer application on the growth, nodulation, yield, N and P contents of soybean and cowpea in the greenhouse. African Journal of Agricultural Research, 3, 759–774. Tanaka H, Kyaw M, Toyota K, Motobayashi T (2006) Influence of application of rice straw, farmyard manure, and municipal biowastes on nitrogen fixation, soil

Biochemistry, 43, 1169–1179. van Zwieten L, Kimber S, Morris S, Downie A, Berger E, Rust J, Scheer C (2010a) Influence of biochars on flux of N2O and CO2 from ferrosol. Australian Journal of Soil Research, 48, 555–568. van Zwieten L, Kimber S, Downie A, Morris S, Petty S, Rust J, Chan KY (2010b) A glasshouse study on the interaction of low mineral ash biochar with nitrogen in a

microbial biomass N, and mineral N in a model paddy microcosm. Biology and Fertility of Soils, 42, 501–505. Topoliantz S, Ponge JF (2005) Charcoal consumption and casting activity by Pontoscolex corethurus (Glossoscolecidae). Applied Soil Ecology, 28, 217–224.

sandy soil. Australian Journal of Soil Research, 48, 569–576. van Zwieten L, Kimber S, Morris S et al. (2010c) Effects of biochar from slow pyrolysis of paper mill waste on agronomic performance and soil fertility. Plant and Soil, 327, 235–246.

© 2012 Blackwell Publishing Ltd, GCB Bioenergy, 5, 202–214

214 L . A . B I E D E R M A N & W . S . H A R P O L E Supporting Information Additional Supporting Information may be found in the online version of this article: Table S1. Author and year of the publications used in the meta-analysis. The treatments include the addition of biochar (B), fertilizer (F), or both in a factorial combination (BFC) or if fertilizer was applied to all conditions (BFF). Lifespan refers to annual (A) or perennial (P) plants, if applicable. The remaining columns refer to the number of experiments within each manuscript that measure those response variables. Table S2. The number of experiments that use activated charcoal in a similar manner as those biochar studies in this meta-analysis and the results of the Wilcoxon rank sum tests comparing effect sizes of biochar (RRB) with activated charcoal. Table S3. Results from the ‘fail safe’ analysis: G is the number of studies where significance was not reported, k is the number of  k is the mean standard normal deviate of the k studies, and X studies that provided significance data for the variable of interest, Z is the number of nonsignificant studies that are necessary to reduce RRB to zero.

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