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University of Helsinki, Department of Environmental Sciences, Niemenkatu 73, 15340 Lahti, Finland
Natural Resources Institute Finland (Luke), 31600 Jokioinen, Finland
A R T I C L E I N F O
Article history:
Received 18 March 2016
Received in revised form 15 June 2016
Accepted 16 June 2016
Available online 1 July 2016
Keywords:
Birch wood biochar
Pyrolysis temperature
Ecotoxicity
A B S T R A C T
The addition of biochar to agricultural soils is recommended to improve soil functions and plant growth.
However, due to high variability in the quality of biochar, its effects on soils and plants are likely to differ.
We explored the impacts of pyrolysis temperature on the quality and usability of birch wood biochar as a
soil amendment. The impact of three biochar types pyrolysed at 300, 375 or 475 C on soil
characteristics and the growth of lettuce (Lactuca sativa), radish (Raphanus sativus), barley (Hordeum
vulgare) and ryegrass (Lolium perenne) was investigated in a greenhouse experiment. In addition, the
potential adverse effects of biochar on soil organisms (nematodes, earthworms, microbial biomass and
activity) were studied.
Biochar produced at the lowest temperature had initial transient negative effect on the germination
and biomass of lettuce, while biochar produced at higher temperatures had no such effect. After ve
weeks, pyrolysis temperature had only a marginal inuence on biochar-induced effects on soil pH, WHC,
soil organisms and plant growth. Our results suggest that birch biochar, irrespective of pyrolysis
temperature, has a parallel effect on plant biomass production and soil characteristics but the effect
depends on plant type and biochar application rate.
2016 Elsevier B.V. All rights reserved.
1. Introduction
Biochar, a carbon-rich material produced for example by the
slow pyrolysis of biomass, is suggested to be added to agricultural
soils to improve soil functions and to increase soil carbon
sequestration (Lehmann et al., 2003). During the past decade,
numerous articles focusing on the use of biochar have been
published, but have shown inconsistent results (Deenik et al., 2010;
Jeffery et al., 2011; Van Zwieten et al., 2010a). In general, the
addition of biochar to agricultural soils changes the physical,
chemical and biological properties of the soil. Biochar may enhance
plant growth, for example by increasing soil water-holding
capacity (WHC) and nutrient retention due to an increase in the
cation exchange capacity (CEC), or by improving physical
characteristics of the soil and mycorrhizal competence (Atkinson
et al., 2010). However, reactions in the soil after the addition of
biochar depend on the characteristics of biochar, soil, climate and
soil-inhabiting organisms. Biochar studies have mainly been
* Corresponding author.
E-mail address: marleena.hagner@helsinki. (M. Hagner).
http://dx.doi.org/10.1016/j.still.2016.06.006
0167-1987/ 2016 Elsevier B.V. All rights reserved.
225
and chemical characteristics of biochar were investigated (Fagerns et al., 2014; Hagner et al., 2015).
2. Materials and methods
2.1. Biochar, soil and plants used
Three types of biochar derived from birch wood (Betula spp.)
were produced by the VTT Technical Research Centre of Finland,
using a pilot-scale slow-pyrolysis unit. Birch branches with
moisture content of 1012% were cut to 25 mm 50150 mm
pieces. A temperature prole with two phases and overall duration
of 7.5 h was used to produce biochar. Temperature was rst raised
to 280 C (3.5 h) and thereafter to nal temperatures of 300 C,
375 C or 475 C (holding time 4 h). The biochar types are identied
according to the nal temperature as BC300, BC375 and BC475.
Pyrolysis temperatures 375 C and 475 C were within the range of
the European Biochar Certicate (EBC, 2012) and typical in Finnish
pyrolysis retorts. The lowest pyrolysis temperature (300 C) was
chosen to study if temperature lower than the one suggested by the
EBC would result in lower biochar quality and usability in the eld.
Volatile matter (%) (SFS-EN 15148), ash content (SFS-EN 14775),
xed carbon (ASTM D 3172), C/H/N- (SFS-EN 15104) and S-content
(SFS-EN 15289) were analysed according standard methods. PAHconcentrations were analysed in Nab Labs Ltd (GC/MS (SIM), ISO
16703). The BET surface area (Standard PANK 2401), water holding
capacities (WHC), pH (v/v 1:5 biochar:distilled water) and other
characteristics of the biochar types are presented in Table 1. The
pyrolysis process and the characteristics of the biochar types were
analysed at VTT Technical Research Centre of Finland and are
reported in detail in Fagerns et al. (2014).
A sandy-silt soil (classied as Cambisol based on Finnish and
FAO classication systems) was shoveled (ca. 10 cm deep surface
layer) from an organic agricultural eld in Rehtijrvi, SW-Finland
in the autumn of 2012. The moisture content of the soil, collected
after a very dry period, was 1.0% (Standard ASTM D2216, ASTM
2010). The soil consisted of 22% medium sand (200600 mm), 57%
ne sand (60200 mm) and 21% of particles under 60 mm (silt and
clay) in size. Soil nutrient analyses (Ca, K, Mg, P) were conducted in
the laboratory of the MTT Agricultural Research Finland according
to the protocol by Vuorinen and Mkitie (1955) used widely in
routine soil testing in Finland. The soil had a pH of 6.02 (1:5 soil:
water v/v), electrical conductivity of 0.68 mS/cm and pore volume
of 47% (Sandbox-method, Eijkelkamp Agrisearch equipment
2013). In general, soil was quite poor as concentrations of Ca, K, Mg,
Table 1
Characteristics of biochar types produced at pyrolysis temperatures of 300 C
(BC300), 375 C (BC375) and 475 C (BC475). Adapted from Fagerns et al. (2014).
Biochar property
Biochar type
BC300
BC375
BC475
0.5
48
52
72
4.9
0.2
23
0.01
2.2
23
5.1
194
0.41
0.7
30
69
80
3.9
0.3
15
0.01
6.4
24
5.2
4100
0.41
1.0
17
82
89
3.1
0.3
7
0.01
44
288
7.5
1107
0.45
a
WHC: water holding capacity (24 h) i.e. the total amount of water a material can
hold (% of biochar mass).
b
Bulk density (g/cm3) = dry mass (g)/volume (cm3).
226
Fig. 1. The greenhouse experimental design. Letters A-D represent the four tables on which the experimental pots resided. Numbers represents the pots on the tables:
1 = Control, 2 = BC300, 3 = BC375 and 4 = BC475, and in an exclusion area (5) around the primary exam pots. For tables A and B, the biochar application level was 20 g/L and for C
and D, 80 g/L of soil.
227
228
3. Statistical analysis
Fig. 2. Mean ( SE) water content (measured using the Grodan WCM control meter)
of the soils in the biochar (80 g/L) treated pots (BC350, BC 375 and BC475 pooled)
and in the controls without biochar amendment (n = 14/treatment). At the
beginning of the experiment (Week 0), before the sowing of radish (Week 5),
before the sowing of barley (Week 10), before the sowing of ryegrass (Week 20) and
after ryegrass was cut (Weeks 25, 26, 28, 29, 30). Statistically signicant differences
to the control are marked with an asterisk * (p < 0.05).
229
Table 2
Germination, biomass and nitrogen content of the lettuce and radish seedlings 14 and 11 days, respectively, after being sown (mean, n = 14). Statistically signicant differences
compared to the control are marked with an asterisk (* p < 0.05; ** p < 0.01).
20 g/L
80 g/L
Plant species
Treatment
Germinated seedlings
N (%)
Germinated seedlings
N (%)
Lactuca sativa
Control
BC300
BC375
BC475
Control
BC300
BC375
BC475
9.2
9.2
9.4
9.6
9.5
9.6
9.6
9.7
37.3
35.2
35.1
36.9
147.8
212.7**
215.4**
219.9**
6.4
6.4
6.6
6.8
7.7
7.6
7.4*
7.3**
9.1
5.9**
8.7
8.7
9.1
9.8
9.1
9.6
34.5
16.4**
27.2**
30.2
109.1
200.5**
208.4**
226.1**
6.4
5.7**
6.0
5.9
8.0
7.7
7.6*
7.2**
Raphanus sativus
Fig. 4. Root biomass (g dry weight/pot) of radish after 5 weeks of growth in the
control and biochar (BC300, BC375 and BC475) treated pots (mean SE, n = 14).
Statistically signicant differences to the control are marked with an asterisk
** (p < 0.01).
when yield in the control pots was signicantly lower than in the
BC300 and BC475 treated pots (p < 0.05). At the higher rate, the
effects became evident: for the rst harvest (3 weeks after sowing)
each biochar type reduced ryegrass biomass signicantly (0.34 g in
control pots and 0.19, 0.25 and 0.30 g in the BC300, BC375 and
BC475 treated pots, respectively, p < 0.005 in all cases) (Fig. 5).
Biomass in the BC300 treated pots was signicantly lower than in
the BC375 or BC475 treated pots (p < 0.05). During the study the
effect of biochar changed and at the last harvest, the yield was
0.87 g in control pots and 1.22, 1.35 and 1.29 g in the BC300, BC375
and BC475 treated pots, respectively (p < 0.001) (Fig. 5). When
ryegrass dry mass during the study period was analysed
cumulatively, all soils treated with biochar (BC300, BC375,
BC475) produced greater yields than the control (p < 0.001). There
were also differences between the biochar types: BC300 produced
lower yields than BC375 and BC475 (p < 0.01).
4.1.4. Effects on soil organisms
At the low application rate, none of the biochar types affected
soil microbial activity. However, at the higher rate, BC300 and
BC375 increased soil microbial activity ca. 42 and 46%, respectively
(p < 0.001 in both cases) ve weeks after placing in the soil
(Table 3). Ten and thirty weeks after mixing the biochar in the soil,
microbial activity did not differ between treatments (p > 0.05 in all
cases). In the separate laboratory study, each biochar types
released CO2 after distilled water was added to the dry biochar.
The amount of CO2 released varied signicantly between biochar
types, being 0.84 in BC300, 1.06 in BC375 and 0.31 mg C/g/h in
BC475 (p < 0.05 in each case). When comparing the transient
abiotic CO2 release from the pure biochar to the CO2 release from
230
Table 3
Mean (SE) microbial activity (mg C g1 dm soil h1) in biochar (BC300, BC375 and
BC485) treated pots at application rates 20 and 80 g L1 and control soils without
biochar amendment. Statistically signicant differences to the control are marked
with a (p < 0.01). Microbial activity of soils that received 20 g L1 biochar were
analysed within a week after sampling. Soils with 80 L1 biochar were stored in a
freezer (max. 2 months) until being analysed.
20 g L1
80 g L1
Control
BC300
BC375
BC475
Control
BC300
BC375
BC475
Week 5
Week 10
Week 30
0.32 0.02
0.27 0.02
0.32 0.07
0.22 0.01
0.14 0.01
0.24 0.04
0.26 0.05
0.15 0.01
0.46 0.09
0.50 0.05
0.49 0.04
0.46 0.04
0.39 0.05
0.44 0.03
0.50 0.05
0.32 0.03
1.32 0.07
1.33 0.06
1.48 0.07
1.56 0.12
0.76 0.03
0.64 0.04
0.58 0.07
0.55 0.10
a
a
the soil samples taken at weeks 5, 10 and 30, the abiotic release
corresponds to ca. 1.5-5% from the observed total CO2 release.
However, as the actual abiotic CO2 release from the biochar types at
5, 10 and 30 weeks after biochar application in the soil is not
known, the attribution of the observed degradation of biochar/CO2
release after biochar addition to abiotic causes is difcult. Thus the
abiotic release of CO2 was not taken into account in the microbial
activity calculations.
At the rst sampling event (Week 5) the number of nematodes
in soils varied between 3.3 and 5.6 individuals/g soil (dm). The
population of nematodes increased during the study being 9.717
and 3548 individuals/g (dm) at Week 10 and Week 30
(respectively) with no differences between control and biochar
treated soils (p > 0.05) (Table 4) or different biochar rates (20 g/L
and 80 g/L). Similarly, none of the biochar types inuenced the
functional group composition of the nematode community. At
Week 5, herbivores were the most prominent functional group. At
Week 10, bacterivores became more frequent, followed by
herbivores and fungivores (Table 4).
4.2. Earthworm studies
4.2.1. Earthworm toxicity test and soil WHC
Biochar types had no toxic effects on the earthworm Eisenia
foetida as deduced from mortality rates of the worms even in the
highest used concentration 102 g/L. As the mortality of earthworms during the 14 days test was <2% in control treatment, the
test met the validation criteria.
Biochar, irrespective of type, had a clear positive effect on soil
WHC. On average, 102 g/L of biochar application increased soil
WHC from 26% in the control soil to 36% in the biochar treated soils
(Fig. 6). The effect of biochar types on WHC of the treated soils did
not differ from each other.
Fig. 6. Effects of biochar application rate (x axis) and biochar types produced at
different temperatures (BC300BC475) on articial soil WHC in earthworm
avoidance study. Control columns (white bars) represent the containers without
biochar addition.
Table 4
Mean number (SE) of nematodes and the proportion (%) of various feeding groups in the biochar treated (BC300, BC375, BC475) and control pots at Weeks 4, 10 and 30 at
biochar application rate 80 g/L.
Individual g
Week 5
Week 10
Week 30
Control
BC300
BC375
BC475
Control
BC300
BC375
BC475
Control
BC300
BC375
BC475
3.3 0.6
3.3 0.6
5.6 1.2
4.4 0.8
9.7 2.7
17.6 5.5
14.4 2.6
15.5 3.0
35.9 4.6
39.8 14.3
37.8 12.0
48.0 13.7
1
dw
Bacterivore
Herbivore
Fungivore
Omnivore
Predator
28.3%
35.9%
41.2%
36.6%
85.3%
92.0%
92.5%
93.3%
86.2%
83.1%
83.5%
94.8%
63.4%
52.1%
51.1%
45.5%
12.3%
6.4%
5.4%
5.2%
7.7%
15.7%
13.9%
5.2%
8.3%
12.0%
7.1%
17.1%
2.1%
1.6%
1.8%
1.6%
6.2%
1.2%
2.5%
0.0%
0.0%
0.0%
0.5%
0.8%
0.3%
0.0%
0.3%
0.0%
0.0%
0.0%
0.0%
0.0%
0.0%
0.0%
0.0%
0.0%
0.0%
0.0%
0.0%
0.0%
0.0%
0.0%
0.0%
0.0%
231
that some phytotoxic compounds remained in the low temperature pyrolysed biochar in our study. Pyrolysis temperature may
affect, for example, the content of volatile organic compounds
(VOC) of biochar. Charcoal with high VOC content can show
negative effects on plant growth (Buss and Masek, 2014; Deenik
et al., 2010). Consequently, differences of VOCs in biochar can
contribute, at least partly, to the often observed differences in their
phytotoxicity (see Spokas et al., 2011). Our results support previous
ndings of e.g. Buss and Masek (2014) and Deenik et al. (2010) as
BC300 with the highest VOC content reduced lettuce germination
and/or growth more than birch wood biochar pyrolysed at higher
temperatures. We assume that some phytotoxic C compounds
remained in biochar produced at lower temperatures but that
these compounds are quickly volatilized in the air or degraded by
soil microbes. Since biochar containing VOC and other dissolved
organic compounds (DOC) that serve as a labile C source to soil
microbes, it is also possible that some of the N was incorporated
into the microbial biomass and was thus not available to plants,
which then decreased plant germination and growth (Deenik et al.,
2010). This conclusion is supported by increased microbial activity
(Week 5) in the soils applied with BC300 and BC375, containing
more labile C than BC475. Consequently, a stabilizing period of a
couple of weeks between the addition of biochar and the sowing of
seeds may help to reduce the phytotoxicity of biochar on plants.
It is also possible that lettuce is more sensitive to some
compounds or effects of biochar than the other plants used in the
current experiment. This warrants a new test with lettuce regrown
in the same soil. Furthermore, PAHs in biochar have been reported
to inhibit plant germination (Rogovska et al., 2011). However, in
our study, PAH concentrations of biochar did not correlate with the
germination of lettuce or radish. An obvious reason for this is that
all the tested biochar types had low total concentrations of PAHs
(Table 1). It is to be noted that the used biochar concentration
(80 g/L) showing phytotoxic effects of plants corresponds to 80 t/ha
at tillage depth of 10 cm, which is considered unrealistically high in
agricultural use.
Contrary to our hypothesis, none of the biochar types had an
effect on the survival of the earthworm E. fetida even at very high
concentrations (102 g/L). Liesch et al. (2010) also showed that
plant-based biochar had no effect on the survival of this
earthworm species. Interestingly, at the start of our experiment,
avoidance behavior increased with increasing pyrolysis temperatures, while later on the worms appeared to be more attracted to
soils with biochar produced at the highest pyrolysis temperature.
Partly supporting our results, Li et al. (2011) reported no effects of
10 g/kg of biochar on E. fetida, but the worms appeared to avoid the
same type of biochar at much higher rates (100 g/kg) unless the
biochar was wetted to its saturation point. The authors concluded
that drying of the soil due to the high rate of biochar was the main
cause for earthworm avoidance behavior. There is some evidence
suggesting that earthworms prefer, albeit only slightly, soils that
are amended with biochar to those without biochar (Chan et al.,
2008; Van Zwieten et al., 2010b). The short-term avoidance
behavior of earthworms in the current study may be due to slight
changes in the soil water potential, despite attempts to adjust soil
moisture separately in each pot according to the WHC of the soilbiochar mixtures.
Few data are available on biocharnematode interactions. Our
study showed that none of the biochar type exerted clear effects on
the total nematode abundance, suggesting that birch-produced
biochar, irrespective of pyrolysis temperature, is nontoxic to soil
inhabiting nematodes. Supporting our results, Zhang et al. (2013)
found no signicant effects of wheat straw biochar (400 C) on total
nematode abundance in stagnic anthrosols. Recently, reduced
number of root-knot and root-lesion nematodes in biochar treated
soils has been reported (George et al., 2016; Rahman et al., 2014).
232
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