Ecotoxicology and Environmental Safety 161 (2018) 290–295

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Ecotoxicology and Environmental Safety

journal homepage: www.elsevier.com/locate/ecoenv

“Assessing the potential of biochar and aged biochar to alleviate aluminum T

toxicity in an acid soil for achieving cabbage productivity”
Qingyi Lina, Lin Zhanga,b, Muhammad Riaza, Mengyang Zhanga, Hao Xiaa, Bo Lva,
⁎
Cuncang Jianga,
a
Microelement Research Center, College of Resources and Environment, Huazhong Agricultural University, Wuhan, Hubei 430070, PR China
b
Zhejiang Agricultural Technology Extension Center, Hangzhou 310020, PR China

A R T I C LE I N FO A B S T R A C T

Keywords: Biochar has a significant effect on alleviating acid soil aluminum (Al) toxicity and promoting plant growth. The
Aged biochar potential effects of aged biochar (long-term applied biochar in soil) on soil amendment have attracted increasing
Red soil attention. Here, the effects of biochar and aged biochar were evaluated through a pot experiment. The seedlings
Aluminum toxicity of cabbage were grown in red soil for 45 days with the following four biochar treatments: CK (0% biochar), PB
Cabbage
(2% primary biochar), WB (2% water washed biochar) and AB (2% acidulated biochar) to investigate the po-
tential effect of biochar and aged biochar on mitigating red soil aluminum toxicity and improving cabbage
growth. Results indicated that biochar increased the content of available potassium, available phosphorus, and
organic carbon in red soil and improved cabbage growth. Biochar not only increased the pH of red soil by 0.42
units, but also reduced exchangeable acid and exchangeable hydrogen (H+) content by 52.74% and 2.86%
respectively compared with CK. Additionally, the amount of the total active aluminum and exchangeable Al3+
were reduced by 26.74% and 66.09%, respectively. However, water washed biochar and acidulated biochar
decreased the effect of relieving the acidity substantially as compared to the primary biochar. Moreover,
acidulated biochar treatment increased the Al3+ content by 8.07% and trend of increasing soil available nu-
trients was declined with aged biochar. Taken together, it is concluded that biochar can reduce aluminum
toxicity by increasing pH of acid soil and available nutrients, thus improves cabbage growth. However, aged
biochar had a negative effect on aluminum toxicity reduction and acidic soil improvement, thus inhibited plant
growth.

1. Introduction
Biochar is a pyrogenic carbon-rich material, derived from the
thermal decomposition of biomass in a closed system with little or no
oxygen (Das et al., 2008; Lehmann et al., 2006; Van Zwieten et al.,
2010). Biochars with suitable physicochemical properties can improve
acidic soil pH, soil fertility, and can reduce the content of active alu-
minum (Al) in the soil, thus alleviating Al toxicity and promoting crop
growth (Alburquerque et al., 2014; Mukherjee et al., 2014; Dong et al.,
2016; Kopittke et al., 2015; Liu et al., 2016; Wang et al., 2015). Several
studies reported that biochar added into the soil under natural condi-
tions is very stable, but the circumstances of freezing and thawing, dry-
wet alternation etc. can affect the stability of the biochar in soil (Fierer
et al., 2002; Feng et al., 2007). After application into the soil, physical
and chemical properties of biochar would be altered in nature, which is
called aged biochar (Dong et al., 2017). Ren et al. (2016) reported that
wheat root biochar after being aged for three months lowered both
micropores and ash contents and remarkably influenced the physico-
chemical properties. The study of 13C synchrotron radiation to char-
acterize Amazon black carbon and by using HNO3/H2SO4 to simulate
the aging process showed that pH of the system was reduced by the loss
of alkaline elements during weathering process of biochar through the
CO2 dissolution and/or increasing the oxidation of C in the biochar with
the formation of surface oxygen-containing functional groups of car-
bonyl and carboxyl (Mao et al., 2010; Yao et al., 2010; Uchimiya et al.,
2011). Hale et al. (2011) reported that after chemical aging of biochar,
the sorption of pyrene was significantly reduced. Long-term biochar
application had no effect on improvement of soil physico-chemical
properties, but it could increase soil total organic carbon and available
potassium contents, and improve the average crop yield (Dong et al.,
2017).
Red soil in Southern China has a low pH, high alumina minerals,

⁎
Corresponding author.
E-mail address: jcc2000@mail.hzau.edu.cn (C. Jiang).

https://doi.org/10.1016/j.ecoenv.2018.06.010
Received 2 March 2018; Received in revised form 29 May 2018; Accepted 4 June 2018
Available online 08 June 2018
0147-6513/ © 2018 Elsevier Inc. All rights reserved.
Q. Lin et al.
and low effective nutrient contents (Zhu et al., 2015). Aluminum is
present in soil as insoluble oxides and aluminosilicates, however, as pH
drops below ≤ 5, soil acidy solubilizes it to Al3+ which is highly toxic
to plants and is a major limiting factor for plant growth and pro-
ductivity (Exley et al., 2012, Riaz et al., 2018a). Higher the con-
centration of soluble aluminum in soil, greater the toxicity of aluminum
to the plant growth will be, leading to loss of agricultural production
(Blaser et al., 2008). Aluminum phytotoxicity interrupts the normal
growth of plant roots, in turn, affects the whole plant's metabolism (Jia
et al., 2008). Haynes and Mokolobate (2001) found that the decom-
position of organic matter can increase soil pH and encourage Al3+
precipitation, while biochar can reduce exchangeable H+ and alu-
minum in the soil (Yuan et al., 2015). Abundant average annual rain-
fall, soil eluviation and consequences of acid rain are attracting great
attention (Zhao et al., 2013). In China, the main ions in acid rain are
SO42- and NO3-; therefore, to simulate biochar aging process, the
treatment of water washed and sulfuric acid/nitric acid are frequently
used (Qian and Chen, 2014). In recent years, researchers focused on the
changes of biochar's physical and chemical properties of aged biochar
(Chen et al., 2016). It is well known that biochar has an obvious effect
on improving the acidic soil. However, due to the complexity of soil
system in nature, the effectiveness of biochar on remediation of various
toxic metals as well as aluminum toxicity is still uncertain. Moreover,
there is lack of knowledge whether the biochar has the same potential
in alleviating acid soil aluminum toxicity and crop growth after biochar
aging. Thereby, a pot experiment on red soil amended with different
biochars was carried out to explore (1) the potential effect of biochar
and aged biochar on cabbage growth, and (2) to improve acid red soil
and to alleviate aluminum toxicity for achieving cabbage productivity.
2. Materials and methods
2.1. Samples collection
A typical acidic arable red soil sample (0–20 cm, topsoil) was col-
lected from hilly area of Ganzhou (Jiangxi province) (113°54′E,
24°29′N). The physicochemical properties of the soil are given as fol-
lows: the pH; 4.41, organic carbon; 5.06 g/kg, alkaline hydrolysable-
nitrogen; 32.34 mg/kg, available phosphorus; 3.35 mg/kg and available
potassium; 30.00 mg/kg. The soil samples were dried in a wooden tray
by spreading in a thin layer in a ventilated dry place, and stones, roots
and debris of plants were removed and soil samples were screened
through 2 mm sieve.
2.2. Biochar preparation
The biochar was obtained from Shenyang Agricultural University,
and was prepared from peanut shells at 400 °C. It was defined as the
primary biochar (PB) with pH 7.80. The PB was oxidized to simulate the
aging process in acidic environments according to Qian and Chen
(2014) method. A mixture of concentrated HNO3 and H2SO4 was se-
lected to oxidize primary biochars in acidic environments (acid rain),
because NO3− and SO42− were the main anions in acid rain in China.
Each biochar sample (5 g) was immersed in deionized water
(400 mL) and maintained at 70 °C for 6 h, followed by draining through
a 325 mesh sieve and then washing with 1 L of deionized water for 1 h
until a stable pH reading (7.80). This was defined as water washed
biochar (WB) with pH 7.80. To prepare acidulated biochar, biochar was
oxidized with the HNO3/H2SO4. Briefly, biochar (5 g) was immersed in
a 1:3 (v/v) mixture of HNO3/H2SO4, then diluted to 20%, and held at
70 °C for 6 h. The oxidized biochar was passed through a 325 mesh
sieve and then washed repeatedly with deionized water for 1 h until the
pH stabilized (2.68). This preparation was defined as acidulated bio-
char (AB) with pH 2.68. The elemental analysis of the biochar before
and after aging of biochar was performed as reported by Lin et al.
(2017).
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Ecotoxicology and Environmental Safety 161 (2018) 290–295
2.3. Experimental design
A pot experiment was carried out with 4 biochar treatments: CK
(control treatment without biochar), PB (2% primary biochar), WB (2%
water washed biochar), and AB (2% acidulated biochar). Each treat-
ment had 4 independent replications and the whole experiment con-
sisted of 16 pots and each pot had 20 cabbage seedlings. Both WB and
AB treatments represent the aged biochar treatments. Each pot was
filled with 1.5 kg of air-dried soil mixed thoroughly with biochar. The
fertilizers applied were 0.21 g/kg KH2PO4, 0.15 g/kg KNO3, 0.35 g/kg
Ca(NO3)2, 0.37 g/kg MgSO4·7H2O, and trace elements modified from
Anon nutrient solution (2.86 mg/kg H3BO3, 1.81 mg/kg MnCl2·4H2O,
0.22 mg/kg ZnSO4·7H2O, 0.08 mg/kg CuSO4·5H2O, 0.09 mg/kg
Na2MoO4, 48.5 mg/kg EDTA-Fe). Pots were irrigated daily to avoid
desiccation. A Chinese cabbage (variety: a 28 fast-growing cabbage)
was grown in red soil with different biochar treatments for 45 days
under natural conditions in a greenhouse at Huazhong Agriculture
University, Wuhan, China.
2.4. Sample collection and measurement
2.4.1. Plant samples and measurement
At the end of the experiment, the plants were harvested from the
pots. The plant growth parameters such as leaf number, leaf area, fresh
and dry biomass, and root length were measured. The active aluminum
content in cabbage was quantified by the method proposed by You
(1997).
2.4.2. Soil samples and measurement
After harvesting the cabbage seedlings from the pots, soil samples
were collected to determine the conventional physical and chemical
indexes as well as active soil aluminum contents. The conventional
physicochemical characteristics of the soil were quantified as reported
by Bao (2000).
2.4.3. Soil physicochemical analysis
Briefly, soils were dried at 105 °C for 48 h for physicochemical
properties. The pH was determined in a 1:2.5 soil/water suspension
with a digital pH meter (FE20/EL20, Shanghai Mettler Toledo Co.,
China). The soil available potassium was extracted with ammonium
acetate and measured with a flame photometer (AP-1200, Shanghai
Precision Instrument Co., China). The available phosphorus was ex-
tracted with sodium bicarbonate and determined with ultraviolet
spectrophotometry (TU-1810, Beijing Pgeneral Instrument Co., China).
The soil alkali-hydrolysable nitrogen was measured with alkaline hy-
drolysis diffusion method and the soil organic matter contents were
determined with potassium dichromate volumetric method.
Soil exchangeable acid and exchangeable hydrogen (H+) were de-
termined through titration (pH 7.0) method using 0.02 mol/L NaOH
after being extracted with 1.0 mol/L KCl.
Proportions of soil aluminum were determined through ultraviolet
spectrophotometry (TU-1810, Beijing Pgeneral Instrument Co., China)
after being extracted with four leaching extraction reagents (KCl,
NH4AC, HCl and NaOH). Detail is provided in the Table S1 (Pang et al.,
1986).
2.4.4. Soil infrared spectrum analysis
The soil was air-dried and sieved through 100 mm sieve at room
temperature. Functional groups associated with soil were measured
with Fourier transform infrared (FTIR) analysis using a VERTEX 70
(Brooker Instrument, Thermo Co., USA). The soil sample was mixed
with potassium bromide powder (KBr) at the ratio of 1% by weight and
ground in an agate mortar. The spectrum was normalized between the
fingerprint regions of 4000–400 cm−1 with a resolution of 4.0 cm−1.
Q. Lin et al. Ecotoxicology and Environmental Safety 161 (2018) 290–295

Table 1
The effect of biochar and aged biochar on growth traits of cabbage exposed to different biochar treatments.
Treatment Emergence ratio Leaf number Leaf area (cm2) Root length (cm) Fresh weight (g) Dry weight (g)

CK 95.00a ± 4.08 3.00b ± 0.00 1.70b ± 0.10 1.60c ± 0.30 0.40c ± 0.03 0.04c ± 0.00
PB 90.00a ± 7.07 4.75a ± 0.50 7.20a ± 1.40 4.10a ± 0.30 3.20a ± 0.48 0.31a ± 0.05
WB 90.00a ± 5.00 3.25b ± 0.50 6.80a ± 1.20 3.40b ± 0.40 1.90b ± 0.29 0.18b ± 0.03
AB 90.00a ± 7.07 3.25b ± 0.50 1.80b ± 0.30 1.70c ± 0.50 0.40c ± 0.04 0.04c ± 0.00

Cabbage was exposed to the biochar treatments as CK (0% biochar), PB (2% primary biochar), WB (2% water washed biochar) and AB(2% acidulated biochar) for 45
days in acid red soil. Values are means of four replicates ± S.E. Columns with different lower case letters (a, b, c, d) are significantly different using the T-test at (
P < 0.05).

2.5. Statistical analysis and data processing

Soil total active aluminum was extracted with NaOH. The propor-
tion of active aluminum in different forms: the content of aluminum in
each form / soil total active aluminum.
The statistical analysis software “SAS 9.1.3” was used to examine
the mean values and standard deviation of each processed data. Tukey's
multiple range test (p < 0.05) was utilized to check significant dif-
ferences among average values of treatments. The FTIR data were
processed with the Microsoft Excel software and OMNIC 8 software,
and plotted with Origin 8.6 “U.S.A, Origin Lab Corp”.

3. Results

3.1. Plant growth and composition
The results showed that biochar application has significantly influ-
enced the growth of cabbage (Table 1, Fig. S1). Primary biochar (PB,
2% biochar) significantly improved the growth of cabbage and accu-
mulated greater biomass as compared to the control treatment. In ad-
dition, PB treatment considerably increased the leaf number, leaf area,
root length, fresh weight and other agronomic traits of cabbage
(Table 1). However, with the aging of biochar, the trend of increasing
plant growth was decreased. Waster washed biochar (WB) and acidu-
lated biochar (AB) remarkably inhibited cabbage growth and related
growth parameters (Table 1), however, such negative effects were more
prominent with the acidulated biochar (AB) as compared to PB treat-
ment. Compared to the control, the fresh weight of cabbage was no-
ticeably enhanced with the addition of biochar (PB, WB). The fresh
weights of PB and WB were increased by 600% and 375% respectively,
while that of AB did not cause any significant effect when compared
with CK. The results indicated that the growth of seedlings under pri-
mary biochar (PB) was better than that of WB and AB treatments (Fig.
S1).
3.2. Aluminum content of cabbage
The results depicted in Fig. 1 (Table S3) indicated that the treat-
ments of PB, WB and AB reduced aluminum content in the plants by
39.76%, 26.69% and 12.63% compared to CK treatment, indicating
that biochar can reduce the uptake of aluminum from the soil, which in
turn decrease aluminum contents in the plant parts. The effects of re-
ducing aluminum uptake is ranked as PB≥WB ≥AB compared to the
CK, indicating that aging of biochar gradually exhibited lower effect in
reducing aluminum contents in plants. The results indicate that as aging
of biochar proceeds, biochar loses its potential to mitigate toxicity of
aluminum i.e. from WB to AB.
3.3. Soil properties and functional groups
Fig. 1. Alumnum content of cabbage that was exposed to different biochar
treatments as CK (0% biochar), PB (2% primary biochar), WB (2% water wa-
shed biochar) and AB (2% acidulated biochar) for 45 days in acid red soil.
Values are means of four replicates ± S.E. Columns with different lower case
letters (a, b, c, d) are significantly different using the T-test at ( P < 0.05).
(Table 2). However, AB treatment reduced acid soil pH by 0.28 units,
indicating that effect of biochar on increasing soil pH decreases as the
biochar being aged. Similarly, PB and WB treatments improved the soil
available potassium, available phosphorus, and organic matter contents
compared to the control treatment. Besides, treatments of PB and WB
remarkably decreased the content of alkaline hydrolysable nitrogen
(N), while AB treatment increased N contents compared to the CK in-
dicating that with the aged biochar, the trend of enhancing available
nutrients decreased while enhanced available N. Therefore, aged bio-
char has a significant impact on red soil pH, soil available potassium,
available phosphorus, alkaline hydrolysable nitrogen, and organic
carbon content.
The influence of aged biochar on soil surface functional groups was
further explored by fourier transform infrared spectral analysis. As
shown in Fig. 2, the main absorption bands of red soil were located
between 3600 and 3700 cm−1, representing a corresponding clay hy-
droxyl absorption band (Peng et al., 2013) and 1000–1080 cm−1 in-
dicates C‒O absorption band of cellulose (Calderón et al., 2011). The
absorption peaks near 3700, 3620, 1000, 913, 471, 428 cm−1 had si-
milar absorption vibration peaks (Table S2). Among them, 913 cm–1
was attributed to Al‒O‒Al stretching vibration peak and 471 cm−1 was
assigned to the Si‒O‒Si stretching vibration peak (Sheng et al., 2016).
Compared with CK, the PB treatment did not create or destroy any
absorption peaks. However, the WB treatment elevated Si‒O‒Si
stretching vibration peak (Sheng et al., 2016) near 1100 cm−1 and
1090 cm−1. The vibration absorption peak was missing at 1110 cm−1
in the AB treatments, only Si‒O‒Si peaks and stretching vibration peaks
near 1090 and 1090 cm –1 were found to be increased (Sheng et al.,
2016).

The application of biochar has a significant influence on increasing

of available nutrients in acid red soil. Interestingly, in contrast to CK, 3.4. Soil potential acid
pH of PB and WB treatments were increased by 0.42, 0.26 units re-
spectively, illustrating that biochar can increase the pH of acidic soil The treatments of PB and WB indicated a decreased amount of red

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Table 2
The physical and chemical properties of acid red soil under different treatments of biochar.
Treatment pH Available potassium (mg kg−1) Available phosphorus (mg kg−1) Available nitrogen (mg kg−1) Organic matter (g kg−1)

CK 4.50c ± 0.08 105.6c ± 3.3 6.77b ± 0.31 33.83b ± 2.02 6.60d ± 0.26
PB 4.92a ± 0.08 183.9a ± 14.1 8.94a ± 0.80 22.17c ± 2.02 16.95ab ± 0.68
WB 4.76b ± 0.07 131.1b ± 6.3 7.36b ± 0.72 23.63c ± 1.75 13.54c ± 0.44
AB 4.22c ± 0.05 112.0c ± 5.1 7.22b ± 0.66 51.63a ± 1.75 14.87b ± 0.26

Cabbage was exposed to the biochar treatments as CK (0% biochar), PB (2% primary biochar), WB (2% water washed biochar) and AB (2% acidulated biochar) for 45
days in acid red soil. Values are means of four replicates ± S.E. Columns with different lower case letters (a, b, c, d) are significantly different using the T-test at (
P < 0.05).

3.5. Different form of soil aluminum

As shown in Fig. 4a (Table S3), biochars can substantially reduce the

Fig. 2. The FTIR average spectra of functional groups of soil exposed to dif-
ferent biochar treatments as CK (0% biochar), PB (2% primary biochar), WB
(2% water washed biochar) and AB (2% acidulated biochar) for 45 days in acid
red soil. Values are means of four replicates ± S.E.
soil exchangeable acid by 52.74% and 22.83% respectively as com-
pared to the CK (Fig. 3a, Table S3). However, AB treatment increased
the exchangeable acid by 8.45%, suggesting that aged biochar could
significantly reduce the soil exchangeable acid. With water washed
biochar, the effect of decreasing exchangeable acid was substantially
weakened. The change of the amount of total soil exchangeable H+
showed a similar changing trend as exchangeable acid (Fig. 3b, Table
S3). Compared with CK, magnitude of red soil exchangeable H+ was
declined by 2.86% and 40.0% under the PB and WB treatments, re-
spectively, while AB treatment elevated by 60%, demonstrating that
with the addition of WB, the content of total soil exchangeable H+
dropped sharply but that of AB showed a rising trend.
total active Al content in soil. Interestingly, when compared with CK,
the total active Al content of PB treatment declined by 26.74% while
that of WB and AB treatments dropped by 21.44% and 13.84% re-
spectively, suggesting that biochar has a potential to lower soil total
active Al content. The results further indicated that the aged acidulated
biochar (AB) not only tended to increase the active Al content but also
total exchangeable aluminum in the soil when compared to PB and WB
treatments.
Among all biochar treatments, colloidal Al(OH)30 and phytotoxic
exchangeable Al3+ were the main forms of active Al, while mono hy-
droxyl Al ions and humic acid-Al occupied a small proportion, as shown
in Fig. 5. When compared with CK, PB and WB treatments increased
mono hydroxyl Al ions and colloidal Al(OH)30 contents in red soil, but
decreased the content of exchangeable Al3+ and humic acid-Al. This
indicates that the treatment of PB and WB can change various forms of
Al in the soil. There is a certain transformative relationship between
each form of Al. Among them, Al3+ is the most bio-toxic form of Al in
the red soil, which was greatly declined by PB and WB.
Fig. 4b (Table S3) shows that the content of exchangeable Al3+ for
PB and WB was declined by 66.09% and 42.70% respectively, while AB
treatment increased by 8.07% as compared to CK demonstrating that
biochar could dramatically diminish the Al3+ content in soil, thus al-
leviating Al toxicity. Both PB and WB treatments can mitigate Al toxi-
city by inhibiting the increase of exchangeable Al3+. Moreover, the
content of acidulated biochar treatment severally accumulated Al3+,
and thus triggered the toxicity of Al in red soil.
4. Discussion
As expected, the treatments of primary biochar, water washed
biochar, and acidulated biochar significantly improved the content of
soil available potassium, available phosphorus, and organic carbon.

Fig. 3. The total content of soil exchangeable acid (A) and the content of soil exchangeable H+ (B). Cabbage was exposed to the biochar treatments as CK (0%
biochar), PB (2% primary biochar), WB (2% water washed biochar) and AB (2% acidulated biochar) for 45 days in acid red soil. Values are means of four
replicates ± S.E. Columns with different lower case letters (a, b, c, d) are significantly different using the T-test at ( P < 0.05).

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Q. Lin et al.
Fig. 4. The effect of biochar and aged biochar on total active Al content (A) and exchangeable Al3+ content (B) of the red soil. Cabbage was exposed to the biochar
treatments as CK (0% biochar), PB (2% primary biochar), WB (2% water washed biochar) and AB (2% acidulated biochar) for 45 days in acid red soil. Values are
means of four replicates ± S.E. Columns with different lower case letters (a, b, c, d) are significantly different using the T-test at ( P < 0.05).
Fig. 5. The effect of biochar on the percentage of active Al of the red soil. CK,
PB, WB and AB are treatments of without biochar, 2% primary biochar, 2%
water washed biochar and 2% acidification biochar, respectively.
Gaskin et al. (2008) found that biochar contains a certain amount of
mineral nutrients, and thus has the potential to increase soil mineral
nutrients. It might be due to the fact that biochar likely transforms soil
mineral elements, which further increases the soil available nutrients
(Williams et al., 1988; Li et al., 2017). With the aged biochar, the trend
of increasing soil available nutrients was reduced. The reason could be
that the microporous structure of biochar damages in the process of
aging, leading to loss of nutrients and weakened the effect of holding
soil nutrient ion on the soil surface (Lin et al., 2017). Therefore, the
damaged biochar structure by the process of aging could not effectively
reduce the leaching of soil nutrient. The addition of primary and waster
washed biochar (to less extent) tended to increase soil pH and decrease
available N content, while AB treatment lowered soil pH and raised the
available N content when compared with CK. This indicates that porous
structure and large surface area of biochar immobilize ammonium N
and inhibit nitrification (Nelissen et al., 2012; Pocknee et al., 1997),
thereby leading to amelioration of soil acidity. The study results also
show that acid red soil mainly contains clay hydroxyl and cellulose C‒O
groups (Fig. 2). The amount and type of functional groups of PB in the
soil did not show much difference with the CK, while with the aged
biochar, the number of functional groups and Si‒O‒Si absorption peaks
increased in the WB and AB treatments. Qian et al. (2013) found that
aluminum in the soil and the silicon in rice straw biochar form silicon-
aluminum complex, thereby alleviating toxic aluminum. This may be
caused by the transformation between effective and soluble silicon in
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Ecotoxicology and Environmental Safety 161 (2018) 290–295
the soil.
In this study, the growth of cabbage was dramatically hampered in
the red soil. However, it was noted that application of biochar sub-
stantially improved plant growth, but under water washed biochar and
acidulated biochar, cabbage growth promoting effect was weaker than
PB. Studies have found that biochar can promote root growth and in-
crease crop yield (Major et al., 2010; Qian et al., 2016; Zhang et al.,
2012). It is likely to be caused by oxidation/mineralization effect and
nutrient elements released during aging process of biochar (Lin et al.,
2017). Biochar amended to soil can significantly reduce the uptake of
aluminum content in plant parts in the acid red soil. Yao (2010) pro-
posed that biochar releases alkaline elements and further acts as liming
for the amelioration of soil. The reason might be that the biochar can
alleviate aluminum toxicity and promote crop growth (Yao et al., 2010;
Biederman et al., 2013). Thereby, biochar relieves plants from the toxic
effect of Al by decreasing its concentrations. However, at low pH,
aluminum can easily be absorbed by plants and inhibit root and plant
growth (Haug and Caldwell, 1985, Riaz et al., 2018b)
After the aging of biochar, water washed biochar still has the po-
tential to reduce the soil exchangeable Al and active Al content, thereby
alleviating Al toxicity. Whereas, acidulated biochar decreased soil total
active Al content, increased the content of exchangeable Al, and so
exacerbated the Al toxicity. Aluminum normally exists in silicate or
other forms of silicate and is present in nontoxic form of Al (Kochian
et al., 2005; Ma, 2007). However, under the condition of acidic soil
(pH < 5.5), solubility of Al3+ greatly increases and ultimately exerts
toxicity disorders to plant (Kochian et al., 2005; Ma, 2007, Riaz et al.,
2018b). This may be related to the role of biochar in reducing soil
exchangeable acid and A13+ content. The exchangeable Al3+ is a key
factor in acidic soils; greater the degree of soil acidity, higher ex-
changeable Al3+ content will be and more serious aluminum toxicity.
This is probably the reason that acidulated biochar can reduce the total
soil active Al content, but cannot alleviate Al toxicity. Qian and Chen
(2014) found that with water washed biochar, the adsorption effect of
Al in the solution is reduced while acidulated biochar increased the
adsorption effect of Al caused by increased amount of carboxylic acid
functional groups. It can be proposed that Al adsorption mechanism of
biochar is different under different environmental conditions. Our re-
sults exhibited that after adding biochar to the soil, the exchangeable
Al3+ and humic acid Al content decreased, while mono Al and colloidal
Al, hydroxyl Al ions content were found to be increased. Moreover,
with the aging of biochar, the degree of exchangeable Al3+ content was
decreased, and also affected other forms and proportions of Al. It has
been reported that with the increase of the solution pH from 4.3 to 5.5,
the concentration of Al3+ in the solution decreases, while the con-
centration of Al(OH)2+ and Al(OH)2+ of Al increases (Qian et al.,
2013). This suggests that the increase of pH decreases the solubility of
Q. Lin et al.
Al3+ or results in the complexation between aluminum forms, such as
Al(OH)2+, A1(OH)2+ and Al(OH)3. All of these changes with the in-
crease of pH play an important role in reducing Al concentration that
could be an effective phenomenon in lessening toxicity of aluminum in
the soil and subsequently in plants (Naramabuye et al., 2006).
5. Conclusion
The results of the present study demonstrated that the addition of
biochar improved nutrient status of an acid soil and reduced aluminum
availability by increasing soil pH which ultimately reduced the alu-
minum content in the plant parts and improved cabbage growth.
However, aged biochar exhibited reduced amount of soil available
nutrients and soil active acid and potential acid content. Aged biochar
not only weakened the declining trend of biotoxic Al3+ content but also
increased the content of Al3+ and aggravated Al toxicity in the soil.
Moreover, aged biochar aggravated acidity of soil. Therefore, in con-
clusion, it could be proposed that biochar can improve soil and in turn
improves plant growth while with the aging of biochar decreases its
ability to lower soil phytotoxic exchangeable Al3+ content, soil pH and
exacerbates aluminum toxicity thus reducing plant growth and its
productivity.
Acknowledgements
This work was funded by “National key research and development
plan of China (2017YFD0200803)” and the “Research Special of Public
Welfare Industry (Agriculture) of China (201303095)”.
Appendix A. Supporting information
Supplementary data associated with this article can be found in the
online version at http://dx.doi.org/10.1016/j.ecoenv.2018.06.010.
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