Biochar (2021) 3:135–147

https://doi.org/10.1007/s42773-021-00085-3

ORIGINAL RESEARCH

Moderate sewage sludge biochar application on alkaline soil for corn

growth: a field study
Shengyu Xie1,2 · Guangwei Yu1 · Ruqing Jiang1 · Jianli Ma3 · Xiaofu Shang3 · Gang Wang1 · Yin Wang1 · Yongan Yang4 ·
Chunxing Li5

Received: 2 October 2020 / Accepted: 12 January 2021 / Published online: 19 February 2021
© The Author(s) 2021

Abstract
In view of the risks induced by the inhibitory effects of applying impracticably large amounts of sewage sludge biochar (SSB)
to the alkaline soil, this field study investigated the influence of moderate biochar amendments (0, 1500, 4500, and 9000 kg/
hm2) on corn growth, alkaline soil properties, and the uptake of potentially toxic elements (PTEs). The results showed that
applying more SSB would decrease the ammonium nitrogen concentration and increase the available phosphorus and potas-
sium concentrations, which inhibited corn plant growth because of high background nutrient levels of the alkaline soil. When
the alkaline soil was amended with 1500 kg/hm2 SSB, the dry weight of 100 niblets increased from 32.11 g in the control
to 35.07 g. There was no significant variation in the total concentration of PTEs in the soil. The concentrations of Mn, Ni,
Cu, and Zn in niblets decreased from 5.54, 0.83, 2.26, and 27.15 mg/kg in the control to 4.47, 0.62, 1.30, and 23.45 mg/kg,
respectively. Accordingly, the health risk from corn consumption was significantly reduced. Furthermore, the combination of
SSB and fertilizer improved corn growth and reduced the risk of consumption of PTEs. Therefore, considering the increase
in corn fruit yield and the decrease in consumption risk, applying 1500 kg/hm2 of biochar to alkaline soils is a realistically
achievable rate, which can broaden the utilization of SSB for remediation of different types of soil.

Keywords Sewage sludge biochar · Alkaline soil · Corn growth · Soil property · Potentially toxic elements · Soil
remediation

Abbreviations 1 Introduction
SSB Sewage sludge biochar
PTE Potentially toxic element Pyrolysis is a proven and promising technology for the harm-
EC Electrical conductivity free treatment of sewage sludge while generating functional
EDI Estimated daily intake products such as biochar, oil, and gas. In slow pyrolysis with
HQ Hazard quotient a low heating rate (< 10 °C/min) and long residence time
(> 1 h), biochar is the main byproduct (Oni et al. 2019).
Converting sewage sludge into sewage sludge biochar (SSB)
* Guangwei Yu has additional advantages such as volume reduction, pol-
[email protected]
lutant elimination, and nutrient retention (Wu et al. 2019).
1
CAS Key Laboratory of Urban Pollutant Conversion, Additionally, some potentially toxic elements (PTEs: Cr,
Institute of Urban Environment, Chinese Academy Mn, Ni, Cu, Zn, As, Cd, and Pb) in untreated sewage sludge
of Sciences, Xiamen 361021, China can cause potential threats to humans via the food chain
2
Graduate School of Environmental Studies, Tohoku (Khan et al. 2020). In our previous study, we studied the
University, 6‑6‑07 Aoba, Aramaki‑aza, Aoba‑ku, Sendai, migration and transformation behavior of PTEs in the sew-
Miyagi 980‑8579, Japan
age sludge pyrolysis process from laboratory- to pilot-scale
3
Tianjin Academy of Environmental Sciences, experiments, and found that most of the PTEs remained in
Tianjin 300191, China
the SSB and were converted from bioavailable fractions to
4
Tianjin High Quality Agricultural Products Development a more stable fraction combined with silicate minerals (Li
Demonstration Center, Tianjin 301508, China
et al. 2018a, 2021; Xie et al. 2020a). Considering the high
5
Department of Environmental Engineering, Technical
University of Denmark, 2800 Kongens Lyngby, Denmark

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136 Biochar (2021) 3:135–147

concentrations of PTEs in SSB, its proper utilization still the development of local agricultural production (Liu et al.
attracts much attention and requires further investigation. 2020), and SSB may have a positive effect in alkaline soils
Currently, the application of biochar for soil remediation because of its pore structure, functional groups, and nutri-
is an attractive method with numerous benefits. For example, ents. However, based on a field soil study considering the
the porosity of biochar can increase the water-holding capac- volume and cost of biochar, 5–10 wt% SSB (~ 100,000 kg/
ity and decrease the bulk density of soil, which increases hm2) is not practicable (Kocsis et al. 2020; Zhang et al.
vegetable productivity and reduces irrigation frequency (Liu 2016). Additionally, excessive application of SSB adversely
et al. 2020). Functional groups such as –COO− and O ­ − in affects plant growth and PTE availability if the soil pH is
+
the surface of biochar can react with ­H in soil to improve greater than 8.0 (Artiola et al. 2012). Therefore, the applica-
the buffering capacity of soil (Wu et al. 2020b). Addition- tion of moderate levels of SSB (< 10,000 kg/hm2) to alkaline
ally, the chemical properties and enzymatic activities of the soil is worthy of further attention for broadening the utiliza-
soil are significantly improved after biochar amendment tion of SSB on different types of soil.
(Pokharel et al. 2020; Rafael et al. 2019). Biochar can also In view of the few reports in this regard, a field trial was
reduce the bioavailability and toxicity of soil by adsorbing conducted to study the effect of moderate SSB addition on
and degrading organic contaminants (Wu et al. 2020a). the alkaline soil for corn planting. We analyzed the influ-
SSB differs from other types of biochar, and further inves- ence of SSB on soil properties, including water retention,
tigation is needed on the safety of SSB with high PTE con- pH, electrical conductivity (EC), and nutrient content during
centrations applied to large-scale plantings (Purakayastha corn growth. Furthermore, the concentrations and chemical
et al. 2019). It has been reported that excess PTEs have a speciation of PTEs in soil were also studied to investigate
negative effect on vegetative growth. More specifically, their accumulation in corn fruits and the potential health
excess Zn can cause chlorosis in plant leaves, excess Cu may risks posed to humans. Our primary objective was to verify,
cause negative effects on plant nutrients, and large amounts in a field study, whether moderate applications of SSB are
of Ni and Co can reduce seed germination and inhibit the suitable for alkaline soils.
growth of plant tissues (Khan et al. 2020; Mohamed et al.
2017). Therefore, several studies have been conducted to
investigate the accumulation of PTEs in plant tissues after 2 Materials and methods
addition of biochar to soil. The results showed that biochar
significantly decreased the concentrations of mobile frac- 2.1 Biochar and planting location
tions (water-soluble, exchangeable, and bound-to-carbonate
fractions) of Ni, Zn, Cd, and Pb in soil, and reduced their SSB was prepared by pyrolysis of hydrothermally treated
concentrations in oilseed rape tissues (Shaheen and Rinklebe sewage sludge at 600 °C for 45 min in a sewage sludge
2015; Shaheen et al. 2015). Khan et al. (2013) found that treatment plant in Xiamen City, Fujian Province, China, to
5–10 wt% SSB amendment decreased the uptake of some reduce the pollutant risk (Li et al. 2018a; Tian et al. 2019).
PTEs (As, Cr, Co, Ni, and Pb) in rice tissues as a result of The obtained biochar was ground and passed through a
increasing the pH, cation exchange capacity, pore structure, 3.2 mm sieve prior to use in the field trial. The planting
and dissolved organic carbon concentration of acidic soil. In experiment was conducted at a national corn farm in Tian-
addition, the reduction in PTE bioaccumulation of SSB has jin, China (39°25.459 N, 117°29.295 E), where the annual
been verified in other plants such as grass, Chinese cabbage, average temperature is 12–15 °C and the total annual pre-
and tomato (Hossain et al. 2010; Yu et al. 2018; Yue et al. cipitation is 550–600 mm, with a temperate continental
2017). In our previous study, we found that 5–10 wt% SSB monsoon climate. The basic properties of the soil and SSB
is the suitable proportion to use in soilless cultivation, and are described in Table 1.
only small amounts of the PTEs in biochar were taken up by
cucumber plants (Xie et al. 2020b). Nonetheless, the health 2.2 Field trial
risk associated with food consumption from applying SSB to
agriculture needs further verification based on a field study. Four different treatments with SSB amendments (0 [CK],
Most studies have focused on the effect of biochar addi- 1500 [C1], 4500 [C3], and 9000 kg/hm2 [C4]) were used to
tion on acidic and infertile soils (Mohamed et al. 2017; Wu investigate the influence of SSB addition on alkaline soil
et al. 2020b). The observed benefits are that the addition of properties and corn growth under normal fertilization con-
alkaline biochar can significantly increase soil pH, which ditions. Additionally, to study the influence of fertilization,
influences the microbial response and PTE solubility (Zhu treatment with 1500 kg/hm2 SSB application without fer-
et al. 2017). In northern China, where corn is the main crop, tilization (C2) was established. The total length and width
most soils are alkaline, containing ­NaCO3 and ­NaHCO3. of the trial site were 65 m and 26 m, respectively. The area
Low water retention and organic matter levels also restrict of each treatment was approximately 333 m2, which was

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Biochar (2021) 3:135–147 137

Table 1  Basic properties of the soil and sewage sludge biochar soil surface, and an agricultural rotary tiller was used to
Items Soil SSB Items (mg/kg) Soil SSB
mix the surface soil and SSB fully (15 cm in depth). The
row spacing for corn sowing was 60 cm. The corn growth
pH 7.65 8.13 Cr 62.62 9623.30 period was divided into the initial stage (before seeding),
EC (mS/cm) 2.06 2.68 Mn 433.83 958.65 budding stage, jointing stage, filling stage, and maturity
C (%) 1.27 7.81 Ni 22.77 1409.99 stage. Water management was conducted according to the
H (%) 1.19 1.32 Cu 14.82 8608.33 practical operation of the local farm. At the initial stage,
N (%) 0.38 0.35 Zn 79.37 8293.10 600 kg/hm2 of base fertilizer (N–P2O5–K2O ≥ 46%) was
S (%) 0.09 1.71 As 44.88 39.97 added to the top 10–15 cm of soil. Additionally, 450 kg/
K (g/kg) 23.02 9.93 Cd –a 2.32 hm2 of urea (N ≥ 46%) was added after the jointing stage.
P (g/kg) 1.56 47.62 Pb 21.52 130.23 At each growth stage, approximately 1 kg of soil sample
a
Not detected was collected by the quartering method in each zone. Corn
fruits, including niblets and corncobs, were collected sepa-
rately after harvest. All samples were transferred to the
divided into three zones, as shown in Fig. 1. Before sow- laboratory for further analysis. Photographs of the field
ing corn seeds (Jingnongke 728), SSB was added to the plantings are shown in Fig. 1.

Fig. 1  Schematic diagram and

photographs of the field plant-
ings

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138 Biochar (2021) 3:135–147

2.3 Analysis methods where ­ConPTE, ­IRniblet, and BW represent the PTE concentra-
tion in niblets (mg/kg), the corn intake rate [398.2 g/adult/
After corn maturity, nine plants were randomly selected day (Zheng et al. 2007)], and average body weight [56.8 kg
from each treatment. The height of each plant was meas- (Khan et al. 2014)], respectively.
ured from the soil surface to the uppermost growing point.
The leaf area was calculated from the maximum length and
HQ = EDI / Rf D, (2)
width. The stem diameter was measured at a location 1 cm where ­RfD represents the oral reference dose, and the values
below the largest leaf. Further details have been described of Cr, Mn, Ni, Cu, Zn, As, Cd, and Pb are 1500, 140, 20,
in our previous study (Xie et al. 2020b). The dry weight of 40, 300, 0.3, 3, and 3.5 µg/kg/day, respectively (Khan et al.
100 niblets was measured and used as an important growth 2020; Shehata and Galal 2020).
parameter. The obtained soil and corn fruits were dried
until their weight could be determined, then ground, sieved
(< 0.15 mm), and stored in a vacuum desiccator. The mois- 2.5 Statistical analysis
ture content of the soil was determined by the mass differ-
ence before and after drying at 105 °C for 12 h according All statistical tests were performed using the Statistical
to the Chinese standard (NY/T 52–1987). The pH and EC Package for the Social Sciences (SPSS) Version 20.0.
of the soil were measured with a pH meter (Ultra Basic, One-way analysis of variance (ANOVA) and Tukey’s hon-
US) and a conductometer (Teltracon 325, Germany), respec- est significant difference test were used to determine the
tively, according to the Chinese standards (NY/T 1377–2007 differences in treatments. Data from different treatments
and HJ 802–2016). The concentrations of nutrient elements showed significant differences when P was less than 0.05.
(ammonium nitrogen, available phosphorus, and available Pearson correlation was used to show the relationships
potassium) were measured by a colorimetric method using between soil properties and the chemical speciation of
a high-precision soil fertilizer nutrient meter (HMQ800, PTEs.
China). The total concentrations of PTEs (Cr, Mn, Ni, Cu,
Zn, As, Cd, and Pb) were digested using a mixture of nitric
acid, perchloric acid, and hydrofluoric acid (5:5:2, v/v/v)
in a graphite digester at 190 °C. The chemical speciation 3 Results and discussion
(F1: exchangeable, F2: reducible, F3: oxidizable, and F4:
residual fractions) was determined by a three-step extraction 3.1 Effects of SSB amendments on corn growth
procedure. The samples (0.5 g) were extracted in turn using
20 mL of acetic acid (0.11 mol/L), 20 mL of hydroxylamine The effects of SSB additions on different growth parameters
hydrochloride (0.5 mol/L), 10 mL of hydrogen peroxide after maturity are shown in Fig. 2. An increased amount of
(30%) digestion, and 25 mL of ammonium acetate (1 mol/L). SSB amendment (≥ 4500 kg/hm2) significantly decreased
Detailed information has been reported in the previous study the plant height, leaf area, and stem diameter of corn plants
(Xie et al. 2019, 2020b). Specifically, F1 is the fraction from (Fig. 2a–c). Additionally, treatment without fertilization
acid-soluble or carbonate-combined metals, F2 is the frac- (C2) markedly inhibited the growth of corn leaves. A small
tion combined with iron and manganese oxides, F3 is the leaf area indicates weakening of chlorophyll synthesis and
fraction associated with sulfur or organic matter, and F4 is photosynthesis during growth (Li et al. 2018b). However,
the fraction bound to silicate minerals. All solutions were the variation in dry weight of 100 niblets after SSB applica-
tested with inductively coupled plasma mass spectrometry tion was not affected by inferior plant height, leaf area, and
(ICP-MS, Agilent 7500cx, USA) after filtration. stem diameter, as shown in Fig. 2d. The dry weight of 100
niblets of corn plants increased by 9.2%, 6.4%, and 7.1%,
2.4 Health risk assessment respectively, with the addition of 1500, 4500, and 9000 kg/
hm2 of SSB (C1, C3, and C4 treatment) compared with CK.
The estimated daily intake (EDI) and hazard quotient (HQ) Moreover, the absence of fertilizer (C2) caused a reduction
indices of PTEs, which have been widely used in the health in the dry weight of 100 niblets compared with the C1 treat-
risk assessment of cilantro, spinach, and rice plantings ment (decreased from 35.07 to 32.56 g). The impact of SSB
(Khan et al. 2014,2020; Zhang et al. 2016), were calculated on corn growth was determined by soil properties, which
using the following equations: will be discussed in the next section. In general, the addi-
tion of SSB could increase the yield of corn fruits, although
(1)
( )/
EDI = ConPTE × IRniblet BW, it inhibited plant growth, and the combination of SSB and
fertilizer could yield better results. The SSB rate of 1500 kg/
hm2 was optimal as an alkaline soil amendment for corn

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Biochar (2021) 3:135–147 139

Fig. 2  Growth performance of corn plants after maturity in different treatments. Letters indicate significant differences among treatments
(P < 0.05)

growth, ensuring the highest fruit yield. Zhang et al. (2016) 3.2 Effects of SSB amendments on physicochemical
also reported that modest applications of SSB (< 5000 kg/ properties of soil
hm2) increased rice grain yields in a field study.
3.2.1 Soil moisture, pH, and EC

The basic properties of the alkaline soil, including moisture,

pH, and EC, were investigated at different growth stages.
Before seeding, there was an insignificant difference among
the five trial areas with 14–18% of soil moisture (Fig. 3a).

Fig. 3  Variation in a soil moisture, b pH and c electrical conductivity during growth. Letters indicate significant differences among treatments
(P < 0.05)

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140 Biochar (2021) 3:135–147

The increase in moisture during the budding stage can be ­Ca2+, ­Mg2+, and ­PO43−) and increases the amount of total
attributed to artificial water management based on local dissolved salts (Figueiredo et al. 2018; Yue et al. 2017). SSB
experience. Furthermore, moderate SSB amendments should be applied to alkaline soils at controlled proportions
increased soil moisture at the budding and jointing stages to avoid potential toxicity to corn plants.
compared with CK, indicating that, owing to its porous
structure, SSB can improve the water-holding capacity of 3.2.2 Soil nutrient elements
soil when corn needs water to grow, similar to the findings
of Haider et al. (2017). There was no significant change Ammonium nitrogen is an important nutrient component
in soil moisture at other stages because the water-holding in soil and can be easily absorbed by plants because of its
capacity of SSB is not sustainable and will change with soil high solubility. However, acidic ammonium ions will be neu-
environmental variation (Li et al. 2020). Moreover, the pH tralized in alkaline soils and lead to nitrogen volatilization
range of soil for the five treatments was 7.6–7.9 (Fig. 3b). (Mandal et al. 2016). As shown in Fig. 4a, the concentration
The soil pH was in dynamic equilibrium and showed insig- of ammonium nitrogen first increased and then decreased
nificant variation during corn growth. This is because soil as growth progressed. The increase in ammonium nitrogen
pH is controlled by the leaching of basic cations (Ca, Mg, in the filling stage was attributed to the second fertilizer
K, and Na), the release of ­H+ from carbonic acid produced application. In the budding stage, the ammonium nitrogen
by ­CO2 dissolution, organic matter humification, and the concentrations in other treatments with SSB application
input and output of N (Liu et al. 2020; Neina 2019). How- were lower than 91.25 mg/kg in CK, and their concentra-
ever, a small amount of SSB application could not mark- tions were lower for C3 and C4 treatments. A similar phe-
edly increase the pH of the alkaline soil because of its high nomenon also occurred at the maturity stage. These results
background level, indicating that the current SSB amount is indicate that an increase in SSB application to alkaline soils
reasonable because higher soil pH may have adverse effects will decrease the concentration of ammonium nitrogen in
on plant growth and PTE availability (Artiola et al. 2012). the soil and promote volatilization of ammonia. The loss of
For soil EC (Fig. 3c), there were significant differences nitrogen may have a negative impact on corn growth. Sun
among the five treatments (1400–2600 µs/cm) and a greater et al. (2019) also observed that ­NH3 volatilization and N ­ 2O
amount of SSB (≥ 4500 kg/hm2) significantly increased emissions increased in acidic soils after the addition of more
the soil EC. Specifically, the C1 and C2 treatments were wheat straw alkaline biochar (20,000 kg/hm2). Phosphorus
rated as non-saline soil (0–2000 µs/cm) and other treat- and potassium, as essential elements, have been shown to
ments were classified as slightly saline soil (2000–4000 µs/ enhance fruit growth (Hossain et al. 2011; Zeeshan et al.
cm) (Scianna 2002). The EC in all treatments presented a 2020). The variation in available phosphorus and potas-
trend of first decrease and then stabilization during growing sium concentrations showed a similar trend during growth
stages because the accumulated nutrients and minerals in the (Fig. 4b, c). In particular, their concentrations in the soil
soil would have been adsorbed and utilized by corn plants were markedly elevated after the addition of increased SSB
(Negasa et al. 2017). In addition, the differences in EC for amendments (C3 and C4 treatments) in the budding stage.
the five trial areas reduced after corn planting, which sug- Therefore, SSB application had a positive influence on soil
gests that plant cultivation can modify the EC level of soil. fertility by increasing the concentrations of available phos-
Additionally, there was no significant difference in soil EC phorus and potassium. Furthermore, SSB had no effect on
in the other stages, although the EC level of the C2 treat- available nutrient concentration in the soil at the filling and
ment was lower than that of CK in the initial stage. This is maturity stages because the immobilization of available
because SSB gradually releases the available nutrients (­ K+, nutrient mitigated this increasing trend. However, the corn

Fig. 4  Variation in a ammonium nitrogen, b available phosphorus, and c available potassium concentrations in the soil during growth. Letters
indicate significant differences among treatments (P < 0.05)

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Biochar (2021) 3:135–147 141

plants in the C3 and C4 treatments had a weaker growth the risk intervention value (100 mg/kg) for soil contamina-
status than those in CK. These results can be attributed to the tion of agricultural land, although it was higher than the risk
fact that the alkaline soil used in the present study, with high screening value (25 mg/kg). The Cd concentration in the soil
background nutrient levels, can reduce nutrient uptake and could not be detected in the initial stage owing to its extra
inhibit plant growth after higher amounts of SSB are added low level. Yue et al. (2017) verified that the concentrations
(Ding et al. 2016; Zhang et al. 2010). Corn fruit accumulates of Zn, Cu, Cr, Pb, As, and Cd the potting soil significantly
more nutrients than other tissues, which is why corn yield increased in response to increasing amounts (1–50 wt%)
has not been affected (El-Fouly et al. 2012). However, the of applied SSB. Therefore, the proportion of SSB applied
detailed reason needs to be further investigated. should be considered, and a moderate proportion would
bring low environmental risk for soil in terms of total PTE
3.3 Effects of SSB amendments on PTE in soil concentrations. During the growth process, the soil con-
centrations of Cr, Ni, Cu, Zn, and As showed decreased
3.3.1 Total PTE concentrations trends, indicating that these PTEs migrated from soil into
corn plants. Moreover, the concentrations of Mn, Cd, and Pb
Although SSB has high PTE concentrations, as listed in varied irregularly due to the synergy between organic matter
Table 1, moderate SSB amendments had no significant decomposition and plant uptake (Li et al. 2017; Xie et al.
effects on total PTE concentrations in the soil in the ini- 2020b). Minor differences were also observed between CK
tial stage (Table 2), whose values were lower than the and other treatments with the addition of SSB at the maturity
risk screening values based on the Chinese standard (GB stage. Furthermore, the concentrations of As and Pb at the
15618–2018, Cr: 250 mg/kg; Ni: 190 mg/kg; Cu: 100 mg/ maturity stage and the Cd concentrations at the jointing,
kg; Zn: 300 mg/kg; Cd: 0.6 mg/kg; and Pb: 170 mg/kg), filling, and maturity stages in the C2 treatment were higher
indicating a lower risk. The concentration did not exceed than those in the C1 treatment, indicating that the absence

Table 2  Potentially toxic Stage Treatment Cr Mn Ni Cu Zn As Cd Pb

element concentrations in the
alkaline soil during growth Initial CK 62.62aa 433.83a 22.77a 14.82a 79.37a 44.88a –b 21.52a
C1 59.68a 410.58a 21.77ab 14.02ab 77.43a 42.63a – 20.21ab
C2 61.33a 418.15a 22.16a 12.78b 77.98a 44.52a – 18.52ab
C3 55.15a 361.43b 19.52b 12.65b 69.38b 41.34a – 18.05b
C4 59.23a 417.55a 20.86ab 14.99a 78.72a 42.30a – 19.07ab
Budding CK 47.60a 330.57a 16.83a 13.21a 49.96a 22.8a 0.20a 26.23a
C1 45.88a 333.43a 16.64a 13.08a 48.15a 21.21ab 0.21a 27.09a
C2 47.04a 311.5ab 15.87ab 13.53a 46.17a 19.35bc 0.17b 24.82ab
C3 46.07a 312.2ab 16.05ab 12.55a 49.76a 20.93ab 0.2a 25.85a
C4 43.06a 295.03b 14.61b 12.67a 49.85a 18.23c 0.17b 21.84b
Jointing CK 43.46a 343.17ab 15.92a 12.06a 41.00a 19.53b 0.19b 25.36a
C1 43.55a 357.13ab 15.72a 12.18a 38.41a 20.16ab 0.20b 25.80a
C2 43.50a 376.47a 16.11a 12.62a 40.88a 22.06a 0.23a 28.47a
C3 45.17a 334.30b 16.45a 12.41a 42.10a 21.44ab 0.20ab 27.82a
C4 43.06a 336.28b 15.46a 12.56a 39.18a 20.41ab 0.20ab 24.45a
Filling CK 38.37a 310.88c 15.41a 10.56b 38.36a 16.38b 0.17b 24.30ab
C1 41.15a 392.67a 12.92a 10.99ab 39.42a 20.64a 0.18b 24.28ab
C2 41.91a 332.87b 13.93a 10.86ab 39.39a 20.75a 0.20a 25.24a
C3 41.18a 284.15d 13.26a 11.18ab 44.01a 18.09b 0.14c 20.88c
C4 40.43a 304.2c 11.89b 12.12a 43.97a 16.97b 0.16bc 21.56bc
Maturity CK 35.56a 291.63ab 12.78a 9.66b 38.75ab 16.45abc 0.15cd 18.93b
C1 34.09a 270.35b 12.92a 9.76b 37.10b 16.08bc 0.17b 18.01b
C2 39.13a 331.30a 13.93a 10.74ab 35.25b 19.46a 0.23a 22.84a
C3 39.20a 288.18b 13.26a 12.20a 42.71a 17.31ab 0.16bc 19.34b
C4 34.36a 283.45b 11.89a 11.32ab 39.69ab 13.94c 0.13d 17.54b
a
Letters after the numerical value show significance differences with each column of data (P < 0.05)
b
Not detected

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142 Biochar (2021) 3:135–147

of fertilizer poses a greater risk to plant uptake of PTEs. the addition of SSB. Our previous study verified that Cr and
Unlike the application of fertilizer that would induce large Pb mainly existed in SSB as stable fractions combined with
amounts of Cd, Pb, and As into soil, as reported by Atafar silicate minerals, similar to soil (Li et al. 2021).
et al. (2008), this variation in PTE concentrations may be Unlike other treatments with fertilizer, the percentage of
influenced by water runoff and organic matter decomposi- the F4 fraction of Cd in the soil for the C2 treatment (with-
tion. However, the total PTE concentrations in soil are not out fertilizer) showed an increasing trend with growth. This
the only factors affecting plant uptake. The chemical specia- indicates that the plant uptake of Cd will not have signifi-
tion and distribution also affect the PTE concentrations in cant changes, although the concentration of Cd in the soil
crop fruits (Khan et al. 2013; Yue et al. 2017). increased in the absence of fertilizer. This inhibition of Cd
stability is attributed to the release of ­NH4+ from fertilizer,
3.3.2 Chemical speciation of PTE which can displace Cd from adsorption sites (Han et al.
2018). Ammar et al. (2016) also observed that the applica-
Based on the extraction of chemical species of PTEs, F1 tion of commercial NPK fertilizer enhances the mobility of
and F2 fractions are identified as bioavailable fractions that Cd in soil. Furthermore, compared with the C2 treatment,
can be easily adsorbed by plants, and the F4 fraction stably the addition of fertilizer in the C1 treatment increased the
exists in soil (Fuentes et al. 2008). With corn growth, the percentage of the F4 fraction of Cu at the jointing stage and
percentage of the F1 and F2 fractions of Mn and Zn signifi- the percentage of the F4 fraction of Zn at the budding stage,
cantly increased in the soil for the five treatments, and the suggesting a lower risk of uptake of PTEs by plants. This
percentage of the F4 fractions of Mn, Ni, Cu, Zn, and As immobilization effect can be attributed to the importance of
decreased markedly (Fig. 5). These results indicate that corn phosphorus fertilizers for the immobilization of PTEs via
growth has negative effects on the immobilization of PTEs, the adsorption or complexation of the phosphate surface on
which was also observed in the soilless cultivation of plants PTE ions and the formation of metal–phosphate precipitates
(Xie et al. 2020b). Throughout the growth stages, there were (Xu et al. 2018; Zeeshan et al. 2020).
minor variations and the F4 fraction was the main chemical
speciation of Cr and Pb in the soil, suggesting that these 3.4 Relation of PTE speciation with soil properties
PTEs stably exist in soil and are adsorbed with difficulty by
corn plants. The Pearson correlation coefficient shows the degree of cor-
SSB amendment had different effects on the chemical relation between different factors and is widely applied in
fractions of other PTEs. Specifically, compared with CK, soil research. Liu et al. (2020) analyzed the correlation of
1500 kg/hm2 of SSB amendment significantly increased the soil characteristics with soybean growth and yield param-
percentage of the F4 fraction of Ni in the budding stage, the eters and found that pH and available nitrogen had a greater
percentage of the F4 fraction of Cu in the budding, jointing, impact on the growth of soybean under alkaline soil condi-
filling, and maturity stages, the percentage of the F4 fraction tions. Wu et al. (2020b) used this method to analyze soil
of Zn in the budding stage, and the percentage of the F4 frac- properties, mineral nutrients, and fruit quality. In the pre-
tion of Cd in the filling, and maturity stages. Accordingly, sent study, the Pearson coefficient was used to determine
the percentage of the F1 and F2 fractions of Zn and Cd for the relationships between the F4 fraction of the PTEs in
the C1 treatment showed a decreasing trend compared with soil and soil physiochemical properties (Fig. 6). The size
CK. These results indicate that low amounts of SSB amend- and color of the squares indicate the strength of correla-
ments can promote immobilization of PTEs in the soil dur- tion, which can be shown by skew-symmetric numbers. The
ing different stages and reduce the risk off uptake by corn cross suggests a non-significant correlation among the dif-
plants, which can be attributed to the modified microbial ferent factors (P > 0.05). Chemical speciation of PTEs was
activity and the interaction between biochar and inorganic markedly influenced by soil pH, EC, and the concentrations
contaminants via ion exchange, anionic attraction, cationic of available phosphorus and potassium. There were signifi-
attraction, and precipitation (Zhu et al. 2017). Additionally, cant negative correlations between pH and the F4 fractions
the development of the pore structure of soil after the addi- of Mn, Ni, Cu, Zn, and As, suggesting that the increase in
tion of SSB will increase the number of exchange sites and soil pH inhibited the immobilization of these PTEs. This is
decrease the mobility of PTEs (Khan et al. 2013). These because these compounds are stable over a range of pH val-
positive effects on the immobilization of PTEs have also ues and higher pH will decrease their solubility in alkaline
been verified in other studies (Shaheen and Rinklebe 2015; soils (Wuana and Okieimen 2011). Compared with pH, the
Shaheen et al. 2015). However, an increase in SSB amend- correlation demonstrated the opposite trend between EC and
ment had a negative influence on the stability of the chemi- the F4 fractions of Mn, Ni, Cu, Zn, and As. Additionally,
cal speciation of Ni, Cu, and Cd. Furthermore, the chemical strong positive correlations were detected between the F4
speciation of Cr and Pb showed no significant variation after fractions of Cr and Zn and the concentrations of available

13
Biochar (2021) 3:135–147 143

Fig. 5  Variation in the chemical speciation of potentially toxic elements in the soil during growth

13
144 Biochar (2021) 3:135–147

et al. 2016). Concentrations of Cr, Mn, Ni, Cu, and Zn

were lower in the niblets than those in the corncobs, indi-
cating a low consumption risk of PTEs. Additionally, SSB
added at 1500 kg/hm2 significantly decreased the concen-
trations of Cr, Mn, Ni, Cu, Zn, and Pb in the niblets and
corncobs. Specifically, the concentrations of Mn, Ni, Cu,
and Zn in the niblets decreased by 19.3%, 25.3%, 42.5%,
and 13.6%, respectively, which was closely related to the
immobilization of PTEs in the soil. However, a greater
amount of SSB increased the Cu and Zn concentrations
in the corncobs. Al-Wabel et al. (2015) also verified that
applying 1.0–5.0 wt% of Conocarpus biochar significantly
reduced Mn, Zn, Cu, and Cd concentrations in corn shoots.
The reduction in corn shoots of Cr and Cu was observed
after the addition of 5 wt% biochar obtained from jujube
leaves and manure (Rafique et al. 2020). Furthermore, the
As and Pb concentrations in the niblets and the Cr, Mn, Ni,
Cu, and Zn concentrations in the corncobs for the C1 treat-
Fig. 6  Pearson correlation between the F4 fractions of potentially ment were significantly decreased compared with those in
toxic elements and soil properties. H2O soil moisture, AN ammonium the absence of the fertilizer (C2) treatment, indicating that
nitrogen, AP available phosphorus, AK available potassium the absence of fertilizer increases the consumption risk of
corn plants.
EDI and HQ are associated with the health risk of PTEs
phosphorus and potassium. This could be attributed to the via niblet intake, as listed in Table 4. The estimated EDI
fact that an increase in inorganic matter induces precipitation values of PTEs (except As) for the control were lower
of PTEs, which enhances the transformation of chemical ­ fD), indicating that the intake
than the tolerable limit (or R
speciation from bioavailable fractions to a more stable frac- of PTEs in humans was without substantial risk over a
tion (Yue et al. 2017). whole lifetime. Furthermore, the addition of moderate SSB
decreased the EDI values of Cr, Mn, Ni, Cu, Zn, and Pb,
3.5 Corn uptake of PTE and health risk assessment which was influenced by the PTE concentrations in the
niblets. If the HQ of food plants is lower than 1, there is
The PTE concentrations in the corn fruits (niblets and no health risk associated with their consumption. It was
corncobs) under different treatments are listed in Table 3. found that the HQ values of PTEs (except As) were far
Corn fruits had higher levels of Zn than those of other lower than the regulated threshold and all HQ values were
PTEs because Zn, as an important element, plays a role lower than those obtained in contaminated soils (Khan
in enzymatic and redox reactions (Singh et al. 2019). This et al. 2020, 2014). Additionally, lower HQ values were
can be verified in other plants, such as cucumber, rice, obtained in the treatments combining SSB and fertilizer,
and tomato (Hossain et al. 2010; Waqas et al. 2014; Zhang suggesting a reduction in the health risk of niblets.

Table 3  Potentially toxic Sample Treatment Cr Mn Ni Cu Zn As Cd Pb

element concentrations in
the corn fruits from different Niblet CK 0.92aa 5.54a 0.83a 2.26a 27.15a 0.08b 0.02a 0.20b
treatments
C1 0.86a 4.47b 0.62b 1.30b 23.45b 0.08b 0.02a 0.18bc
C2 0.78a 4.66b 0.60b 1.25b 23.35b 0.10a 0.02a 0.41a
C3 0.21c 3.61c 0.31c 1.30b 18.99c 0.08b 0.02a 0.16bc
C4 0.59b 4.00bc 0.33c 1.32b 16.89c 0.03c 0.02a 0.14d
Corncob CK 9.32a 8.98a 4.43a 2.71b 35.70a 0.06c 0.02a 0.18a
C1 4.00c 5.20d 1.70d 1.96c 18.59c 0.06c 0.02a 0.11c
C2 5.71b 6.81b 2.33c 3.19a 27.38b 0.06c 0.02a 0.11c
C3 6.95b 8.56a 3.49b 3.05a 32.72a 0.08b 0.03a 0.12bc
C4 3.63c 6.46bc 1.17e 2.67b 35.71a 0.13a 0.02a 0.14b
a
Letters after the numerical value show significance differences with each column of data (P < 0.05)

13
Biochar (2021) 3:135–147 145

Table 4  Estimated daily intake EDI HQ

(µg/kg/day) and hazard quotient
for potentially toxic elements CK C1 C2 C3 C4 CK C1 C2 C3 C4
associated with the consumption
of corn Cr 6.45 6.03 5.47 1.47 4.14 0.00 0.00 0.00 0.00 0.00
Mn 38.84 31.34 32.67 25.31 28.04 0.28 0.22 0.23 0.18 0.20
Ni 5.82 4.35 4.21 2.17 2.31 0.29 0.22 0.21 0.11 0.12
Cu 15.84 9.11 8.76 9.11 9.25 0.40 0.23 0.22 0.23 0.23
Zn 190.34 164.40 163.70 133.13 118.41 0.63 0.55 0.55 0.44 0.39
As 0.56 0.56 0.70 0.63 0.21 1.87 1.87 2.34 1.87 0.70
Cd 0.14 0.14 0.14 0.14 0.14 0.05 0.05 0.05 0.05 0.05
Pb 1.40 1.26 2.87 1.12 0.98 0.40 0.36 0.82 0.32 0.28

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With the amendment of 1500 kg/hm2 sewage sludge bio- permitted by statutory regulation or exceeds the permitted use, you will
char applied to the alkaline soil, the fruit yield of corn need to obtain permission directly from the copyright holder. To view a
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(4500–9000 kg/hm2) inhibited the growth of corn plants due
to the high nutrient levels. Moderate sewage sludge biochar
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