Effects of Biochar on Fluxes and Turnover of Carbon in Boreal Forest Soils

Abstract

Core Ideas
We tested the effects of different addition rates (0, 0.5, and 1.0 kg m⁻²) of wood‐derived biochar (pyrolysis temperatures 650°C) on the fluxes and turnover rates of soil C in a boreal forest in southern Finland.
Biochar amendments significantly increased soil total organic C stocks, C/N ratio, and moisture content, whereas the impacts of biochar on soil N concentration and temperature sensitivity (Q10) of soil organic matter decomposition were not clear.
Our results suggest that biochar addition doesn't accelerate the mineralization of soil organic C and could lead to larger stable C stocks in the surface soil layer.

Biochar has been used in different ecosystems to mitigate greenhouse gas emissions and increase C sequestration. However, the impacts of biochar addition in cold environments, such as boreal forests, are still poorly understood. We tested the effects of different addition rates (0, 5, and 10 Mg ha–1) of wood‐derived biochar (pyrolysis temperature 650°C) on the fluxes and turnover rates of soil C in a boreal forest in southern Finland. Biochar amendments significantly increased soil total organic C (TOC) stocks, C/N ratio, and moisture content, whereas the impacts of biochar on soil N concentration and the temperature sensitivity (Q10) of soil organic matter decomposition were not clear. Significantly lower values of TOC and total N (TN) were observed in the moss and organic layer in the 5 Mg ha–1 biochar plots, however, in the mineral layer, there were no differences in C and N content between the treatments. We found a slight but statistically nonsignificant increase in soil respiration after biochar addition which increased with the amount of biochar added into the soil. However, the soil C turnover time was similar in biochar plots and control plots. We also observed a slight but statistically nonsignificant decrease in the instantaneous C fluxes normalized by the amount of C in the soil during the incubation which decreased with the application rates of biochar. Our results suggest that biochar addition doesn't accelerate the mineralization of soil organic C and could lead to larger stable C stocks in the surface soil layer. Thus, it seems that biochar is a promising tool to enhance the C sequestration in boreal forest soils.

Full text

Soil Science Society of America Journal
Soil Sci. Soc. Am. J.
doi:10.2136/sssaj2018.04.0149
Received 19 Apr. 2018.
Accepted 18 Sept. 2018.
*Corresponding author (zhaopeng1988@cau.edu.cn).
© Soil Science Society of America, 5585 Guilford Rd., Madison WI 53711 USA. All Rights reserved.
Effects of Biochar on Fluxes and Turnover
of Carbon in Boreal Forest Soils
Soil Biology & Biochemistry
Biochar has been used in different ecosystems to mitigate greenhouse gas
emissions and increase C sequestration. However, the impacts of biochar addi-
tion in cold environments, such as boreal forests, are still poorly understood.
We tested the effects of different addition rates (0, 5, and 10 Mg ha–1) of
wood-derived biochar (pyrolysis temperature 650°C) on the uxes and turn-
over rates of soil C in a boreal forest in southern Finland. Biochar amendments
signicantly increased soil total organic C (TOC) stocks, C/N ratio, and mois-
ture content, whereas the impacts of biochar on soil N concentration and the
temperature sensitivity (Q10) of soil organic matter decomposition were not
clear. Signicantly lower values of TOC and total N (TN) were observed in the
moss and organic layer in the 5 Mg ha–1 biochar plots, however, in the mineral
layer, there were no differences in C and N content between the treatments.
We found a slight but statistically nonsignicant increase in soil respiration
after biochar addition which increased with the amount of biochar added into
the soil. However, the soil C turnover time was similar in biochar plots and
control plots. We also observed a slight but statistically nonsignicant decrease
in the instantaneous C uxes normalized by the amount of C in the soil dur-
ing the incubation which decreased with the application rates of biochar. Our
results suggest that biochar addition doesn’t accelerate the mineralization of
soil organic C and could lead to larger stable C stocks in the surface soil layer.
Thus, it seems that biochar is a promising tool to enhance the C sequestration
in boreal forest soils.
Abbreviations: AIC, Akaike information criteria; CN, soil C/N ratio; Q10, soil
organic matter decomposition; SOM, soil organic matter; SWC, soil water con-
tent; TOC, total organic C; TN, total nitrogen; TR, treatment;
Biochar is charcoal produced by heating biomass in conditions with low
oxygen concentration. It is carbon-rich and structurally resistant to de-
composition caused by fused aromatic structures (Kumar et al., 2005;
Schimmelpfennig and Glaser, 2012). Thus, the production of biochar, in combi-
nation with its storage in soils, has been suggested as one possible way to reduce C
emissions, sequester C into the soil, and reduce the atmospheric CO2 concentra-
tion (Lehmann et al., 2006; Woolf et al., 2010). Black carbon, a type of pyrogenic
carbon formed in forest fires in natural conditions, has been found to be the oldest
fraction of C in soils compared even with the most protected C in soil aggregates
and organo-mineral complexes (Pessenda et al., 2001). This C, can persist in soil
for millennia (Kuzyakov et al., 2009). Recently, the application of industrially pro-
duced charcoal from biomass (biochar) in soils has become more common, espe-
cially in agriculture (Baronti et al., 2014; Lu et al., 2014; Ventura et al., 2014; Pei et
al., 2017). It has the potential to improve soil properties and enhance soil microbial
activity and water holding capacity (Yu et al., 2013). Although many studies have
been conducted to assess the effects of biochar addition into the soil mainly in
agricultural ecosystems, few have investigated the effects of newly added biochar
Peng Zhao*
Dep. of Environmental and Biological
Sciences, Univ. of Eastern Finland,
Yliopistonranta 1 E (P.O. Box 1627),
70211 Kuopio, Finland
and
Center for Agricultural Water Research
in China, China Agricultural Univ.,
100083 Beijing, China
Marjo Palviainen
Kajar Köster
Dep. of Forest Sciences, Univ. of
Helsinki, Latokartanonkaari 7
(P.O. Box 27), 00014 Helsinki, Finland
Frank Berninger
Dep. of Environmental and Biological
Sciences, Univ. of Eastern Finland,
Yliopistokatu 7 (P.O. Box 111),
80101 Joensuu, Finland
Viktor J. Bruckman
Commission for Interdisciplinary
Ecological Studies,
Austrian Academy of Sciences (ÖAW),
Dr. Ignaz Seipel-Platz 2,
1010 Vienna, Austria
Jukka Pumpanen
Dep. of Environmental and Biological
Sciences, Univ. of Eastern Finland,
Yliopistonranta 1 E (P.O. Box 1627),
70211 Kuopio, Finland
Core Ideas
•We tested the effects of different
addition rates (0, 0.5, and 1.0 kg m−2)
of wood-derived biochar (pyrolysis
temperatures 650°C) on the uxes
and turnover rates of soil C in a
boreal forest in southern Finland.
•Biochar amendments signicantly
increased soil total organic C stocks,
C/N ratio, and moisture content,
whereas the impacts of biochar on
soil N concentration and temperature
sensitivity (Q10) of soil organic matter
decomposition were not clear.
•Our results suggest that biochar
addition doesn’t accelerate the
mineralization of soil organic C and
could lead to larger stable C stocks in
the surface soil layer.
Published online December 27, 2018

∆ Soil Science Society of America Journal
in forested ecosystems, such as the decomposition of the large
old soil organic matter (SOM) pool. However, in countries with
large forested areas, the forest soil can provide a potential site for
C sequestration.
Previous studies have assessed the effects of biochar addi-
tion on soil C turnover and emissions of CO2 in subtropical and
temperate forests, but the responses have been unclear and incon-
sistent, since both positive, negative, and null effects have been
observed (Bruckman et al., 2015; Liu et al., 2016b; Sackett et al.,
2015; Hawthorne et al., 2017; Wardle et al., 2008; Zhou et al.,
2017). However, studies on the effects of large-scale application
of biochar in boreal forests are rare. Biochar addition may increase
forest soil C pools since it is structurally resistant to decomposition
(Ouyang et al., 2014; Bruckman et al., 2015), but its effects on soil
respiration and turnover of soil C are not clear (Liu et al., 2016b).
An increase in soil respiration within the first several months after
biochar incorporation into the soil has been reported in previous
studies, which could be attributed to the rapid decomposition of
labile component of C in the biochar (Cross and Sohi, 2011; Luo
et al., 2011; Ouyang et al., 2014; Bruckman et al., 2015), acceler-
ated decomposition of native soil C induced by the biochar (prim-
ing effect; Singh and Cowie, 2014; Wang et al., 2016a), and/or the
increasing soil temperature since biochar addition decreases the
soil surface albedo (Genesio et al., 2012; Palviainen et al., 2018).
However, in the long term the positive impacts of biochar on soil
respiration decreased with time or no longer existed, and even neg-
ative priming may have occurred because of the rapid depletion of
the small component of labile C in the biochar (Bruckman et al.,
2015), the stabilization of SOC caused by biochar-induced orga-
no-mineral interactions (Cross and Sohi, 2011; Singh and Cowie,
2014), and/or because the biochar particles were covered by the
newly grown vegetation (Palviainen et al., 2018).
The increased decomposition of labile C in biochar and/or na-
tive soil could increase soil CO2 emissions, which contradicts the
idea of C capture in the soils (Palviainen et al., 2018). However, some
studies have indicated that the possible increasing CO2–C evolved
from the soil and decreasing soil organic C after biochar application
could be more than compensated for by the increased soil C caused
by the incorporation of biochar into the soil (Luo et al., 2011). This
may be because of the fact that the fraction of recalcitrant C pools
in biochar may be more than 97%, thus contributing directly to the
long-term C sequestration in soil (Wang et al., 2016a).
Apart from the direct impacts of biochar on soil respiration,
the response of the temperature sensitivity of soil organic matter
decomposition (Q10) to biochar application is not yet clear (Fang
et al., 2014), knowledge of which is critical to the modeling and
prediction of future climate change (Davidson and Janssens, 2006;
Smith et al., 2008), especially in forest ecosystems where wildfires
may occur. Previous studies have indicated that biochar addition
in soil may influence the labile C content of soil (Bell and Worrall,
2011) and soil C stabilization (Liang et al., 2010), as well as the en-
zymatic activities (Bailey et al., 2010) and microbial communities
(Lehmann et al., 2011), leading to a change in Q10 (Pei et al., 2017).
The addition of biochar into the soil may increase soil water
holding capacity because of the high porosity of biochar (Yu et
al., 2013; Baronti et al., 2014) and influence the biomass and ac-
tivity of soil microbes, resulting in either an increase or a decrease
in the mineralization of soil organic matter and soil CO2 emis-
sions (Dempster et al., 2012; Ouyang et al., 2014; Zhang et al.,
2014). Moreover, biochar may have impacts on soil N dynamics,
but the changes in soil N stocks after biochar amendment in for-
est ecosystems have been inconsistent and are not yet understood
(Noyce et al., 2015; Sackett et al., 2015). Moreover, the variable
effects of biochar on soil microbial biomass and its activity and
other characteristics may be attributed to the variations in bio-
char feedstock material, pyrolysis conditions, biochar composi-
tion, application rate, and soil type (Kolb et al., 2009; Luo et al.,
2011; El-Mahrouky et al., 2015).
The aims of our study were to determine: (i) whether bio-
char addition increases the organic C and N concentrations and
moisture content in boreal forest soils; (ii) how soil CO2 emis-
sions are affected by biochar amendments; and (iii) whether bio-
char amendment is a feasible strategy for C sequestration in bo-
real forests. We hypothesized that biochar amendment increases
the turnover rate of soil organic C, resulting in elevated soil respi-
ration. We also hypothesized that the addition of biochar is posi-
tively correlated with soil water content and soil C stock and that
the effect is stronger with a higher amount of biochar. The ef-
fects of biochar on soil C and N stocks and CO2 emissions were
studied in the second year (16 mo) after the biochar amendment.
MATERIALS AND METHODS
Study Site
The study site is located at Hyytiälä Forestry Field Station in
Southern Finland (61° 51' N, 24° 17' E, 181 m above sea level),
in four approximately 20-yr-old Scots pine (Pinus sylestris L.)
stands. In the year 2015, the average height of trees was 5.0 m,
breast height (1.3 m) diameter 4.9 cm, and the number of trees
4025 ha–1 (Palviainen et al., 2018). The soil is a nutrient-poor,
well-drained, coarse-sand-textured haplic podzol (IUSS Working
Group WRB, 2015), with a mean thickness of the organic layer
of 2.6 cm. The average soil C and N concentrations were 29.82
and 0.91% in the organic layer, and 3.23 and 0.11% in the upper
(0–5 cm) mineral soil layer, respectively. The long-term (1981–
2010) mean annual air temperature in the area is 3.5°C and the
annual precipitation 700 mm (Pirinen et al., 2012).
Biochar was spread on two subplots (15 m ×15 m) at differ-
ent rates: 5 and 10 Mg ha–1, respectively, and there was a control
subplot without biochar addition. The experimental design was
replicated in four stands (called blocks). In the middle of May
2015, biochar was spread manually on the surface of the organic
layer and not mixed with the mineral soil layer. The biochar was
produced from Norway spruce [Picea abies (L.) H. Karst] wood
chips at 650°C (manufactured by Sonnenerde GmbH) using the
Pyreg process and the grain size of the biochar was 5 to 10 mm
(Bruckman et al., 2015). The C and N concentrations in the bio-
char were 60.61 ± 1.88% and 0.29 ± 0.10% (N = 7). Soil tem-

www.soils.org/publications/sssaj ∆
perature was measured continuously on all sample plots at 3-h
intervals with iButton temperature sensors (Maxim Integrated),
that were installed under the organic layer (Palviainen et al.,
2018). More details about the study site and the characteristics
of the biochar have been described in Palviainen et al. (2018).
Soil Sampling and Incubation
Soil samples (altogether 108 samples; 9 samples per subplot
and 36 samples per treatment) were collected from the upper 10-
cm soil layer using PVC soil corers (inner diameter 4.5 cm, height
10 cm) at nine locations in each subplot in the early October of
2016. The soil samples were kept in the corers and packed in plas-
tic bags separately, and then stored at +5°C for 4 wk prior to the in-
cubation experiment. We assumed that the autotrophic respiration
from roots was already ceased by then. The girdling experiments
performed in boreal forests have shown that root respiration stops
within 14 d after the flow of recent carbohydrates to the roots has
been stopped (Högberg and Read, 2006). We also assumed that
the possible heterotrophic respiration from dead roots was the
same in all treatments because our samples were taken from plots
which were similar concerning vegetation and tree biomass.
All the 108 samples were incubated for 8 h at 5, 15, and 25°C
in a climate chamber (WEISS WK11 340, Weiss Klimatechnik
GmbH, Germany) and CO2 production was measured. During
the incubation, the samples were placed in 3100-mL incubation
bottles separately, and the bottles were flushed with compressed
air with ambient CO2 concentration and sealed before each in-
cubation temperature. Before incubation at each temperature,
the samples were placed in a climate chamber for around 13 h
until soil temperature was stable and corresponded to the next
incubation temperature. A 50-mL gas sample was taken from
each bottle by 60-mL polypropylene syringe (BD Plastipak 60,
BOC Ohmeda) in the beginning and end of the incubation at
each temperature level and injected into a 12-mL exetainer vial
(Labco limited). The gas samples were stored at +5°C until ana-
lyzing the CO2 concentrations by gas chromatograph (Hewlett-
Packard Co.). The C production during the incubation (Cprod,
mg C bottle–1 s–1) was calculated for each sample at each in-
cubation temperature, based on the CO2 concentration in the
bottles before and after the incubation.
We fitted the temperature response of the C production by
regressions between the Cprod and the corresponding incubation
temperature (5, 15, and 25°C) for each soil sample using the fol-
lowing function:
( /10)
10
T
prod ref
C RQ= ×
[1]
where Rref is the reference respiration at 0°C; Q10 is the temperature
sensitivity of respiration and T is the incubation temperature (°C).
After the incubation, all soil samples were packed back into
plastic bags and stored at +5°C for the following analyses.
Soil Analyses
First, the length of the whole soil core was measured from
each sample. Then each sample was separated into three subsam-
ples; living mosses, organic layer (including the F-, L- and OH-
layers), and mineral soil including the E-layer (eluvial horizon)
and the surface of the B-layer (illuvial horizon) in the podzolic
soil profile. The thickness and the fresh and dry weights (60°C
for 24 h) of each subsample were determined. Big roots and stones
were separated by sieving the samples through a 2-mm sieve and
the masses of the separated roots and stones were measured. The
biochar particles were pushed through the sieve during the siev-
ing. Then the subsamples were homogenized and ground with a
mortar and placed into the paper bags separately. After that, ~2 g
soil samples were taken from each subsample, placed into small vi-
als, and ground with a ball mill (Retsch MM301). The TOC and
TN concentrations from each ground subsample in the vials were
measured with an elemental analyzer (varioMAX CN elemental
analyzer, Elementar Analysensysteme GmbH). The TOC and
TN pool in the whole soil cylinder was calculated based on the
dry weight of the three subsamples (mosses, organic, and mineral
layers). This pool was used to normalize both the instantaneous
and annual respirations by the C content of the soil. The C/N ra-
tio of the soil was calculated by dividing the TOC concentrations
by TN concentrations. In our study site, the ground floor vegeta-
tion consisted mainly of mosses, and it was practically impossible
to separate the moss from the biochar because there was newly
grown moss on top of the biochar layer and also moss beneath it.
Thus we kept the moss and organic layer (including mosses) and
mineral soil separately and calculated the corresponding TOC
and TN respectively, to see the effects of biochar addition on C
and N in different layers. The volumetric water content (SWC,
cm3 cm–3) for each sample was calculated based on the volume
of whole soil core before dividing it into layers as well as the fresh
and dry weight of the total sample.
Annual Soil Heterotrophic Respiration and
Turnover Time
The annual heterotrophic respiration of the whole soil cyl-
inder (Rs annual) under field conditions was calculated based on
Eq. [1] obtained from the incubation of each cylinder. Since there
were no significant differences in the field observed soil tempera-
tures among the treatments under the organic layer (Palviainen et
al., 2018), the daily average soil temperature of all the plots was
used in calculating the respiration. Then the daily respiration of
each soil cylinder (g C d–1) was calculated using Eq. [1], and the
annual respiration (Rs annual cylinder, g C yr–1 per cylinder) was
summed over the period from 5 Oct. 2015 to 4 Oct. 2016.
The turnover time (Tturn, years) of the TOC was calculated
for each cylinder as follows:
mass
turn
s annual cylinder
TOC
[2]
where TOCmass is the mass of total organic C in each cylinder (g C).

∆ Soil Science Society of America Journal
Rs annual cylinder was converted into annual respiration per
m2 (Rs annual, g C m–2 yr–1) as follows:
s annual cylinder
s annual 2
( / 2)
=
×
R
R
d
π
[3]
where d is the diameter of the soil cylinder (m).
Finally, the annual respiration was normalized by the C pool
of the cylinder (Rs annual C, g C m–2 yr–1 (g C)–1) as follows:
s annual
s annual C
mass
TOC
=
R
R
[4]
Additionally, the instantaneous respiration in soil cylinders
during incubation (C flux, g C m–2 d–1) was also normalized
by the C pool of the cylinder (normalized C flux, g C m–2 d–1
(g C)–1) as follows:
mass
flux
normalized C flux TOC
=
C
[5]
Data analysis
One-way ANOVA was used to test the effect of biochar
amendment on instantaneous respiration, TOC, TN, soil C/N
ratio, SWC, Q10, Rs annual, Tturn, and Rs annual C. Differences were
considered statistically significant when P was ≤ 0.05. Correlations
between treatments (biochar amount), TOC, TN, soil C/N ra-
tio, SWC, Q10, Rs annual, Tturn, and Rs annual C were studied using
Pearson correlation. Statistical tests were performed using IBM
SPSS version 23 (IBM Corp, Armonk, NY). The results of the
statistical tests are presented in the supplementary material.
The factors affecting the variation in Rs annual, Q10, and Rs
annual C were studied by using linear mixed-effect model followed
by Fisher’s least significant difference (LSD) test where the Rs
annual, Q10, and Rs annual C were used as dependent variables
(Table1). Significant correlations were observed between treat-
ments and SWC (P < 0.001), and between treatments and soil
C/N ratio (P < 0.001). The effects of treatments (TR, biochar
addition), soil water content (SWC), soil C/N ratio (CN), and
the interaction between treatment and SWC (TR×SWC) and
between treatment and C/N ratio (TR´CN) were used as inde-
pendent variables, whereas the replicated stands for each treat-
ment (area) were treated as a random effect. Data were checked
for normality with the Shapiro–Wilk test, and the equality of
variances was also tested. To find the best model we started
with a full model and reduced the number of variables using the
Akaike information criteria (AIC) as the criteria.
The initial model including all factors was:
y = a + b TR + c SWC + d CN + e (TR×SWC) +
f (TR×CN) + r(A) [6]
where y is the dependent variable (Rs annual, Q10 and Rs annual C);
TR is the treatment (the amount of biochar), SWC is the soil wa-
ter content (cm3 cm–3), and CN is the soil C/N ratio. The r(A)
means the random effect (area), a is the intercept of the model,
and b, c, d, e, and f are the regression coefficients for the factors.
The linear mixed effect model analyses were performed with R
using the “lme4” package (Bates et al., 2015).
RESULTS
Instantaneous Respiration
Biochar addition increased the instantaneous respira-
tion in soil cylinders incubated at 5°C in the plots treated with
10 Mg ha–1 of biochar and at 25°C in the plots treated with
5 Mg ha–1 of biochar, and it had a nonsignificant effect at 15°C
(Fig. 1a). After being normalized by the amount of C in the soil
cylinder, the instantaneous respiration did not show significant
differences between the treatments (Fig. 1b). The respiration in-
creased with incubation temperature (P < 0.01).
Soil Carbon and Nitrogen
The C concentration in the 0- to 10-cm layer (whole cylin-
der) was higher in the biochar amendment plots than in the con-
trol plots (P < 0.01), whereas between the plots treated with 5 and
10 Mg ha–1 of biochar, there was no significant difference (P =
0.969) in the C concentration (Fig. 2). In the moss and organic
layer, the C concentration was lower in
the 5 Mg ha–1 plots (P < 0.05) and high-
er in the 10 Mg ha–1 plots (P < 0.01)
than in the control plots. In the mineral
soil, there was no significant difference
(P = 0.372) in the C concentration be-
tween treatments.
The N concentration in the 0- to
10-cm layer was higher in the plots
treated with 5 Mg ha–1 of biochar than
that in the control plots (P = 0.01)
(Fig. 2). However, the differences be-
tween the plots treated with 10 Mg ha–1
of biochar and the other two treatments
(control and 5 Mg ha–1 biochar) were
not significant (P > 0.05). In the moss
and organic layer, the N concentration
Table 1. Linear mixed-effects models tted against annual soil respiration (Rs annual,
g C m
-2
yr
-1
), annual soil respiration normalized to carbon pool of the sample [R
s annual C
,
g C m-2 yr-1 (g C)-1] and Q10. TR is treatment (the amount of biochar), SWC is soil water
content (cm3 cm−3), CN is soil C/N ratio, r(A) means the random effect (area), and e the
error term.
Dependent variable Model Model Expression
Rs annual,
g C m–2 yr–1 1y = a + b TR + c SWC + d CN + e (TR×SWC) + f (TR×CN) + r(A) + e
2y = a + b TR + c SWC + d CN + e (TR×SWC) + r(A) + e
3y = a + b TR + c SWC + d CN + r(A) + e
4† y = a + c SWC + d CN + r(A) + e
Rs annual C,
g C m–2 yr–1 (g C)–1 5y = a + b TR + c SWC + d CN + e (TR×SWC) + f (TR×CN) + r(A) + e
6y = a + b TR + c SWC + d CN + e (TR×SWC) + r(A) + e
7y = a + b TR + c SWC + d CN + r(A) + e
8† y = a + c SWC + d CN + r(A) + e
Q10 9y = a + b TR + c SWC + d CN + e (TR×SWC) + f (TR×CN) + r(A) + e
10 y = a + b TR + c SWC + d CN + e (TR×SWC) + r(A) + e
11 y = a + b TR + c SWC + d CN + r(A) + e
12† y = a + c SWC + d CN + r(A) + e
† Denotes best-tted model.

www.soils.org/publications/sssaj ∆
was lower in the 5 Mg ha–1 plots than that in the control (P <
0.001) and the 10 mg ha–1 plots (P < 0.001). In the mineral soil,
there were no significant differences in N concentration between
treatments (P = 0.659).
The biochar amendment significantly increased the C/N
ratio in the 0- to 10-cm layer compared with the control plots
(P < 0.05) (Fig. 2). However, the difference was not statistically
significant between the 5 and 10 Mg ha–1 plots (P = 0.152).
In the moss and organic layer, the C/N ratio was higher in the
10 Mg ha–1 plots than in the control (P < 0.001) and 5 Mg ha–1
plots (P = 0.001). In the mineral layer, there were no significant
differences in the C/N ratio between the treatments (P = 0.423).
Soil Water Content and Q10
Biochar amendment increased the SWC compared with the
control plots (P < 0.01) (Fig. 3). The average SWC in the sam-
pled soils was 0.150, 0.191, and 0.193 cm3 cm–3 in the control,
5, and 10 Mg ha–1 plots, respectively.
The temperature sensitivity of soil respiration (Q10) was
higher in the 5 Mg ha–1 plots than in the control (P < 0.05) and
10 Mg ha–1 plots (P < 0.01) (Fig. 3). However, the difference in
Q10 between the control and 10 Mg ha–1 plots was not signifi-
cant (P = 0.42). When we used the mixed effect model analysis
between Q10 and the experimental factors, we observed that,
based on the AIC, the best model explaining Q10 was Model
12, where the variables considered were SWC, CN, and r. It ex-
plained 65.3% of the variation in Q10. According to the model,
Fig. 1. (a) The Mean (± SE) instantaneous respiration (g C m-2 d-1) and
(b) respiration normalized by the C pool of the sample [g C m-2 d-1
(g C)-1] in each incubation temperature (5, 15, and 25°C) in the
control plots and in the 5 Mg ha-1 and 10 Mg ha-1 biochar treatments.
Statistically signicant differences (P < 0.05) between the treatments
in each temperature group are indicated by different lower-case
letters, whereas statistically signicant differences (P < 0.05) between
the temperatures are indicated by upper-case letters in parenthesis.
Fig. 2. Mean (± SE) values of soil total organic carbon concentration
(TOC, g C kg-1 soil dry weight), soil total nitrogen concentration
(TN, g N kg
-1
soil dry weight) and soil C/N ratio in each layer (moss
and organic layer and mineral layer) and in the 0- to 10-cm layer
in control plots and 5 and 10 Mg ha
-1
biochar treatments. Different
letters indicated statistically signicant differences (P < 0.05)
between the treatments.

∆ Soil Science Society of America Journal
SWC (P = 0.827) and soil C/N ratio (P = 0.998) failed to affect
the Q10 significantly (Table 2). The reference respiration in Eq.
[1] (Rref, at 0°C) showed no significant differences between the
treatments (Fig. 3).
Annual Soil Heterotrophic Respiration and
Turnover Time of Soil Carbon
Biochar did not induce significant effects on annual res-
piration, carbon turnover time (Tturn), and annual respiration
normalized by the C content (Fig. 4). The average annual res-
piration increased with the amount of biochar, being 397, 429,
and 455 g C m–2 yr–1 in the control, 5, and 10 Mg ha–1 plots,
respectively. However, the difference was not significant (P =
0.484 and 0.094 in the 5 and 10 Mg ha–1 plots, respectively) be-
cause of the high variation within each treatment. When we used
the linear mixed effect model analysis between annual respira-
tion and the explaining variables, the AIC indicated that the best
model was Model 4 which explained about 34% of the variation
in the annual respiration. Of the variables considered, the annual
respiration was not affected by soil water content (P = 0.310)
and soil C/N ratio (P = 0.627) (Table 2).
The average turnover time was similar in different treat-
ments, being 9.46, 10.01, and 9.82 yr in the control, 5, and
10 Mg ha–1 plots, respectively (Fig. 4).
The annual respiration normalized by soil C content was,
on average, lower in the biochar plots than that in the control
plots. However, this difference was not significant (P > 0.05)
(Fig. 4). The best model (Model 8) explained 44.8% of the varia-
tion in the annual respiration normalized by soil C content indi-
cating that it was not influenced by SWC (P = 0.887) and soil
C/N ratio (P = 0.738) (Table 2).
DISCUSSION
Soil Carbon and Nitrogen
Our results showed that the biochar amendment to the soil
surface had increased the TOC concentration in the 0- to 10-
cm layer (whole cylinder) (Fig. 2), thus confirming its potential
in increasing the C storage in soil (Lehmann et al., 2006). As
a carbon-rich solid material, biochar is very recalcitrant to de-
composition, especially when produced under high-temperature
pyrolysis (>550°C) from woody feedstocks. This is because of
the fused aromatic ring structures (Singh and Cowie, 2008;
Keiluweit et al., 2010; Ouyang et al., 2014). A meta-analysis per-
formed by Wang et al. (2016a) showed the stability of biochar in
soil and its very low turnover rate. Thus, the high recalcitrance of
biochar plays an important role in its ability to increase C seques-
tration into the soil (Woolf et al., 2010).
An increase in soil organic C content after biochar addi-
tion has also been reported in previous studies, for example, in
forests (Ouyang et al., 2014; Bruckman et al., 2015), croplands
(Fernández et al., 2014; Liu et al., 2016c; Pei et al., 2017), and
grasslands (Case et al., 2012). However, in our study, we ob-
served a lower TOC concentration in the moss and organic layer
in the plots treated with 5 Mg biochar ha–1 compared with the
control (Fig. 2). An explanation for this could be that the soil
dry weight and bulk density were significantly higher in the
plots treated with 5 Mg biochar ha–1 (14.01 g and 0.189 g cm–3)
when compared with the control (7.61 g and 0.144 g cm–3),
although the mass of TOC in the soil in the 5 Mg ha–1 plots
(2.67 kg C m–2) was also significantly higher than that in the
control plots (1.82 kg C m–2) (Table S3).
The concentration of TOC in the mineral soil did not dif-
fer statistically significantly between the treatments (Fig. 2, Table
S2). Similar results were also reported by Sackett et al. (2015)
who observed no differences in the TOC concentration in the
mineral soil layer (5- to 15-cm depth) between treatments 1 yr
after biochar addition in a temperate hardwood forest. This was
explained by the fact that the biochar that was spread on the soil
surface had not yet entered the mineral soil in their experiment.
Fig. 3. Mean (± SE) values of soil water content (SWC, cm3 cm-3),
Q10, and reference soil respiration (Rref, g C m-2 d-1) in control plots
and 5 and 10 Mg ha-1 biochar treatments. Different letters indicated
statistically signicant differences (P < 0.05) between the treatments.

www.soils.org/publications/sssaj ∆
Few studies have investigated the in situ effects of biochar ad-
dition on soil N content in forests. In our study, there was a tenden-
cy toward increasing TN concentration after the biochar addition,
which may be attributed to soil N retention through sequestration
by biochar. However, the TN concentrations in the 0- to 10-cm
layer (whole cylinder) were higher than in the control plots only in
the 5 Mg ha–1 plots (P = 0.01), and not in the 10 Mg ha–1 plots.
Lower TN concentration was observed in the moss and organic
layer in the 5 Mg ha–1 plots as compared with the control plots.
This may be because of the significantly higher soil dry weight and
bulk density in the moss and organic layer in the plots treated with
5 Mg biochar ha–1 as discussed above. There were no differences in
the TN concentration in the mineral layer between the treatments,
which could be because the biochar spread on the soil surface had
not yet entered the mineral soil as in the study of Sackett et al.
(2015). An increasing TN concentration after biochar addition
was also observed in cropland (Liu et al., 2016c). Pei et al. (2017)
reported an increase in soil TN that was positively correlated with
the amount of biochar applied, unlike the results reported here. A
meta-analysis of 371 independent studies showed that despite the
variability introduced by soil and climate, the addition of biochar
to soils resulted in, on average, an increased total soil N compared
with control conditions (Biederman and Harpole, 2013).
In boreal forest soil, Gundale et al. (2015) found that biochar
application (10 Mg ha–1) enhanced the net soil N mineralization
rates and soil NH4+ concentrations, but had no impact on the avail-
ability of NO3−. However, in the same site, as in the present study,
Palviainen et al. (2018) reported that biochar addition had no
significant effect on soil microbial biomass, biological N fixation,
and N mineralization rates in the organic layer. Moreover, previous
studies also reported unchanged soil N content in forests (Noyce et
al., 2015; Sackett et al., 2015), farmlands (Liu et al., 2016c; Novak
et al., 2010), pasture (Scheer et al., 2011), and Miscanthus field
(Case et al., 2012) after the application of biochar.
In our study, the soil C/N ratio in the whole cylinder was
higher in the biochar plots than in the control plots (P = 0.012
and <0.001 in the 5 and 10 Mg ha–1 plots, respectively). The
biochar spread on the soil surface had a much higher C/N ra-
tio (364 ± 70.4) than the native forest soil (33 ± 0.5 in the or-
ganic layer and 29 ± 0.8 in the uppermost 5 cm of the mineral
soil), thus leading to an increase in soil C/N ratio. Ouyang et al.
(2014) also reported a significantly higher soil C/N ratio in plots
amended with woodchip biochar than in control plots in forest
loamy soils. Similar results were reported by Case et al. (2012)
who observed that the C to N ratios were significantly increased
by biochar addition in soils collected from a Miscanthus field.
Soil water content and Q10
Biochar addition increased SWC in plots treated with
5 Mg ha–1 (P < 0.01) and 10 Mg ha–1 (P < 0.001) of biochar com-
pared with the control plots (Fig. 3). Our results were consistent
with previous studies which also indicated soil water holding capac-
ity to increase significantly when biochar was added (Yu et al., 2013;
Baronti et al., 2014; Liu et al., 2016a). The mechanism behind this
is likely the increased porosity (Yu et al., 2013). The responses in
water holding capacity to biochar addition are affected by soil type.
Gamage et al. (2016) reported that biochar amendment had a more
pronounced effect on the water retention in a sandy soil compared
with a sandy loam soil. The feed stock material and the pyrolysis
temperature of biochar also have a large effect on soil water reten-
tion capacity (Yu et al., 2013; Baronti et al., 2014; Hardie et al.,
2014; Ventura et al., 2014; Liu et al., 2016a; Yeboah et al., 2017).
Table 2. Values of the parameters of the tted Models 1–12. TR is treatment (the amount of biochar), SWC is soil water content
(cm3 cm−3), CN is soil C/N ratio.
Model 1 2 3 4 5 6 7 8 9 10 11 12
Adjusted R20.360 0.353 0.350 0.343 0.446 0.447 0.427 0.448 0.65 0.654 0.653 0.653
AIC 1315.9 1314.4 1312.5 1311.7 968.6 966.6 966.2 964.7 −63.59 −65.46 −66.81 −68.61
Signicance
value
0.126 0.086 0.046 0.032 < 0.001 < 0.001 < 0.001 < 0.001 0.027 0.023 < 0.001 < 0.001
Intercept
(stderr, P)
249.364
(202.240,
P = 0.218)
358.013
(120.903,
P = 0.077)
393.101
(82.750,
P = 0.052)
420.750
(79.617,
P = 0.037)
174.633
(40.524,
P = 0.388)
172.733
(24.388,
P = 0.393)
150.188
(16.915,
P = 0.458)
154.237
(15.989,
P = 0.446)
2.304
(0.349,
p < 0.001)
2.396
(0.234,
p < 0.001)
2.512
(0.186,
p < 0.001)
2.512
(0.186,
p < 0.001)
SWC
(stderr, P)
683.192
(580.072,
P = 0.239)
766.088
(568.317,
P = 0.187)
560.395
(227.334,
P = 0.334)
589.508
(225.289,
P = 0.310)
-219.759
(116.015,
P = 0.705)
-221.297
(113.482,
P = 0.703)
−86.533
(45.771,
P = 0.881)
−82.254
(45.232,
P = 0.887)
0.614
(0.941,
P = 0.514)
0.681
(0.923,
P = 0.46)
-0.002
(0.373,
P = 0.996)
-0.015
(0.072, P
= 0.827)
CN
(stderr, P)
0.342
(6.485,
P = 0.958)
-3.711
(2.369,
P = 0.567)
-3.740
(2.371,
P = 0.564)
-3.152
(2.330,
P = 0.627)
-2.316
(1.293,
P = 0.721)
-2.244
(0.471,
P = 0.729)
-2.239
(0.475,
P = 0.730)
-2.169
(0.467,
P = 0.738)
0.003
(0.01,
P = 0.796)
-0.001
(0.004,
P = 0.84)
-0.0008
(0.0038,
P = 0.822)
-0.001
(0.373,
P = 0.998)
TR
(stderr, P)
95.432
(92.807,
p = 0.304)
44.763
(53.598,
P = 0.630)
25.647
(23.491,
P = 0.782)
−9.674
(18.594,
P = 0.917)
−8.787
(10.813,
P = 0.925)
3.511
(4.949,
P = 0.970)
0.073
(0.16,
P = 0.647)
0.03
(0.105,
P = 0.773)
-0.032
(0.072,
P = 0.655)
TR×SWC
(stderr, P)
−69.968
(282.579,
P = 0.804)
-109.842
(276.676,
P = 0.697)
70.036
(56.423,
P = 0.804)
70.761
(55.130,
P = 0.802)
-0.326
(0.453,
P = 0.471)
-0.359
(0.444,
P = 0.419)
TR×CN
(stderr, P)
-1.865
(2.795,
P = 0.505)
0.033
(0.557,
P = 0.991)
-0.002
(0.004,
P = 0.722)

∆ Soil Science Society of America Journal
In the present study, considering that soil samples were col-
lected 16 mo after the biochar amendment, the labile biochar C
should have been nearly exhausted by soil microbes in the field.
Therefore, the temperature sensitivity of soil respiration (Q10)
reported here should mainly reflect the temperature responses of
native soil C decomposition, with negligible contribution from
the biochar itself (Pei et al., 2017). In the present study, the Q10
was higher in plots treated with 5 Mg biochar ha–1 than in the
control and the 10 Mg ha–1 biochar plots. The responses of Q10
to biochar addition reported in previous studies have been in-
consistent since both positive (Lu et al., 2014; Wang et al., 2014;
Zhou et al., 2017), negative (Fang et al., 2014; Pei et al., 2017),
and null effects have been observed (Fang et al., 2014; Ventura et
al., 2014; Bamminger et al., 2018)-depending on soil properties,
biochar properties, and incubation temperature (Fang et al., 2014,
2015). In our study, the higher Q10 observed in the plots treated
with 5 Mg biochar ha–1, compared with that of the control and
the 10 Mg ha–1 plots, was probably caused by the increasing soil
moisture content since the temperature sensitivity of SOM could
be higher under wet conditions (Almagro et al., 2009; Suseela et
al., 2012). However, in the 10 Mg ha–1 plots, Q10 was nearly the
same as in the control, which was unexpected. Previous studies re-
ported that biochar addition could decrease Q10 by protecting soil
native C from microbial attack and thus limiting the temperature
responses of C decomposition (Fang et al., 2014; Pei et al., 2017).
Present study is not able to explain the changes in Q10 because we
do not have deeper process data about these issues. Further studies
in the future will be required to resolve this process.
Soil Respiration and Carbon Turnover
We observed higher instantaneous respiration at tempera-
tures of 5°C in the plots treated with 10 Mg of biochar ha–1 and at
temperatures of 25°C in plots treated with 5 Mg of biochar ha–1,
indicating a possible increasing tendency of soil respiration after
biochar application. However, the instantaneous respiration nor-
malized by the C content did not show significantly lower values
in the biochar plots than in the control, indicating that biochar
addition probably leads to larger stable C stocks in soils.
There was no increase in the annual respiration in treatments
with biochar addition in our study, indicating that there was no
priming effect. The soil CO2 flux measurements conducted with
chambers in our experimental plots in June and July 2016 also
showed no clear differences between treatments after biochar ap-
plication (Palviainen et al., 2018). The unchanged soil respiration
could be attributed to that the biochar used in our study was wood-
derived and produced at high pyrolysis temperature (650°C) being
thus very recalcitrant to decomposition (Zimmerman et al., 2011;
He et al., 2017). Therefore, it likely only contributed slightly to
soil CO2 emissions. Furthermore, the labile part of the biochar
was probably mineralized in the initial stages after biochar appli-
cation in the soil, resulting in rate of soil C mineralization that was
not significantly different between the treatments at later stages
(Ouyang et al., 2014; Bruckman et al., 2015). In addition, the po-
tential increase in soil C mineralization rate caused by the biochar-
induced increase in soil temperature observed in 2015 had already
vanished when we conducted our sampling in the areas in early
October of 2016, as the biochar particles spread on the soil were
already covered by mosses in the second summer after the biochar
amendment (Genesio et al., 2012; Palviainen et al., 2018). Thus,
in the summer of 2016, there were no differences in soil tempera-
tures between the treatment plots according to continuous mea-
surements recorded by temperature loggers buried in the soil be-
tween the organic and mineral soil layers (Palviainen et al., 2018).
The priming effects of biochar addition on soil respiration
have been unclear and inconsistent in previous studies, since
both positive (Smith et al., 2010; Ameloot et al., 2013; Sagrilo
et al., 2015; Hawthorne et al., 2017; Zhou et al., 2017), negative
Fig. 4. Mean (± SE) values of annual soil respiration (Rs annual, g
C m-2 yr-1), turnover time (Tturn, years), and annual soil respiration
normalized by the C pool of the sample [R
s annual C
, g C m
-2
yr
-1
(g C)
-1
]
in the control plots and in the 5 and 10 Mg ha-1 biochar treatments.
The same letters indicate no statistically signicant differences between
the treatments.

www.soils.org/publications/sssaj ∆
(Zimmerman et al., 2011; Case et al., 2012; Wang et al., 2016b;
Bamminger et al., 2018), and null effects (Scheer et al., 2011;
Ameloot et al., 2013; Lu et al., 2014; Bruckman et al., 2015; Liu
et al., 2016c) have been observed. Furthermore, the responses
have been dependent on the feedstock material (Zimmerman et
al., 2011; Ouyang et al., 2014) and pyrolysis temperature used
in the biochar production (Zimmerman et al., 2011; Ameloot
et al., 2013; Sheng et al., 2016). The application rates (Smith
et al., 2010; Hawthorne et al., 2017), the time after biochar ap-
plication (Bruckman et al., 2015; Bamminger et al., 2018), and
soil characteristics (Case et al., 2012; Sheng et al., 2016) have
also affected the results in the previous priming studies. Field
chamber measurements performed earlier in our study site by
Palviainen et al. (2018) have indicated that soil CO2 efflux in
the plots treated with 10 Mg of biochar ha–1 produced at 650°C
was significantly higher compared with the control in the initial
few months after biochar addition, which was attributed to the
increasing soil temperature immediately after spreading the bio-
char. In the second summer, however, similar soil CO2 effluxes
between the control and biochar treatments were observed in the
field because biochar had largely disappeared under the newly
grown moss layer (Palviainen et al., 2018).
Gundale et al. (2015) mixed 10 Mg ha–1 biochar to boreal
forest soil and found no significant effect on soil respiration two
growing seasons after biochar addition. In a temperate forest in
Austria, an initially weak positive priming effect on soil respira-
tion was observed after amending 10 Mg ha–1 of biochar derived
from woodchips and pyrolyzed at 550°C to soil (Bruckman et al.,
2015). The effect vanished after the first 2 wk because the small la-
bile fraction in the fresh biochar was quickly used by soil microbes.
The soil C mineralization rates in the biochar treatments remained
comparable with the control plots during the 15 mo following
the amendment (Bruckman et al., 2015). Similar initial positive
priming effect and null/negative priming effects at later stages af-
ter biochar application in soil were reported by Zimmerman et al.
(2011) and Bamminger et al. (2018). Overall, soil C mineraliza-
tion was usually greater than in control plots (positive priming)
in soils amended with biochar produced at low temperatures and
from grasses, particularly during the early stage after amendment,
while null/negative priming usually happened in soils amended
with biochar produced at high temperatures and from woods, par-
ticularly during the later stage (Zimmerman et al., 2011).
Interestingly, the turnover rate of C was similar in all plots with
and without biochar amendment, indicating that biochar addition
did not accelerate the mineralization of soil organic C in our study.
Since an increase was observed in both TOC and annual soil
respiration after biochar addition, though the latter was not sig-
nificant, we calculated the Rs annual C (Rs annual normalized to C
pool of the sample), to assess the effects of biochar application
on C sequestration potential. A slightly, but not significantly,
lower Rs annual C was observed in biochar plots compared with
control plots, thus net C sequestration was always occurring. This
indicates that from a C sequestration point of view, it can be con-
cluded that biochar addition leads to higher stable C stocks in
the soil, especially in biochar produced from woodchip at higher
temperatures (Zimmerman et al., 2011; Ouyang et al., 2014).
CONCLUSIONS
Our results indicate that wood-derived biochar produced at
high pyrolysis temperatures had no significant effects on soil het-
erotrophic respiration obtained from lab incubations in boreal
Scots pine forests at 5 to 10 Mg ha–1 application rates. Biochar
addition increased soil total organic C, C/N ratio, and moisture
content, but had no clear effect on soil total N, nor on the tem-
perature sensitivity of soil respiration. The turnover time of soil
C was unaffected by biochar addition. These results indicate that
from a C sequestration point of view, it can be concluded, that bio-
char addition did not accelerate the mineralization of soil organic
C and could lead to higher stable C stocks in the surface soil layer.
SUPPLEMENTAL MATERIAL
is article contains supplementary material available to authorized users.
ACKNOWLEDGMENTS
e research was funded by e Foundation for Research of Natural
Resources in Finland (2016085). We also thank the Academy of
Finland to support the study through the Academy of Finland Centre
of Excellence program and the project number 286685. We thank for
the sta of Hyytiälä Forestry Field Station for supporting us in the eld
work and Anu Riikonen for help with laboratory analyses.
REFERENCES
Almagro, M., J. López, J.I. uerejeta, and M. Martínez-Mena. 2009. Temperature
dependence of soil CO2 eux is strongly modulated by seasonal patterns
of moisture availability in a Mediterranean ecosystem. Soil Biol. Biochem.
41:594–605. doi:10.1016/j.soilbio.2008.12.021
Ameloot, N., S. De Neve, K. Jegajeevagan, G. Yildiz, D. Buchan, Y. Nkwain
Funkuin, W. Prins, L. Bouckaert, and S. Sleutel. 2013. Short-term CO2 and
N2O emissions and microbial properties of biochar amended sandy loam
soils. Soil Biol. Biochem. 57:401–410. doi:10.1016/j.soilbio.2012.10.025
Bailey, V.L., S.J. Fansler, J.L. Smith, and H. Bolton, Jr. 2010. Reconciling apparent
variability in eects of biochar amendment on soil enzyme activities
by assay optimization. Soil Biol. Biochem. 43:296–301. doi:10.1016/j.
soilbio.2010.10.014
Bamminger, C., C. Poll, and S. Marhan. 2018. Osetting global warming-
induced elevated greenhouse gas emissions from an arable soil by biochar
application. Glob. Change Biol. 24:e318–e334. doi:10.1111/gcb.13871
Baronti, S., F.P. Vaccari, F. Miglietta, C. Calzolari, E. Lugato, S. Orlandini, R.
Pini, C. Zulian, and L. Genesio. 2014. Impact of biochar application
on plant water relations in Vitis vinifera (L.). Eur. J. Agron. 53:38–44.
doi:10.1016/j.eja.2013.11.003
Bates, D., M. Maechler, B. Bolker, and S. Walker. 2015. Fitting linear mixed-eects
models using lme4. J. Stat. Sow. 67:1–48. doi:10.18637/jss.v067.i01
Bell, M.J., and F. Worrall. 2011. Charcoal addition to soils in NE England:
A carbon sink with environmental co-benets? Sci. Total Environ.
409:1704–1714. doi:10.1016/j.scitotenv.2011.01.031
Biederman, L.A., and W.S. Harpole. 2013. Biochar and its eects on plant
productivity and nutrient cycling: A meta-analysis. Glob. Change. Biol.
Bioenergy 5:202–214. doi: https://doi.org/10.1111/gcbb.12037
Bruckman, V.J., T. Terada, B.B. Uzun, E. Apaydin-Varol, and J. Liu. 2015. Biochar
for climate change mitigation: Tracing the in situ priming eect on a forest
site. Energy Procedia 76:381–387. doi:10.1016/j.eg ypro.2015.07.845
Case, S.D.C., N.P. McNamara, D.S. Reay, and J. Whitaker. 2012. e eect of
biochar addition on N2O and CO2 emissions from a sandy loam soil—
e role of soil aeration. Soil Biol. Biochem. 51:125–134. doi:10.1016/j.
soilbio.2012.03.017
Cross, A., and S.P. Sohi. 2011. e priming potential of biochar products in
relation to labile carbon contents and soil organic matter status. Soil Biol.

∆ Soil Science Society of America Journal
Biochem. 43:2127–2134. doi:10.1016/j.soilbio.2011.06.016
Davidson, E.A., and I.A. Janssens. 2006. Temperature sensitivity of soil carbon
decomposition and feedbacks to climate change. Nat. Geosci. 440:165–173.
Dempster, D.N., D.B. Gleeson, Z.M. Solaiman, D.L. Jones, and D.V. Murphy.
2012. Decreased soil microbial biomass and nitrogen mineralisation with
Eucalyptus biochar addition to a coarse textured soil. Plant Soil 354:311–
324. doi:10.1007/s11104-011-1067-5
El-Mahrouky, M., A.H. El-Naggar, A.R. Usman, and M. Al-Wabel. 2015.
Dynamics of CO2 emission and biochemical properties of a sandy
calcareous soil amended with conocarpus waste and biochar. Pedosphere
25:46–56. doi:10.1016/S1002-0160(14)60075-8
Fang, Y., B.P. Singh, and B. Singh. 2014. Temperature sensitivity of biochar and
native carbon mineralisation in biochar-amended soils. Agric. Ecosyst.
Environ. 191:158–167. doi:10.1016/j.agee.2014.02.018
Fang, Y., B. Singh, and B.P. Singh. 2015. Eect of temperature on biochar
priming eects and its stability in soils. Soil Biol. Biochem. 80:136–145.
doi:10.1016/j.soilbio.2014.10.006
Fernández, J.M., M.A. Nieto, E.G. López-de-Sá, G. Gascó, A. Méndez, and C.
Plaza. 2014. Carbon dioxide emissions from semi-arid soils amended with
biochar alone or combined with mineral and organic fertilizers. Sci. Total
Environ. 482-483:1–7. doi:10.1016/j.scitotenv.2014.02.103
Gamage, D.N.V., R.B. Mapa, R.S. Dharmakeerthi, and A. Biswas. 2016. Eect of
rice-husk biochar on selected soil properties in tropical Alsols. Soil Res.
54:302–310. doi:10.1071/SR15102
Genesio, L., F. Miglietta, E. Lugato, S. Baronti, M. Pieri, and F.P. Vaccari. 2012.
Surface albedo following biochar application in durum wheat. Environ.
Res. Lett. 7:014025. doi:10.1088/1748-9326/7/1/014025
Gundale, M.J., M.-C. Nilsson, N. Pluchon, and D.A. Wardle. 2015. e eect
of biochar management on soil and plant community properties in a
boreal forest. Glob. Change Biol. Bioenergy 8:777–789. doi:10.1111/
gcbb.12274
Hardie, M., B. Clothier, S. Bound, G. Oliver, and D. Close. 2014. Does biochar
inuence soil physical properties and soil water availability? Plant Soil
376:347–361. doi:10.1007/s11104-013-1980-x
Hawthorne, I., M.S. Johnson, R.S. Jassal, T. Andrew Black, N.J. Grant, and S.M.
Smukler. 2017. Application of biochar and nitrogen inuences uxes of
CO2, CH4 and N2O in a forest soil. J. Environ. Manage. 192:203–214.
doi:10.1016/j.jenvman.2016.12.066
He, Y., X. Zhou, L. Jiang, M. Li, Z. Du, G. Zhou, J. Shao, X. Wang, Z. Xu, S.H.
Bai, H. Wallace, and C. Xu. 2017. Eects of biochar application on soil
greenhouse gas uxes: A meta-analysis. Glob. Change Biol. Bioenergy
9:743–755. doi:10.1111/gcbb.12376
Högberg, P., and D.J. Read. 2006. Towards a more plant physiological
perspective on soil ecology. Trends Ecol. Evol. 21:548–554. doi:10.1016/j.
tree.2006.06.004
IUSS Working Group WRB. 2015. World reference base for soil resources 2014,
update 2015 international soil classication system for naming soils and
creating legends for soil maps. World soil resources report no. 106. FAO,
Rome.
Keiluweit, M., P.S. Nico, M.G. Johnson, and M. Kleber. 2010. Dynamic
molecular structure of plant biomass-derived black carbon (biochar).
Environ. Sci. Technol. 44:1247–1253. doi:10.1021/es9031419
Kolb, S.E., K.J. Fermanich, and M.E. Dornbush. 2009. Eect of charcoal quantity
on microbial biomass and activity in temperate soils. Soil Sci. Soc. Am. J.
73:1173–1181. doi:10.2136/sssaj2008.0232
Kumar, A., R .F. Lobo, and N.J. Wagner. 2005. Porous amorphous carbon models
from periodic Gaussian chains of amorphous polymers. Carbon 43:3099–
3111. doi:10.1016/j.carbon.2005.06.030
Kuzyakov, Y., I. Subbotina, H. Chen, I. Bogomolova, and X. Xu. 2009. Black
carbon decomposition and incorporation into soil microbial biomass
estimated by 14C labelling. Soil Biol. Biochem. 41:210–219. doi:10.1016/j.
soilbio.2008.10.016
Lehmann, J., J. Gaunt, and M. Rondon. 2006. Bio-char sequestration in terrestrial
ecosystems–A review. M. Mitig Adapt. Strat. Glob. Change. 11:403–427.
doi:10.1007/s11027-005-9006-5
Lehmann, J., M.C. Rillig, J. ies, C.A. Masiello, W.C. Hockaday, and D.
Crowley. 2011. Biochar eects on soil biota: A review. Soil Biol. Biochem.
43:1812–1836. doi:10.1016/j.soilbio.2011.04.022
Liang, B., J. Lehmann, S.P. Sohi, J.E. ies, B. O’Neill, L. Trujillo, J. Gaunt, D.
Solomon, J. Grossman, E.G. Neves, and F.J. Luizão. 2010. Black carbon
aects the cycling of non-black carbon in soil. Org. Geochem. 41:206–
213. doi:10.1016/j.orggeochem.2009.09.007
Liu, C., H. Wang, X. Tang, Z. Guan, B.J. Reid, A.U. Rajapaksha, Y.S. Ok, and
H. Sun. 2016a. Biochar increased water holding capacity but accelerated
organic carbon leaching from a sloping farmland soil in China. Environ Sci
Pollut R 23:995–1006. doi:10.1007/s11356-015-4885-9
Liu, S., Y. Zhang, Y. Zong, Z. Hu, S. Wu, J. Zhou, Y. Jin, and J. Zou. 2016b.
Response of soil carbon dioxide uxes, soil organic carbon and microbial
biomass carbon to biochar amendment: A meta-analysis. Glob. Change
Biol. Bioenergy 8:392–406. doi:10.1111/gcbb.12265
Liu, X., J. Zheng, D. Zhang, K. Cheng, H. Zhou, A. Zhang, L. Li, S. Joseph, P.
Smith, D. Crowley, Y. Kuzyakov, and G. Pan. 2016c. Biochar has no eect
on soil respiration across Chinese agricultural soils. Sci. Total Environ.
554-555:259–265. doi:10.1016/j.scitotenv.2016.02.179
Lu, N., X.R. Liu, Z.L. Du, Y.D. Wang , and Q.Z. Zhang. 2014. Eect of biochar
on soil respiration in the maize growing season aer 5 years of consecutive
application. Soil Res. 52:505–512. doi:10.1071/SR13239
Luo, Y., M. Durenkamp, M.D. Nobili, Q. Lin, and P.C. Brookes. 2011. Short
term soil priming eects and the mineralisation of biochar following its
incorporation to soils of dierent PH. Soil Biol. Biochem. 43:2304–2314.
doi:10.1016/j.soilbio.2011.07.020
Novak, J.M., W.J. Busscher, D.W. Watts, D.A. Laird, M.A. Ahmedna, and
M.A.S. Niandou. 2010. Short-term CO2 mineralization aer additions of
biochar and switchgrass to a Typic Kandiudult. Geoderma 154:281–288.
doi:10.1016/j.geoderma.2009.10.014
Noyce, G.L., N. Basilik, R. Fulthorpe, T.E. Sackett, and S.C. omas. 2015. Soil
microbial responses over 2 years following biochar addition to a north temperate
forest. Biol. Fertil. Soils 51:649–659. doi:10.1007/s00374-015-1010-7
Ouyang, L., L. Yu, and R. Zhang. 2014. Eects of amendment of dierent
biochars on soil carbon mineralisation and sequestration. Soil Res. 52:46–
54. doi:10.1071/SR13186
Palviainen, M., F. Berninger, V.J. Bruckman, K. Köster, C. Ribeiro Moreira
de Assumpção, H. Aaltonen, N. Makita, A. Mishra, L. Kulmala, B.
Adamczyk, X. Zhou, J. Heinonsalo, E. Köster, and J. Pumpanen. 2018.
Eects of biochar on carbon and nitrogen uxes in boreal forest soil. Plant
Soil. Available online: https://doi.org/10.1007/s11104-018-3568-y
Pei, J., S. Zhuang, J. Cui, J. Li, B. Li, J. Wu, and C. Fang. 2017. Biochar decreased
the temperature sensitivity of soil carbon decomposition in a paddy eld.
Agric. Ecosyst. Environ. 249:156–164. doi:10.1016/j.agee.2017.08.029
Pessenda, L.C.R., S.E.M. Gouveia, and R. Aravena. 2001. Radiocarbon dating
of total soil organic matter and humin fraction and its comparison with
14C ages of fossil charcoal. Radiocarbon 43:595–601. doi:10.1017/
S0033822200041242
Pirinen, P., H. Simola, J. Aalto, J.-P. Kaukoranta, P. Karlsson, and R. Ruuhela.
2012. Climatological statistics of Finland 1981-2010. Finnish
Meteorological Institute, Helsinki, Finland
Sackett, T.E., N. Basiliko, G.L. Noyce, C. Winsborough, J. Schurman, C. Ikeda,
and S.C. omas. 2015. Soil and greenhouse gas responses to biochar
additions in a temperature hardwood forest. Glob. Change Biol. Bioenergy
7:1062–1074. doi:10.1111/gcbb.12211
Sagrilo, E., S. Jeery, E. Hoand, and T.W. Kuyper. 2015. Emission of CO2
from biocharamended soils and implications for soil organic carbon. Glob.
Change Biol. Bioenergy 7:1294–1304. doi:10.1111/gcbb.12234
Scheer, C., P.R. Grace, D.W. Rowlings, S. Kimber, and L. Van Zwieten. 2011. Eect
of biochar amendment on the soil-atmosphere exchange of greenhouse
gases from an intensive subtropical pasture in northern New South Wales,
Australia. Plant Soil 345:47–58. doi:10.1007/s11104-011-0759-1
Schimmelpfennig, S., and B. Glaser. 2012. One step forward toward
characterization: Some important material properties to distinguish
biochars. J. Environ. ual. 41:1001–1013. doi:10.2134/jeq2011.0146
Sheng, Y., Y. Zhan, and L. Zhu. 2016. Reduced carbon sequestration potential
of biochar in acidic soil. Sci. Total Environ. 572:129–137. doi:10.1016/j.
scitotenv.2016.07.140
Singh, B.P., and A.L. Cowie. 2008. A novel approach, using 13C natural
abundance, for measuring decomposition of biochars in soil. In: L.D.
Currie and L.J. Yates, editors, Carbon and nutrient management in
agriculture, Fertilizer and Lime Research Centre Workshop Proc. Massey
University, Palmerston North, New Zealand. p. 549.
Singh, B.P., and A.L. Cowie. 2014. Long-term inuence of biochar on native
organic carbon mineralisation in a low-carbon clayey soil. Sci. Rep. 4:3687.

www.soils.org/publications/sssaj ∆
doi:10.1038/srep03687
Smith, J.L., H.P. Collins, and V.L. Bailey. 2010. e eect of young biochar
on soil respiration. Soil Biol. Biochem. 42:2345–2347. doi:10.1016/j.
soilbio.2010.09.013
Smith, P., C. Fang, J.J.C. Dawson, and J.B. Moncrie. 2008. Impact of global
warming on soil organic carbon. Adv. Agron. 97:1–43. doi:10.1016/
S0065-2113(07)00001-6
Suseela, V., R.T. Conant, M.D. Wallenstein, and J.S. Dukes. 2012. Eects of soil
moisture on the temperature sensitivity of heterotrophic respiration vary
seasonally in an old-eld climate change experiment. Glob. Change Biol.
18:336–348. doi:10.1111/j.1365-2486.2011.02516.x
Ventura, M., C. Zhang, E. Baldi, F. Fornasier, G. Sorrenti, P. Panzacchi, and G.
Tonon. 2014. Eect of biochar addition on soil respiration partitioning
and root dynamics in an apple orchard. Eur. J. Soil Sci. 65:186–195.
doi:10.1111/ejss.12095
Wang, J., Z. Xiong, and Y. Kuzyakov. 2016a. Biochar stability in soil: Meta-
analysis of decomposition and priming eects. Glob. Change Biol. 8:512–
523. doi:10.1111/gcbb.12266
Wang, J., Z. Xiong, X . Yan, and Y. Kuzyakov. 2016b. Carbon budget by priming
in a biochar-amended soil. Eur. J. Soil Biol. 76:26–34. doi:10.1016/j.
ejsobi.2016.07.003
Wang, Z.L., Y.F. Li, S.X. Chang, J.J. Zhang, P.K. Jiang, G.M. Zhou, and Z.M.
Shen. 2014. Contrasting eects of bamboo leaf and its biochar on soil
CO2, eux and labile organic carbon in an intensively managed Chinese
chestnut plantation. Biol. Fertil. Soils 50:1109–1119. doi:10.1007/
s00374-014-0933-8
Wardle, D.A., M.C. Nilsson, and O. Zackrisson. 2008. Fire-derived charcoal causes
loss of forest humus. Science 320:629–629. doi:10.1126/science.1154960
Woolf, D., J.E. Amonette, F.A. Street-Perrott, J. Lehmann, and S. Joseph. 2010.
Sustainable biochar to mitigate global climate change. Nat. Commun.
1:56. doi:10.1038/ncomms1053
Yeboah, S., R. Zhang, L. Cai, L. Li, J. Xie, and Z. Luo. 2017. Soil water content
and photosynthetic capacity of spring wheat as aected by soil application
of nitrogen-enriched biochar in a semiarid environment. Photosynthetica
55:532–542. doi:10.1007/s11099-016-0672-1
Yu, O.Y., B. Raichle, and S. Sink. 2013. Impact of biochar on the water holding
capacity of loamy sand soil. Int. J. Energy Environ. Eng. 4:44–52.
Zhang, Q.Z., F.A. Dijkstra, X.R. Liu, Y.D. Wang, J. Huang, and N. Lu. 2014.
Eects of biochar on soil microbial biomass aer four years of consecutive
application in the north China plain. PLoS One 9:e102062. doi:10.1371/
journal.pone.0102062
Zhou, G., X. Zhou, T. Zhang, Z. Du, Y. He, X. Wang, J. Shao, Y. Cao, S. Xue,
H. Wang, and C. Xu. 2017. Biochar increased soil respiration in temperate
forests but had no eects in subtropical forests. For. Ecol. Manage.
405:339–349. doi:10.1016/j.foreco.2017.09.038
Zimmerman, A.R., B. Gao, and M.-Y. Ahn. 2011. Positive and negative carbon
mineralization priming eects among a variety of biochar-amended soils.
Soil Biol. Biochem. 43:1169–1179. doi:10.1016/j.soilbio.2011.02.005