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 decom-
position, 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 leach-
ing. 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

decades to centuries (Lehmann et al., 2006; Novak et al.,

Introduction
2010; although see Wardle et al., 2008). One analysis esti-
Atmospheric CO2 concentration is nearly 400 ppm and mates that widespread use of biochar could mitigate up
continues to rise due to human activities, with conse- to 12% of current anthropogenic CO2 emissions (Woolf
quences to global climate, human health (Lafferty, 2009; et al., 2010).
Anderson et al., 2012), agriculture (Auffhammer et al., In addition to biochar’s potential to sequester recently
2012), and biodiversity (Bakkenes et al., 2002; Bellard fixed atmospheric carbon, its porous structure, high sur-
et al., 2012). Among the many proposed solutions to mit- face area, and affinity for charged particles (Keech et al.,
igate this increase in atmospheric carbon is to enhance 2005) interact with physical and biological components
long-term sequestration of carbon through the applica- of the soil (Glaser et al., 2002; Steiner et al., 2008a) and
tion of biochar to the soil (Marris, 2006; Lehmann, can have cascading effects throughout the ecosystem
2007b). Biochar is a carbon-rich coproduct resulting from (Hammes & Schmidt, 2009). Recent reviews have high-
pyrolyzing biomass under high-temperature, low oxy- lighted the benefits of adding biochar to agricultural
gen conditions for biofuel production (Lehmann, 2007a; soils (Glaser et al., 2002; Marris, 2006; Lehmann, 2007b;
Laird et al., 2009) and although it is similar to other char- Warnock et al., 2007). These benefits include the promo-
coals, biochar is defined by its intentional application to tion of plant growth (Chan et al., 2008; Asai et al., 2009;
the soil for environmental applications (Lehmann & Major et al., 2009; Graber et al., 2010; Hossain et al.,
Joseph, 2009). It contains highly condensed aromatic 2010), the improvement of soil water-holding capacity
structures that resist decomposition in soil and thus can (Laird et al., 2010b), diminishing disease incidence in
effectively sequester a portion of the applied carbon for crops (Matsubara et al., 2002; Elad et al., 2010; Elmer &
Pignatello, 2011), limiting the bioavailability of heavy
Correspondence: Lori A. Biederman, tel. 515-509-6346, metals (Park et al., 2011), reducing soil N2O emission
fax (515)-204-1337, e-mail: lbied@iastate.edu (Kammann et al., 2011; Taghizadeh-Toosi et al., 2011),

202 © 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 fertilizer and evaluated synergistic interactions (Glaser
can reduce fertilizer needs (Liang et al., 2006; Laird et al., 2002; Chan et al., 2008; Lau et al., 2008). The poten-
et al., 2010a). Because biochar is a coproduct of bioener- tial effects of accidental biochar exposure on nonagricul-
gy production and can contribute to carbon sequestra- tural species were assessed by comparing the responses
tion goals, while also simultaneously increasing yield of annual and perennial plant species and evaluating
and reducing fertilizer use, biochar has been touted as a the effect of biochar on soil organisms. Finally, because
‘win-win-win’ solution to meeting global environmental biochar as a product can be chemically highly variable,
challenges (Laird, 2008). we examined the ability of particular biochar character-
There is, however, considerable variation in plant and istics arising from feedstock and production methodolo-
soil responses to biochar that cannot be evaluated in a gies to influence plant growth to inform best use
single study and may be lost in the overall message of a practices.
literature review. Source material and pyrolysis condi-
tions introduce significant variation in the structure,
nutrient content, pH, and phenolic content of the bio-
Materials and methods
char products (Novak et al., 2009a). Interactions with cli-
mate, soil type (texture, chemistry, hydrology) (Tryon,
Literature search
1948; van Zwieten et al., 2010a), and fertilization status We conducted an exhaustive literature search in Web of Sci-
(van Zwieten et al., 2010b; Haefele et al., 2011) can also ence (thomsonreuters.com) and Google Scholar (scholar.google.
contribute to uncertainty in how biochar interacts with com) databases using the keywords ‘biochar’, ‘char’, ‘black car-
organisms. bon’, ‘charcoal’, and ‘agchar’ (most recent search, June 25,
There are also many concerns about the production of 2012). The literature cited sections of published literature
reviews (e.g., Glaser et al., 2002; Atkinson et al., 2010; Spokas
biochar and the release of this novel material into the
et al., 2011) were consulted for additional sources. For each
environment. In addition to apprehensions about food
identified article, we evaluated the title and abstract to deter-
prices and potential land-use changes due to its manu-
mine if it contained original data and measured the responses
facture and transport (Hill et al., 2006; Stoms et al., of interest (plant growth, soil nutrients, and soil organisms).
2012), it remains unclear if there will be negative exter- Those articles that met these criteria were examined in detail.
nalities associated with the widespread application of Although biochar specifically refers to pyrolyzed biomass
biochar. Specifically, there has been limited research on that is intentionally applied to the soil for environmental appli-
the impacts to nonagricultural species, such as soil cations (Lehmann & Joseph, 2009), we included charcoal
organisms and perennial plants that inhabit field mar- derived from hydrothermal carbonization (Rilling et al., 2010).
gins or other nontarget ecosystems, especially aquatic We excluded studies that examined the response to wildfire
systems. Effective implementation of biochar as a deposition and historical charcoal applications, such as those
found in ‘Terra Preta’ soils, because the exact nature and quan-
climate-mitigating tool would require the application of
tity of amendment material cannot be known. Those studies
vast quantities of biochar into the environment; expo-
that included soil contaminants, tested alleopathic interference,
sure of nontarget terrestrial and aquatic systems to bio-
averaged responses among different trials, or did not contain
char is likely as wind and water can translocate up to appropriate controls were also excluded. This process identi-
53% of applied biochar material during application fied 114 published articles.
(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 Data extraction
relatively few studies, a quantitative understanding of Data from ecosystem variables that were measured in more
its potential impacts to ecosystems is needed prior to its than five studies were extracted from the identified articles,
adoption as a major climate mitigation tool. including plant production and nutrient content, soil organism
We performed a comprehensive meta-analysis of pub- composition, and nutrient availability. Data concerning gas
lished studies that tested the effects of biochar on one or fluxes and process rates were outside the scope of this analysis.
more ecosystem functions including plant productivity, Within each article, data were divided into ‘experiments’ based
on differences in soil, biochar material, and/or plant species,
nutrient uptake, soil properties, and on ecosystem ser-
resulting in 371 independent experiments (Supplemental table
vices, such as crop yield. Our primary question was to
1). Different application rates of biochar and supplemental
ask whether the central tendencies in the published
nutrient addition (inorganic and organic) were considered vari-
empirical literature supported the often-enthusiastic ables within an experiment.
claims of previous reports (Marris, 2006; Lehmann, During data extraction, we selected treatments and experi-
2007a; Kleiner, 2009). Furthermore, because the effects mental conditions that were most representative of normal field
of biochar have been described as analogous to effects conditions. For example, if soil organisms were manipulated
of fertilization, we compared the effect of biochar vs. within an experiment only data from nonsterilized soils were

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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 observed effect of adding both biochar and fertilizer, using a
data of repeated measurements and nutrient data from the one-sided Wilcoxon rank sum test. Second, for those cases
uppermost soil layer. We also had to manipulate data pre- where fertilizer was applied to both control and biochar condi-
sented to allow for comparisons. In 43% the experiments, the tions, we used a Wilcoxon signed rank test to determine if RRBFF
biochar application rate was presented as mass per area, these was different from zero. We compared biochar’s effect on
data were converted to percent volume, assuming a soil bulk annual and perennial plants by comparing productivity
density of 1.5 g cm 3 unless otherwise provided. pH values responses (RRB) using Wilcoxon rank sum tests.
measured with CaCl2 were made comparable with pH Our ability to assess how site conditions interact with bio-
measured with distilled water using the formula pH- char was limited by the lack of consistent reporting of biochar
H2O = 1.65 + (0.86*pH-[CaCl2]) (Augusto et al., 2008). Produc- chemistry and soil characteristics among studies and it was
tivity data from plants grown in a mixed-species community only possible to analyze those variables with more than 100
were summed. The ratio of aboveground-to-belowground tis- studies: aboveground productivity and pH. The mean RRB for
sue and total biomass were also calculated in those cases where biochars of different source materials were compared with ANO-
both above- and belowground data were reported. We also VA, and the effects of latitude, pyrolysis temperature, and C : N
obtained auxiliary information whenever possible, including ratio were determined using regression. We used robust stan-
experimental setting, study length, fertilizer type, soil nutrients dard errors for regressions using pH to correct for heteroske-
and pH, biochar composition, feedstock source, pyrolysis con- dastity.
ditions, and activation status. The target organisms’ functional Many literature reviews of biochar effects, such as Lehman
group was noted and if it is plant, we recorded its life span. et al. (2011), Atkinson et al. (2010), and Spokas et al. (2011),
We used the natural log-transformed response ratio as a include activated charcoal within their broader definition of bio-
measure of effect size (Hedges et al., 1999; Lajeunesse & Forbes, char. We compared the response ratios (RRB) of our biochar data
2003): RRX = ln (T/C), where T is the measured value of the with response ratios from studies that used activated charcoals
response variable to treatment X [biochar (B), fertilizer (F), or (Ridenour & Callaway, 2001; Kulmatiski & Beard, 2006; Chan
both (BF)] and C is the value in the untreated soils – the con- et al., 2008; Lau et al., 2008; Weißhuhn et al., 2009; Wurst et al.,
trol. For those studies where fertilizer was added to both the 2010; Hale et al., 2011; Hass et al., 2012; Rajkovich et al., 2012),
control and biochar treatments, the response ratio was modi- and used Wilcoxon rank sum tests to determine if the responses
fied RRX = ln (BF/F). We used RRBFC and RRBFF to distinguish of these two products are similar (Supplemental table 2).
between the true factorial conditions and those where all treat- To evaluate the potential of bias introduced from unpub-
ments receive fertilizer, respectively. With the exception of the lished data we estimated the hypothetical number of unre-
analysis of biochar rate (described below), we calculated the ported zero effect studies needed to produce a nonsignificant
mean response to material application prior to calculating RRX overall effect (Rosenthal, 1979; Harpole et al., 2007). This ‘fail-
when studies included multiple biochar (n = 20) or fertilizer safe’ number is calculated as X = (k/2.706) [k(Z
k )2 – 2.706].
application rates. To ensure that our results were not affected Where k is the number of studies that measured the variable of
by this decision, we calculated a response ratio using the maxi- interest, and Z
k is the mean of the normalized standard devia-
mum response and compared it with the mean response sce- tions of the k studies. We excluded studies that did not report
nario and they were not significantly different. the significance of their data. A conservative estimate of
The effect of biochar application rate on aboveground pro-
= 1.645 can be used for studies with significant effects
Z
ductivity was calculated in a manner similar to RRB, but in this (P < 0.05) and Z
= 0 for studies reporting nonsignificant
case the response to biochar was calculated for each reported responses to biochar (Supplementary table 3).
biochar application rate, rather than averaged over all applica-
tion amounts. The slope of each of the response surfaces was
determined. Results
The addition of biochar to soils resulted in increased
Analysis aboveground productivity (P < 0.01), crop yield (P <0.01),
All statistical analyses and graphical presentation were per- SMB (P < 0.01), rhizobia nodulation (P < 0.05), plant K
formed in R 2.12.2 and the ggplot2 package (Wickham, 1999; R tissue concentration (P < 0.05), soil P (P < 0.001), soil K
Development Core Team, 2011). Because the data distributions (P < 0.001), total soil N (P < 0.001), and total soil C
tended to be slightly skewed, we used nonparametric tests. (P < 0.001), on average, compared with control condi-
To determine if biochar significantly affected ecosystem vari- tions (Fig. 1; RRB > 0). Also, on average, soil pH
ables, we used Wilcoxon signed rank tests to compare the mean increased, or became less acidic, with biochar addition
RRB with zero. We used paired Wilcoxon signed rank tests to
(P < 0.001). Those variables that showed no significant
compare the effect size of biochar with that of fertilizer (RRB vs.
mean effect of biochar included belowground produc-
RRF). To determine if there was a superadditive effect of apply-
tivity, aboveground : belowground biomass ratio, per-
ing both biochar and fertilizer we used two tests to determine if:
First, for factorial application studies we calculated a test statis- cent mycorrhizal colonization of roots, plant tissue N
tic (θ) from the original data [θ = ln ((biochar/control) + (fertil- and P concentration, and soil inorganic N.
izer/control))] that represents the potential additive effect of The effect size of aboveground productivity did not
adding both materials. We compared θ with RRBFC, or the change as biochar application rate increased (Fig. 2).

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 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

different than the additive expectation ( ). In those stud-

** n = 67
ies where fertilizer was added to all treatments (RRBFF),
Aboveground
aboveground productivity (P < 0.01), crop yield
Belowground ns n = 28 (P < 0.001), plant tissue K concentration (P < 0.01), pH
Above:below ratio ns n = 21 (P < 0.005), and soil total C (P < 0.01) increased signifi-
cantly with biochar.
Yield ** n = 30
Belowground biomass in perennial plants did not
SMB ** n = 16 change in biochar treatments, which was significantly
(P < 0.01) different than the belowground response by
Rhizobia nodules * n=6
annual plants (Fig. 3). This difference contributed to a
% mycorrhizae col. ns n = 23 significantly smaller total productivity for perennial
plants in biochar-treated soils (P < 0.001). Perennial and
Tissue N conc. ns n = 25
annual plants did not differ in aboveground productiv-
Tissue P conc. ns n = 21 ity and the ratio of aboveground : belowground tissue
Tissue K conc. * n = 12
in response to biochar.
Aboveground productivity RRB varied significantly
Soil inorganic N ns n = 33 with latitude (adj. R2 = 0.095, P < 0.01); the effect size of
Soil P *** n = 53 biochar was more positive in the tropical regions than
in temperate zones (Fig. 4). There was also a significant
Soil K *** n = 31
effect (P < 0.01) of feedstock source of the biochar mate-
pH *** n = 146 rial on aboveground productivity: grass- and manure-
origin biochars increased productivity compared with
Total N *** n = 39
control conditions (Fig. 5a) and forb-origin biochar
*** n = 26
Total C reduced productivity, although there were limited data
for this class of biochar. The C : N ratio of the biochar
–0.5 0.0 0.5 1.0 1.5 source had no predictable effect on productivity (adj.
RRB R2 = 0, P = 0.96) (Fig. 5b). Higher pyrolysis temperature
biochars produced greater effects (adj. R2 = 0.076,
Fig. 1 The relative effect size (mean  CI) of biochar treat- P < 0.05) (Fig. 5c) and the pH of the biochar product
ments (RRB) on a range of ecosystem variables. Significance of significantly influenced aboveground productivity (adj.
Wilcoxon signed rank tests: *P < 0.05, **P < 0.01, ***P < 0.001. R2 = 0.172, P < 0.01), with alkaline biochars having a
more pronounced positive effect than acidic biochars
However, the variation around the mean response at (Fig. 5d). The change in soil pH following the applica-
each application rate, as measured by standard error, tion of biochar is a function of both the initial soil pH
increased with application rates greater than 0.5%. In (adj. R2 = 0.069, P < 0.01) and the pH of the biochar
the 20 studies that reported multiple biochar application (adj. R2 = 0.139, P < 0.001). Acidic soils showed a
rates the overall mean (CI) response slope was greater positive response to biochar than alkaline soils.
0.002  0.181, indicating no clear relationship between The effect of biochar on soil pH was greater for alkaline
productivity and biochar application rate. Of those 20 biochars. Both biochar and activated charcoal affected
studies, 8 had negative slopes (< 0.02), meaning the the ecosystem variables similarly. The average length of
addition of more biochar reduced productivity, 10 had the studies analyzed was 113.4 days and the longest
positive slopes (>0.02) meaning increasing biochar study was 3 years.
application increased productivity, and 2 studies had For most variables, the number of hypothetical stud-
flat slopes ( 0.02 to 0.02) suggesting no effect of increas- ies necessary to overturn the results of the meta-analysis
ing biochar application rate. was sufficiently large that our results are unlikely to be
The average effect size of fertilization was signifi- biased by unreported null responses (Supplemental
cantly greater than that of biochar addition for above- table 3). For example, at least 1172 unreported null-
ground productivity (P < 0.01), yield (P < 0.05), and soil response studies would be needed to cause the overall
P (P < 0.01) when compared with control conditions mean effect of biochar on aboveground productivity to
(Table 1 and Fig. 1). Biochar addition, however, was be nonsignificant. For SMB, rhizobia nodules, and tissue
more effective than fertilization at increasing plant tis- nutrient concentration, however, the number of hypo-
sue P (P < 0.05) and K (P < 0.05) concentration. For all thetical unreported nonsignificant studies that would
variables except soil total C (P < 0.001), the addition of cause an overall nonsignificant mean effect would be
both biochar and fertilizer (RRBFC) was not significantly less than 25.

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

Standard error
2

RRB aboveground

2
0.02% 0.14% 1% 7.4% 54.6%

4 2 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. Experi-
ments 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.

duction variables of the biochar (Hass et al., 2012), and is

Discussion
short lived, as the nutrients are used by plants and/or
In our meta-analysis of 371 independent experiments are leached from the soil (Steiner et al., 2007; Major et al.,
we find that despite variability introduced by soil type, 2010). Long-term effects of biochar on nutrients occur
climate, and production methods, the average effect of through complex physiochemical reactions with soil par-
biochar on various ecosystem properties was neutral to ticles (Spokas et al., 2011). One such reaction that affects
positive. This is consistent with previous reviews P is biochar-induced increases in soil alkalinity (liming).
reporting the beneficial aspects of this product (Leh- In acidic soils phosphorus can be adsorbed onto iron oxi-
mann et al., 2006; Atkinson et al., 2010). Most impor- des, which makes it unavailable to plants. Liming agents
tantly for agricultural systems, aboveground production reduce the concentration of iron and aluminum in the
and yield were increased in biochar-treated soils. soil solution and the previously bound phosphorus then
Biochar has been shown to promote plant productivity becomes available (Cui et al., 2011). Liming also reduces
and yield though several mechanisms. Physical condi- the mobility of toxic elements, such as Al and Cd
tions change with biochar; its dark color alters thermal (Ritchey & Snuffer, 2002; Hass et al., 2012). Changes in
dynamics and facilitates rapid germination, allowing plant productivity with biochar pH support this mecha-
more time for growth compared with controls (Genesio nism; alkaline biochars are more effective at increasing
et al., 2012). Biochar can also improve soil water-holding biomass than acidic biochars (Fig. 5d). Biochar was also
capacity (Laird et al., 2010b), facilitating biomass gain most effective at changing soil pH in acidic soils, which
(Kammann et al., 2011). Plant growth can also be affected would be particularly beneficial in low latitudes (Fig. 4)
by biochar-induced changes in soil nutrient conditions, where soils are acidic and agriculture is limited by P
particularly the cycling of P and K (Dempster et al., availability (Steiner et al., 2008b).
2012a,b; Taghizadeh-Toosi et al., 2012). In this analysis, Another way biochar may affect soil nutrients is
we found that plant tissue K concentration and soil P through the reduction in leaching losses (Laird et al.,
and K increased following biochar application (Fig. 1). 2010a). Biochar’s porous structure, large surface area,
These nutrients may be directly introduced to the soil and negative surface charge (Bird et al., 2008; Cheng
through labile organic compounds associated with bio- et al., 2008; Downie et al., 2009; Novak et al., 2009a)
char and become available as these compounds weather increase the soil’s cation exchange capacity and allow
(Topoliantz & Ponge, 2005; Yamato et al., 2006; Rajkovich for the retention of nutrients, such as K (Liang et al.,
et al., 2012). This effect, however, depends on the pro- 2006; Major et al., 2011). Biochar can also slow cation

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Table 1 The mean (CI) effect size for the fertilizer (RRF) and Annuals
fertilizer plus biochar treatments (RRBFC and RRBFF). Bold val-
Perennials

1.5
ues 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

1.0
values indicate a significant difference from zero

RRF RRBFC h RRBFF

Aboveground 0.65  0.23 0.96  0.29 1.22 0.18  0.1

0.5
Belowground 0.64  0.74 1.38  1.4 1.48 0.23  0.18
Above : 0.41  0.7 0.56  0.69 0.95 0.03  0.18

RRB
below ratio
Yield 0.69  0.35 0.83  0.37 1.18 0.35  0.16
SMB 0.31  0.45 0.48  0.62 0.92 0.05  0.52

0.0
Rhizobia 0.21  0.1 0.55  0.33 0.89 Insufficient
nodules data
% Mycorrhizae 0.05  0.25 0.21  0.14 0.78 0.22  0.18
col.

−0.5
Tissue N conc. 0.25  0.17 0.23  0.17 0.84 0.06  0.16
Tissue P conc. 0.05  0.07 0.08  0.15 0.76 0.09  0.12 n = 51 n = 16 n = 14 n = 14 n = 11 n = 10 n = 15 n = 10

Tissue K conc. 0.04  0.08 0.39  0.25 0.76 0.08  0.08

Aboveground Belowground Above:below Total biomass
Soil inorganic N 3.83  1.03 0.55  1.16 1.06 0.00  0.19
ns ** ns ***
Soil P 1.43  0.73 1.66  0.73 2.16 0.21  0.41
Soil K 0.23  0.2 0.66  0.37 1.15 0.51  0.33 −1.0
pH 0.002  0.03 0.11  0.04 0.76 0.08  0.03
Soil total N 0.04  0.08 0.33  0.12 0.89 0.13  0.16
Fig. 3 The relative effect size (mean  CI) of biochar treat-
Soil total C 0.11  0.08 1.27  0.27 0.93 0.94  0.51
ments (RRB) for annual and perennial plant productivity. Sig-
nificance of Wilcoxon signed rank tests: *P < 0.05, **P < 0.01,
***P < 0.001.
loss by inducing a shift in soil water nutrient transport
from bypass to matrix flow (Laird et al., 2010a). Nutri-
ents, such as P, can be adsorbed to biochar’s surface,
which slows leaching (Laird et al., 2010a; Beck et al.,
2011).
2

The analysis of application rate provided little insight

into how biochar maybe best applied; there was no
obvious threshold or trend with increasing application
RRB − aboveground

rates (Fig. 2). Variability in plant response, however,

1

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);
0

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

Biochar–fertilizer interactions
0 10 20 30 40 50
Although biochar altered the soil nutrient environment
Degree latitude
and promoted plant growth, it is effects are not equiva-
lent to that of fertilizer, as fertilizer alone was more Fig. 4 The relative effect size of biochar treatments (RRB) for
effective for improving plant productivity and soil P aboveground productivity as a function of latitude. (Adj.
(Table 1). Furthermore, unlike in the fertilizer treat- R2 = 0.079, P < 0.01).

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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 bio- zadeh-Toosi et al., 2012). Soil type and existing soil N
char treatments. Plants typically respond to improved status are strong controls on soil N cycling and because
nutrient conditions by reducing the allocation of tissue this meta-analysis generalizes across a wide range of
belowground (Brouwer, 1962; Poorter & Nagel, 2000), soils these effects may be masked. There were, however,
and a lack of change following biochar exposure sug- increases in total soil N, presumably because the N
gests that it is not similarly alleviating belowground within the structure of the biochar material contributed
competition for nutrients. In contrast, biochar amend- to this pool, but is unavailable to plants and microbes.
ments were better than fertilizer at increasing plant P
and K tissue concentrations. As explained above, bio-
Effects on perennial species and soil organisms
char can improve the availability of these nutrients
through soil liming and by reducing leaching losses. Belowground, annual plants responded positively to
Despite the differential effects of these materials, how- biochar, whereas perennial species (including native
ever, there was limited evidence of a superadditive or and naturalized grasses and forbs, forage crops, and
synergistic effect when both biochar and fertilizer are sugar cane) had no response and the difference between
applied. these two life forms was significant (Fig. 3). Rather than
Our analysis finds that biochar’s effects on N are lim- producing differences in tissue allocation, biochar
ited, as both soil available N and the concentration of N affects overall plant productivity; increasing it for
in plant tissues were unaffected by its application. Fur- annual plants and with limited effect on perennials.
thermore, aboveground productivity did not change There was also considerable variability in plant
with the nitrogen content of the biochar, as measured response, especially for annual plants belowground.
by C : N ratio. This contradicts studies that find com- Numerous volatile and biologically active compounds,
plex interactions between fertilizer, biochar, and the N such as ethylene, butyric acids, benzoic acid, quinones,
cycle (DeLuca et al., 2006; Laird et al., 2010a; Taghi- and 2-phenoxyethanol, are introduced into the soil with

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 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., a net loss of carbon to the atmosphere (Wardle et al.,
2010) and depending on concentration, these com- 2008; Rogovska et al., 2011). Recent studies, however,
pounds may promote growth, or produce toxic effects have found priming to be negligible in soils that are
(Keely & Pizzorno, 1986; Elad et al., 2010; Meller Harel unaffected by phenolic compounds (Bell & Worrall,
et al., 2012). Differences in allocation and phenology, 2011; Jones et al., 2011; Zimmerman et al., 2011).
such as higher growth rates in annual species (Pitelka,
1977), may contribute to functional group sensitivity to
Biochar characteristics
these compounds. Documented changes following his-
torical charcoal applications (not included in the analy- The net ability of biochar to enhance ecosystem services
sis) underscore biochar’s potential effect on plant depends, in part, on the specific qualities of the biochar
community composition (Chidumayo, 1988). For exam- and site conditions (Haefele et al., 2011). Within the lit-
ple, annual weed cover and legume density was erature surveyed there was little uniformity on the pro-
increased, and perennial sprouting reduced, on Terra duction methods of biochar; materials were created in a
Preta soils compared with adjacent nonaffected areas range of pyrolyzers from highly sophisticated industrial
(Major et al., 2005). Plant species composition is also equipment to primitive earthen mounds. Temperature
affected by the alkaline soils and altered calcium con- conditions also varied, and there was no precise defini-
centrations found in former charcoal production areas tion of terminology, such as the time and temperature
(Mikan & Abrams, 1995; Young et al., 1996). conditions of ‘fast’ or ‘slow’ pyrolysis processes (Mohan
Biochar has variable effects on plant-associated soil et al., 2006). Furthermore, the reporting of production
microbes. Root nodulation by rhizobia generally (feedstock source, time and temperature of pyrolysis,
increased (Fig. 1), presumably because conditions asso- kiln type) variables and the resulting qualities (pH,
ciated with efficient N-fixation, such as slightly alkaline C : N ratio, and nutrient content) of the biochars was
soil and access to P, have improved (Graham, 1981; inconsistent and there were few data available to
Rondon et al., 2007; Lehman et al., 2011). In contrast, correlate with the variables of interest. Because pyroly-
biochar did not significantly alter root colonization by sis conditions affect the behavior of biochar in the soil
mycorrhizal fungi, although the wide confidence inter- (Bruun et al., 2012), the lack of data limits our ability to
vals suggest that there is considerable variability. Bio- understand biochar’s interaction with soil and its organ-
char changes the plant’s nutrient environment, isms (Spokas et al., 2011).
increasing P availability for example, and this may There was considerable variation in how feedstock
reduce plant dependence on mycorrhizae (Raznikiewicz source influences aboveground productivity (Fig. 5);
et al., 1994). Biochar could also affect the adsorption and biochars from grass and manure/sewage increased
desorption of signaling compounds that would other- aboveground productivity. This was unexpected given
wise promote root–fungi connections (Akiyama et al., the reputation of grass- and manure-sourced biochars
2005; Warnock et al., 2007). for producing unpredictable effects due to high concen-
Biochar application increased total soil C, thus it con- trations of silicates (Lehman et al., 2011). We also found
tributes to the sequestration of carbon at least in the that biochars produced at higher temperatures were
short term (3 years) (Fig. 1). Although much of this car- more effective at promoting aboveground productivity.
bon sequestration is due to the inert portions of the bio- High-temperature biochars tend to be alkaline (Bagreev
char material, there was also an increase in SMB, et al., 2001; Novak et al., 2009b) and contain less biologi-
another soil carbon pool. Biochar can contribute to SMB cally active volatile compounds (Gundale & DeLuca,
through various mechanisms. It augments the availabil- 2006; Hale et al., 2012) that can otherwise limit plant
ity of micropore habitat providing refugia for soil growth. High-temperature biochars are also more resis-
microbes from larger fauna, thus increasing microbe tant to decomposition and would, therefore, be better
population size (Zackrisson et al., 1996; Pietik€ainen et al., candidates to fulfill the C sequestration function (Novak
2000). Labile organic compounds, a by-product of the et al., 2010; Harvey et al., 2012).
production process, are introduced to the soil with bio-
char and decompose readily. Microbial food resources
Future research needs and environmental concerns
are also enhanced by the retention of native dissolved
organic matter on the charged surface of biochar (Steiner We found that the addition of biochar generally
et al., 2008a; Deenik et al., 2010) and through biochar- improves, or at least does not harm, many aspects of
induced increases in plant productivity (Graber et al., the ecosystem and its functioning, including plant pro-
2010; Jones et al., 2012). It is also possible that biochar ductivity and soil nutrient content. This is consistent
addition could increase microbe populations by ‘prim- with the findings of other nonquantitative reviews
ing’ the decomposition of native soil carbon, leading to (Glaser et al., 2002; Marris, 2006; Lehmann, 2007b;

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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 Beck DA, Johnson GR, Spolek GA (2011) Amending greenroof soil with biochar to
affect runoff water quantity and quality. Environmental Pollution, 159, 2111–2118.
goals for carbon sequestration, such as 12% of current Beesley L, Moreno-Jimenez E, Gomez-Eyles JL (2010) Effects of biochar and green-
anthropogenic CO2 emissions (Woolf et al., 2010), large waste compost amendments on mobility, bioavailability and toxicity of inorganic
quantities of biochar would have to be applied to a sig- and organic contaminants in a multi-element polluted soil. Environmental Pollu-
tion, 158, 2282–2287.
nificant portion of the earth’s arable land. Because of Bell MJ, Worrall F (2011) Charcoal addition to soils in NE England: a carbon sink
the ability of applied biochar to be transported by wind with environmental co-benefits? Science of the Total Environment, 409, 1704–1714.
and water, nontarget organisms will be affected by this Bellard C, Bertelsmeier C, Leadley P, Thuiller W, Courchamp F (2012) Impacts of cli-
mate change on the future of biodiversity. Ecology Letters, 15, 365–377.
activity, but there are limited data available for bio- Berglund M, DeLuca H, Zackrisson O (2004) Activated carbon amendments to soil
char’s effects on nonagricultural species, including alters nitrification rates in scots pine forests. Soil Biology and Biochemistry, 36, 2067
native plant communities, aquatic systems, and soil –2073.
Bird MI, Ascough PL, Young IM, Wood CV, Scott AC (2008) X-ray microtomograph-
organisms. For example, only 16 studies have tested ic imaging of charcoal. Journal of Archaeological Science, 35, 2698–2706.
biochar effects on perennial plants and relatively few Birk JJ, Steiner C, Teixiera WC, Zech W, Glaser B (2009) Microbial response to char-
studies are needed to overturn the positive findings for coal amendments and fertilization of a highly weathered tropical soil. In: Amazo-
nian Dark Earths: Wim Sombroek’s Vision (eds Woods WI, Teixeira WJ, Lehmann J,
rhizobia and SMB. Changes in community composition Steiner C, WinklerPrins AMGA, Rebellato L), pp. 309–324. Springer Sci-
following biochar application are also very limited and ence + Business Media, Berlin.
the different responses by annual and perennial plants 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 agro-
demonstrate that we still do not understand the mecha- nomic and economic perspective. Australian Journal of Soil Research, 48, 531–545.
nism by which it interacts with organisms. Perennial Bolster CH, Abit SM (2012) Biochar pyrolyzed at two temperatures effects Escherichia
plants and soil creatures perform many critical ecosys- 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
tem services, such as erosion prevention and pest pre- mineral-nutrition properties of sand-based turfgrass root zones amended with
dation, in agricultural systems. It is imperative that we biochar. Agronomy Journal, 102, 1627–1631.
understand how biochar interacts with all aspects of the Brouwer R (1962) Nutritive influences on the distribution of dry matter in the plant.
Journal of Agricultural Science, 10, 399–408.
environment prior to its widespread application. Bruun W, M€ uller-St€
over D, Ambus P, Hauggaard-Nielsen H (2011) Application of bio-
char to soil and N2O emissions: potential effects of blending fast-pyrolysis biochar
with anaerobically digested slurry. European Journal of Soil Science, 62, 581–589.
Acknowledgments 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 Agricul- chemistry, 46, 73–79.
ture for funding this project, Joseph Garrison, Erich Sneller, Chan KY, Van Zwieten L, Meszaros I, Downie A, Joseph S (2007) Agronomic values
and Emily Zimmerman for assistance, and Dean Adams and of greenwaste biochar as a soil amendment. Australian Journal of Soil Research, 45,
David Laird for technical advice. 629–634.
Chan KY, van Zwieten L, Meszaros , I , Downie A, Joseph S (2008) Using poultry lit-
ter biochars as oil amendments. Australian Journal of Soil Research, 46, 437–444.
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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), fertil-
izer (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 mea-
sure those response variables.
Table S2. The number of experiments that use activated charcoal in a similar manner as those biochar studies in this meta-analy-
sis 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
studies that provided significance data for the variable of interest, Z
k is the mean standard normal deviate of the k studies, and X
is the number of nonsignificant studies that are necessary to reduce RRB to zero.

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