Environmental Pollution 252 (2019) 1142e1153

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Environmental Pollution
journal homepage: www.elsevier.com/locate/envpol

A novel clean production approach to utilize crop waste residues as

co-diet for mealworm (Tenebrio molitor) biomass production with
biochar as byproduct for heavy metal removal
Shan-Shan Yang a, Yi-di Chen a, Ye Zhang a, Hui-Min Zhou a, Xin-Yu Ji a, Lei He a,
De-Feng Xing a, Nan-Qi Ren a, Shih-Hsin Ho a, **, Wei-Min Wu b, *
a
State Key Laboratory of Urban Water Resource and Environment, School of Environment, Harbin Institute of Technology, Harbin, 150090, China
b
Department of Civil and Environmental Engineering, William & Cloy Codiga Resource Recovery Center, Center for Sustainable Development & Global
Competitiveness, Stanford University, Stanford, CA, 94305, USA

a r t i c l e i n f o a b s t r a c t

Article history: Proper management of waste crop residues has been an environmental concern for years. Yellow
Received 9 April 2019 mealworms (larvae of Tenebrio molitor Linnaeus, 1758) are major insect protein source. In comparison
Received in revised form with normal feed wheat bran (WB), we tested five common lignocellulose-rich crop residues as feedstock
26 May 2019
to rear mealworms, including wheat straw (WS), rice straw (RS), rice bran (RB), rice husk (RH), and corn
Accepted 6 June 2019
Available online 8 June 2019
straw (CS). We then used egested frass for the production of biochar in order to achieve clean production.
Except for WS and RH, the crop residues supported mealworms’ life activity and growth with con-
sumption of the residues by 90% or higher and degraded lignin, hemicellulose and cellulose over 32 day
Keywords:
Crop wastes
period. The sequence of degradability of the feedstocks is RS > RB > CS > WS > RH. Egested frass was
Tenebrio molitor Linnaeus converted to biochar which was tested for metal removal including Pb(II), Cd(II), Cu(II), Zn(II), and Cr(VI).
Insect biomass Biochar via pyrolysis at 600
C from RS fed frass (FRSBC) showed the best adsorption performance. The
Clean production adsorption isotherm fits the Langmuir model, and kinetic analysis fits the Pseudo-Second Order Reaction.
Biochar The heavy metal adsorption process was well-described using the Intra-Particle Diffusion model.
Heavy metal removal Complexation, cation exchange, precipitation, reduction, deposition, and chelation dominated the
adsorption of the metals onto FRSBC. The results indicated that crop residues (WS, RS, RB, and CS) can be
utilized as supplementary feedstock along with biochar generated from egested frass to rear mealworms
and achieve clean production while generating high-quality bioadsorbent for environment remediation
and soil conditioning.
© 2019 Published by Elsevier Ltd.

1. Introduction
Crop residue management including rice straw, corn straw,
wheat straw, etc., has been a global problem for years. China is a
large agricultural country which produces approximately 800
million tons of crop residues (Jiang et al., 2012), accounting for
17.3% of the total global mass and 63.4% of the total mass in Asia. In
recent years, approximately 20% of the residue was burned in the
field, causing severe air pollution in China (Yu et al., 2018). Finding
This paper has been recommended for acceptance by Joerg Rinklebe.
* Corresponding author.
** Corresponding author.
E-mail addresses: stephen6949@hit.edu.cn (S.-H. Ho), billwu@stanford.edu
(W.-M. Wu).
use for the crop residues is significant because the huge amount of
crop wastes is a serious burden on local ecosystems as well as a
cause for concern over environmental pollution after harvest sea-


son (Cilerd 
zi

c et al., 2016). Crop residues, which contain 30e45%
cellulose, 10e40% hemicellulose, and 5e25% lignin (Wadhwa and
Bakshi, 2013), contain high quantities of lignocellulose and are
difficult to digest, meaning that they are not direct high-quality
feedstock for animals. Additionally, crop residues resist biodegra-
dation, resulting in requirements of harsher pretreatment
(Mussoline et al., 2013). These leftover residues exhibit not only
resource loss but also a missed opportunity to improve a farmer's
income. The use of crop residues in various fields are being
explored by researchers across the world (Pandey et al., 2016).
Yellow mealworms, or the larvae of Tenebrio molitor Linnaeus
1758, are a holometabolic insect belonging to the order Coleoptera

https://doi.org/10.1016/j.envpol.2019.06.028
0269-7491/© 2019 Published by Elsevier Ltd.
 S.-S. Yang et al. / Environmental Pollution 252 (2019) 1142e1153
(beetles) and family Tenebrionidae (common name “darkling bee-
tle”), a cosmopolitan family of beetles (Wikipedia, 2019). As hol-
ometabolic insects, they go through four life stages: egg, larva,
pupa, and adult. Mealworms are considered a profitable animal
food source and are available in pet markets and stores. They are a
more sustainable source of edible protein for humans than milk,
chicken, pork, or beef, and are mass reared as feed for birds, rep-
tiles, amphibians, and fish (Yang et al., 2018). Mealworm farming is
popular in China, the USA, and Europe. In China, millions of tons of
mealworm biomass are generated as animal feedstocks for do-
mestic uses and for export. Recent research has also found that
mealworms are also capable of biodegrading persistent petroleum-
based plastics including polystyrene and polyethylene in their guts
(Yang et al., 2018; Brandon et al., 2018), suggesting that mealworms
have powerful digestive systems. At present, the commercial pro-
duction of the mealworm biomass uses wheat bran (WB) or fresh
oats as the primary feedstock (Wikipedia, 2019). Because of the
high digestibility of mealworms, we hypothesized that crop resi-
dues such as rice straw (RS), rice husk (RH), wheat straw (WS), and
corn straw (CS) may serve as a supplementary food to reduce cost of
feedstock. In addition, currently, millions of tons of frass wastes
must be handled or treated by mealworm farming businesses.
Proper management of waste frass is still a costly issue for meal-
worm farming, although the frass has been suggested for use as
organic fertilizer. A sustainable approach is to convert the frass into
valuable product to achieve waste-free clean production for meal-
worm farming business.
Biochar adsorption amendment technology has attracted
widespread attention in the remediation of heavy metal pollution
in soil and sediment due to its potential use as a soil amendment
that can improve soil and sediment quality and immobilization of
metals, such as Cu(II), Pb(II), Cd(II), Zn(II), Cr(VI), etc. (Niazi et al.,
2017; Peng et al., 2017; Gong et al., 2018; Ding et al., 2019; Xu
et al., 2019). Generated from biomass via pyrolysis under oxygen-
limited conditions, biochar has been considered for soil carbon
sequestration and remediation of contaminated soil owing to its
enviable properties such as high efficiency, easy handling, low
operational costs, availability, and so on (Huang et al., 2017, 2019;
Sun et al., 2017; Biswas et al., 2019). Various organic wastes have
been tested as raw materials for biochar production, including crop
residues, pruning waste from gardens and laws, aquatic plant ma-
terial, animal manure and waste activated sludge (Sun et al., 2017;
Wang et al., 2019a; Lin et al., 2018) for carbon sequestration, soil
amendment, and wastewater decontamination (Beesley et al.,
2011). A variety of crop residues, such as WS, RS, rice bran (RB),
RH, CS, and sugarcane bagasse, etc., have been converted into
biochars, used as adsorbents, and have been proved to have good
adsorption capabilities for heavy metals (Zhang et al., 2011; Xu
et al., 2014). The animal wastes tested for biochar included cow
manure (Xu et al., 2013), chicken manure (Huang et al., 2018),
earthworm manure (Wang et al., 2017), and swine manure (Meng
et al., 2014; Xu et al., 2018; Han et al., 2017; Wang et al., 2018).
In this study, we tested a novel clean production approach that
uses crop resides as feedstock to rear mealworms for insect
biomass production, after which the mealworm frass is utitlized as
raw material to generate biochar for heavy metal removal in
wastewater treatment or soil remediation. We used wheat bran as a
control to test five lignocellulose-rich crop residues, i.e., WS, RS, RB,
RH, and CS, in rearing mealworms and compared their consump-
tion and biodegradation. We then used the frass egested by meal-
worms fed respective feedstocks as raw material to generate
biochar. We specially characterized the performance of biochars
derived from the different feedstocks to adsorb five heavy metals,
i.e., Pb(II), Cd(II), Cu(II), Zn(II), and Cr(VI), and investigated the
adsorption mechanism of the heavy metal ions in relation to the
1143
frass-derived biochars. The results demonstrated that all tested
crop residues, except for RH, can be well digested by mealworms
and that the biochars made from the frass performed better than
biochar made from original crop residues. Biochar made from frass
with RS as feedstock demonstrated the best metal removal
performance.
2. Materials and methods
2.1. Source of mealworms
Mealworms (the larvae of Tenebrio molitor Linnaeus) purchased
from a mealworm farm in Harbin, China (named Harbin strain of
T. molitor), were in 6e7 instar age with 60e70 mg per worm. Prior
to arrival, the larvae were fed wheat bran. Before the tests, the
mealworms were maintained under starving conditions for two
days to empty their guts.
2.2. Crop residue feedstocks
Mealworms were divided into six feeding groups, each fed with
WB and one of the five crop residues (WS, RS, RB, RH, and CS)
(Fig. 1A). WB was purchased from a farm in Harbin, China. WS and RS
were obtained from farmlands in Shandong Province, China, which
were reaped in 2018 and 2017, respectively. RB and RH were pur-
chased from Liaoning Province, China, which were harvested and
stored in 2017. CS was collected from a farmland in Harbin, China,
2018. Prior to tests, all straws were cut into small pieces, washed with
tap water and then distilled water to eliminate the dirt. In accordance
with the guidelines of the American Society for Testing and Materials
(ASTM) E1757-01 (ASTM, E1757-01, 2007), the collected crop resi-
dues were dried in a forced-air drying oven at 45
C for 48 h, after
which the samples were stored in clean polyethene bags at 4
C for
further usage. The compositions of the lignocellulosic substances of
the six feedstocks are presented in Table 1.
2.3. Consumption and biodegradation of crop residues by
mealworms
Rectangular food grade polyethylene storage containers (size:
length, width, and height of 40  20  5 cm) were used as indi-
vidual incubators, each containing around 2000 ± 100 mealworms
with an average weight of 68.45 ± 0.65e68.76 ± 0.48 mg/worm
based on the weight of mealworms added (Table 1). Duplicates of
incubators with mealworms were maintained in a 250 L artificial
climate incubator (Artificial climate incubator, Shanghai Shuli,
Shanghai, China). The temperature was controlled at 25 ± 1
C with
humidity of 60 ± 5%. The housing density was around 25,000
worms/m2.
Six different feedstocks including WB (as control), WS, RS, RB,
RH, and CS were examined for the survival rate (SR), as well as
feedstock consumption and biodegradation by mealworms.
Initially, each feedstock of 10.0 g was added to the respective con-
tainers. Over a 32-day period, 10.0 g of each feedstock was sup-
plemented into the respective incubator every four days. The
number of live mealworms were counted, dead mealworms were
removed, and residual feedstock and the corresponding egested
frass in respective incubators were collected and weighed. The SRs
of the mealworms and the mass loss yields of the feedstocks were
calculated every four days.
2.4. Collection and characterization of frass and preparation of
biochars
For clean frass collection, mealworms fed each feedstock were
1144 S.-S. Yang et al. / Environmental Pollution 252 (2019) 1142e1153

Fig. 1. (A) Photos of the different crop residues of feed for six group of mealworms, (B) SR (%) of mealworms and (C) feedstock consumption rates (%) of different feedstocks at the
end of 32-day period, and (D) Photos of the frass egested from mealworms feeding different crop residues feedstocks and biochar made from the frass.

cleansed with a stream of compressed air and transferred to clean
boxes for egested frass collection. After 12 h’ stay, the mealworms
were then returned to the original incubators. The collected frass
samples were stored at 4
C for further lignocellulose content
analysis.
Pyrolysis of the as-prepared biochars (six feedstocks and six
frass samples) was performed in a vacuum tube furnace (Vacuum
tube furnace Shanghai Micro-X furnace Co., Ltd., Shanghai, China)
under a nitrogen atmosphere at 600
C for 90 min. The pyrolysis
heating rate was set at 15
C/min. The biochar ash was annealed
under an air atmosphere at 600
C for 120 min (Ho et al., 2017).
When the temperature dropped to 50
C, the pyrolyzed samples
were removed from the furnace and left to cool. All biochar samples
were milled to pass a 200-mesh sieve for subsequent adsorption
tests.
The as-prepared biochars from the crop residue feedstocks (WB,
WS, RS, RB, RH, and CS) and the corresponding frass samples were
named and labelled as WBBC (#1), FWBBC (#2), WSBC (#3), FWSBC
(#4), RSBC (#5), FRSBC (#6), RBBC (#7), FRBBC (#8), RHBC (#9),
FRHBC (#10), CSBC (#11), and FCSBC (#12), respectively.
2.5. Heavy metal adsorption experiments
Batch adsorption experiments were carried out using aqueous
solutions of PbCl2, Cd(NO3)2∙4H2O, CuSO4∙5H2O, ZnCl2, and
K2Cr2O7 to provide Pb(II), Cd(II), Cu(II), Zn(II) and Cr(VI) metals,
respectively. The metal stock solutions were prepared by dissolving
the metal salts in ultrapure water (Millipore, 18 MUcm) with the
initial concentration of 200 mg/L. Then 0.02 g of biochar sample
was measured into 40 mL of a brown glass vial and filled with
 S.-S. Yang et al. / Environmental Pollution 252 (2019) 1142e1153 1145

Table 1
Composition and biodegradation of six feedstocks by mealworms over a 32-day rearing period.

Feed mass g Component Total feedstock Feedstock Component Component Component Component Component Average mealworm weighte
ingested, g consumed Contenta consumedb in frass Digestedc g Reductiond
Initial mg End mg Change,
% % g g %
%

WB Cellulose 80.02 ± 0.80 100.00 ± 0.00 16.40 ± 0.08 13.12 ± 0.20 9.59 ± 0.00 3.53 ± 0.19 26.91 ± 1.06 68.69 ± 0.38 73.13 ± 0.54 6.46
80.02 ± 0.80 Hemicellulose 33.39 ± 0.44 26.72 ± 0.62 18.56 ± 0.05 8.16 ± 0.57 30.52 ± 1.42
Lignin 5.25 ± 0.65 4.21 ± 0.56 1.99 ± 0.12 2.22 ± 0.44 52.30 ± 3.44
WS Cellulose 27.47 ± 0.97 34.33 ± 1.02 37.72 ± 0.73 10.37 ± 0.57 4.83 ± 0.12 5.54 ± 0.44 53.39 ± 1.35 68.57 ± 0.36 69.86 ± 0.49 1.88
80.00 ± 0.45 Hemicellulose 26.80 ± 0.24 7.36 ± 0.33 3.02 ± 0.03 4.34 ± 0.29 58.87 ± 1.39
Lignin 8.11 ± 0.01 2.23 ± 0.08 1.31 ± 0.00 0.92 ± 0.08 41.27 ± 2.11
RS Cellulose 74.49 ± 2.98 93.03 ± 3.34 35.15 ± 0.47 26.20 ± 1.40 12.39 ± 0.62 13.81 ± 0.78 52.70 ± 0.16 68.45 ± 0.65 70.92 ± 0.63 3.61
80.07 ± 0.33 Hemicellulose 22.15 ± 0.17 16.50 ± 0.79 7.34 ± 0.37 9.16 ± 0.42 55.53 ± 0.12
Lignin 8.98 ± 0.21 6.70 ± 0.42 3.36 ± 0.17 3.34 ± 0.25 49.78 ± 0.64
RB Cellulose 74.04 ± 2.96 92.49 ± 2.87 42.38 ± 0.82 31.40 ± 1.86 19.68 ± 0.98 11.72 ± 0.88 37.29 ± 0.60 68.76 ± 0.48 70.75 ± 0.58 2.89
80.04 ± 0.72 Hemicellulose 18.26 ± 0.33 13.53 ± 0.78 10.72 ± 0.54 2.81 ± 0.24 20.73 ± 0.61
Lignin 11.27 ± 0.46 8.36 ± 0.67 5.69 ± 0.28 2.67 ± 0.39 31.75 ± 2.16
RH Cellulose 20.25 ± 0.61 25.30 ± 0.57 33.48 ± 0.25 6.78 ± 0.25 6.22 ± 0.06 0.56 ± 0.19 8.18 ± 2.57 68.62 ± 0.61 69.07 ± 0.45 0.66
80.02 ± 0.61 Hemicellulose 17.04 ± 0.87 3.46 ± 0.28 2.45 ± 0.02 1.01 ± 0.26 28.69 ± 5.2
Lignin 8.54 ± 0.11 1.73 ± 0.07 1.72 ± 0.06 0.01 ± 0.01 0.68 ± 0.68
CS Cellulose 72.16 ± 2.89 90.10 ± 2.87 47.59 ± 0.09 34.34 ± 1.44 21.62 ± 1.08 12.72 ± 0.36 37.07 ± 0.51 68.39 ± 0.26 70.19 ± 0.31 2.63
80.07 ± 0.65 Hemicellulose 25.18 ± 0.71 18.19 ± 1.24 13.79 ± 0.69 4.40 ± 0.55 24.10 ± 1.38
Lignin 9.23 ± 1.09 6.69 ± 1.05 4.53 ± 0.23 2.16 ± 0.82 31.14 ± 7.40
a
Components including cellulose, hemicellulose, and lignin in the raw feedstock were expressed as % (w/w).
b
Mass of consumed feedstock was calculated based on the accumulated mass of each feedstock minus residues over a 32-day rearing period.
c
Digested mass and reduction percentage were calculated based on the accumulated mass ingested, averaged content in the feedstocks and egested frass over a 32-day
rearing period.
d
Digested mass and reduction percentage were calculated based on the accumulated mass ingested, averaged content in the feedstocks and egested frass over a 32-day
rearing period.
e
Digested rate was calculated based on total mass digested per 100 worms over 32-day period. Note: Composition and biodegradation of WB and WS feedstocks by
mealworms over a 32-day rearing period are adapted from Yang et al. (2019).

20 mL of 200 mg/L of heavy metal solution for contact time studies Qm are respectively the adsorption capacity and the maximum
(0-720 min). Also, equilibrium adsorption isotherm data was ob- adsorption capacity of metal ion onto the adsorbents (mg/g), and KL
tained by varying initial adsorbate concentrations for the five heavy is the Langmuir constant (L/mg).
metals solutions (25e600 mg/L) for 720 min equilibrium contact Freundlich model:
time. All the tested vials were shaken at 180 rpm at 25
C. After the
adsorption experiments, the suspension was filtered with 0.45 mm logQe ¼ logKF þ 1=n logCe (2)
membrane to collect filtrate for the measurement of residual metal
ion concentration using inductively coupled plasma atomic emis- where KF is the Freundlich adsorbent capacity (mg/g) and n is the
sion spectroscopy (Optima 8300, PerkinElmer, USA). heterogeneity factor.
To examine the effect of pH on adsorption capacity, the pH Three kinetic models including the pseudo-first-order kinetic
values of the metal solutions of Pb(II), Cd(II), Zn(II), and Cr (VI) were model, the pseudo-second-order kinetic model, and the intra-
adjusted to pH 1.0, 2.0, 3.0, 4.0, 5.0, and 6.0 using 1 M HCl or 1 M particle diffusion rate model were used to investigate the heavy
NaOH solution prior to addition of adsorbent. The pH value of Cu(II) metal adsorption kinetics on adsorbents:
solution was adjusted to 1.0, 2.0, 3.0, 4.0, and 5.0, respectively in Pseudo-first-order model:
order to avoid the precipitation of Cu(II) at above pH 5.5. The
dosage of adsorbent was 1.0 mg/ml as solid mass/liquid volume. qt ¼ qe ð1  ek1 t Þ (3)
The initial and final pH values were measured before and after Pseudo-second-order model:
adsorption experiments.
Three pyrolysis temperatures of 300, 450, and 600
C were k2 q2e t
conducted for 90 min in a vacuum tube furnace (Vacuum tube qt ¼ (4)
1 þ k2 qe t
furnace Shanghai Micro-X furnace Co., Ltd., Shanghai, China) under
a nitrogen atmosphere to examine the effect of temperature on the Intra-particle diffusion model:
adsorption performance of biochars. The optimal pyrolysis tem-
perature and pH value was chosen for the subsequent adsorption qt ¼ kp t 0:5 þ C (5)
isotherm and kinetics experiments.
where t is the contact time (min), and qe and qt represent
adsorption capacity (mg/g) at equilibrium and at time t (min),
2.6. Adsorption isotherm and kinetics models
respectively. k1 (min1) and k2 (g/mg∙min) are the rate constants of
the pseudo-first-order rate constant and the pseudo-second-order
Adsorption isotherm and kinetics experiments were carried out
kinetic models, kp is the intra-particle diffusion rate constant (mg/
at 298.0 ± 1.0 K. Langmuir and Freundlich isotherm models were
g∙min0.5), and C is the thickness of the boundary layer (mg/g).
evaluated to fit the data of the heavy metal adsorption to biochar
as:
Langmuir model: 2.7. Analytical methods

Ce = Qe ¼ Ce =Qm þ 1=ðQm KL Þ (1) The contents of the cellulose, hemicellulose, and lignin in crop
residues and frass were measured by using a Fiber analyzer A200i
where Ce is the metal concentration at equilibrium (mg/L), Qe and (ANKOM Co., USA) as described by Dong et al. (2018). The main
1146 S.-S. Yang et al. / Environmental Pollution 252 (2019) 1142e1153
elements in biochars were measured by an elemental analysis (EA)
(Bruker, Germany). The micro-morphological images were acquired
by using scanning electron microscopy (SEM) and SEM-energy-
dispersive spectrometry (SEM-EDS, TM3030, Hitachi, Japan).
Fourier transform infrared spectroscopy (FTIR) analysis (SPECTRUM
one, PerkinElmer, USA) was used to characterize the major func-
tional groups in the range 400e4000 cm1. The surface composi-
tion was determined by X-ray photoelectron spectroscopy (XPS)
(ESCA Lab 250Xi, Thermo Fisher, USA) within a depth less than
10 nm. After being degassed for 6 h at 150
C, the surface area, pore
volume, and average pore diameter were measured by Brunauer-
Emmett-Teller (BET, JW-BK132F, JWGB SCI & TECH, China). Each
sample was analyzed in triplicate.
3. Results and discussion
3.1. Digestion rates of different crop residues by mealworms
Six groups of mealworms were fed at 25
C with either WS, RS,
RB, RH, or CS in comparison with normal food WB as a control
(Fig. 1A). The frass egested from mealworms fed different feed-
stocks appeared similar in irregular granular particles with a size of
0.3e0.8 mm (Fig. 1D). The results of consumption and removal of
respective crop residues, as well as weight change of mealworms
over 32 days are summarized in Table 1.
Mealworms ate all six crop residues. At the end of the test, the
SR of mealworms fed normal feedstock WB was 95.25 ± 0.32%.
Mealworms fed WS, RS, RB, and CS, respectively, showed SRs of
95e97%, which indicated no significant difference from the meal-
worms fed WB only (Fig. 2B). The SR of mealworms fed an RH-only
diet was slightly lower (89.79 ± 0.45%) but it was still higher than
unfed mealworms (74.94 ± 0.57%). This suggested that mealworms
ate all crop residues as well as confirmed our previous observation,
that certain crop residues such as RS are a suitable energy source for
mealworm's life activities (Yang et al., 2018).
The tests were performed using a total accumulated dosage of
80 g of the respective feedstocks with 2000 mealworms over 32
days. The ingestion rates of the six feedstocks were different
(Fig. 2C and Table 1). The normal feedstock WB was consumed
completely (100%) by mealworms, as expected, while the ingestion
of other feedstocks was incomplete. The sequential ingestion rate
was WB, 100 ± 0.00%; RS, 93.03 ± 3.34%; RB, 92.49 ± 2.87%; CS,
90.10 ± 2.87%; WS, 34.33 ± 1.02%; and RH, 25.30 ± 0.57%. This
indicated that mealworms ate all crop residues at different rates
depending on the tastes of the larvae. We observed that WS and RH
are hard to eat or swallow for mealworms. The digestion rates of
ingested feedstocks, which were calculated on the basis of solid
mass of feedstock ingested and frass egested, were also different. In
particular, because of the low ingestion rate of RH, it did not provide
mealworms enough energy source for their life activities, resulting
in the relatively low SR for the mealworms fed RH only. The effect of
feedstock on the weight increase of mealworms was in sequence as
WB, 6.46%; RS, 3.61%; RB, 2.89%; CS, 2.63%; WS, 1.88%; and RH,
0.66%. RS, RB, and CS likely supported the growth of mealworms.
However, due to limited protein contents in these materials (3e4%,
w/w), they could not serve as primary feedstock. Further study is
needed for the enhancement of mealworms growth rate and yield
using the crop residues with other high protein feedstock and/or
enhancement of protein content in the crop residues by fungal
treatment (Madadi and Abbas, 2017).
All feedstocks tested contain cellulose, hemicellulose, and lignin
materials (Table 1). Lignin materials are high-molecular-weight,
insoluble plant polymers and have complex and variable struc-
tures. They are composed essentially of many methoxylated de-
rivatives of benzene (phenylpropanoid alcohols), especially
coniferyl, sinapyl, and coumaryl alcohols. WB contained low con-
tents of cellulose (16.40%), lignin (5.25%), and high hemicellulose
(33.39%). Other feedstocks contained significant amounts of lignin
(8.11e11.27%) and more cellulose (33.48e47.59%). The results
indicated that cellulose, hemicellulose, and lignin components in
crop residues groups of WS, RS, RB, RH, and CS were partially bio-
degraded. Cellulose, hemicellulose, and lignin components were
partially digested by 26.91 ± 1.06 to 53.39 ± 1.35%, 20.73 ± 0.61 to
58.87 ± 1.39%, and 0.68 ± 0.68 to 52.30 ± 3.44%. Based on digestion
rates, the favorable biodegradation rates were observed using WS
and RS with 53.39% and 52.70% for cellulose; 58.87% and 55.53% for
hemicellulose; and 41.27% and 49.78% for lignin (Table 1). Results
also showed almost no degradation of lignin in the RH group. Re-
sults obtained in this study confirmed that the mealworms digest
lignocelluloses at different rates, probably depending on their
structure and chemical components.
It is well known that microorganisms, especially some fungi, are
capable of degradation of lignocelluloses (Madadi and Abbas, 2017).
Further study is needed to understand the mechanism and impact
factors controlling and influencing lignocellulose biodegradation in
mealworms, e.g. whether degradation or digesting is conducted by
the enzymes of mealworms themselves, their gut microbes, or
both, in order to break down or depolymerize the lignocellulolytic
structure in a similar manner as insect-phytophagous scarab larvae,
Holotrichia parallela larvae, Dendroctonus rhizophagus larvae
(Morales-Jime
nez et al., 2012; Sheng et al., 2016).
The poor ingestion rate of RH was because it is formed from hard
materials, including opaline silica and lignin structure. Although
WS is not a high protein or energy source, it has been used as
supplementary feedstock for cows in the USA. In this study, how-
ever, mealworms chew and ingested WS inefficiently
(34.33 ± 1.02% in Table 1). Therefore, we suggest not considering RH
and WS as a supplementary feedstock for mealworms. The results
indicated that RS, RB, and CS are better supplementary feedstocks,
as they ensured the energy for life activities of the mealworms and
were nutritional sources for their growth, comparable to WB, when
provided over the 32-day period. Among the five crop residues
tested, RS was the most favorable candidate based on the ingestion
rate, specific digestion rate, and digestion rates of cellulose, hemi-
cellulose, and lignin. Further study will address improvement of
nutritional contents (such as protein) in RS based feedstock.
3.2. Heavy metal removal performance with biochars
In this study, we selected removal of heavy metal to examine
biochar performance as case study although biochar generated
could have a variety of application. Batch adsorption experiments
were carried out using aqueous solutions of Pb(II), Cd(II), Cu(II),
Zn(II), and Cr(VI). The initial concentration of each metal ion was
200 mg/L. As shown in Fig. 2A, the as-prepared biochars exhibited
different adsorption capabilities on the five metals. The biochars
from the frass fed with WB, WS, RS, RB, RH, and CS (FWBBC (#2),
FWSBC (#4), FRSBC (#6), FRBBC (#8), FRHBC (#10), FCSBC (#12))
showed better performance of metal ion removal than those made
from their corresponding raw feedstocks (#1, #3, #5, #7, #9, and
#11). The enhanced adsorption capabilities of frass-based biochars
could be a synergetic effect of chemical and physical modification
of the feedstock materials after chewing and gut digestion by gut
bacteria and by host enzymatic activity as the feedstocks pass
through the digestive system of the larvae of T. molitor.
Among all frass-derived biochars, FRSBC (#6) from frass origi-
nating from rice straw displayed the best removal capacities of
188.20 ± 4.71 mg/g for Pb(II), 49.56 ± 1.49 mg/g for Cu(II),
58.94 ± 2.95 mg/g for Cd(II), 18.60 ± 0.93 mg/g for Cr(VI), and
41.98 ± 2.01 mg/g for Zn(II) (Fig. 2A). At the equilibrium with FRSBC
 S.-S. Yang et al. / Environmental Pollution 252 (2019) 1142e1153
Fig. 2. Adsorption capabilities of Pb(II), Cu(II), Cd(II), Cr(VI), and Zn(II) onto 12 biochars produced from raw feedstocks and the frass of mealworms fed different feedstocks; (B) Effect
of initial pH on heavy metal ions adsorption capabilities onto #6 (FRSBC); (C) Final pH versus initial pH after heavy metal ions adsorption onto FRSBC; (D) Effect of pyrolysis
temperatures of 300, 450, and 600
C on adsorption capabilities of Pb(II), Cu(II), Cd(II), Zn(II) and Cr(VI) onto FRSBC with respective initial pH of 6.0, 5.0, 6.0, 6.0 and 1.0.
as adsorbent, the highest removal was Pb(II) up to approximately
94.10 ± 2.36% with the initial Pb(II) concentration of 200 mg/L,
while the lowest removal was Cr(VI) at 9.13 ± 0.47% with 200 mg/L
initial concentration. Compared with biochar RSBC (#5) made from
original raw RS feedstock, the respective heavy metal removal
performances were enhanced to 37.17%, 24.34%, 40.47%, 26.88%,
and 67.65%. Consequently, the sequence of the adsorption capac-
ities of the heavy metal Pb(II) onto biochars at the same pyrolysis
temperatures of 600
C is: FRSBC (#6) > FCSBC (#12) > RSBC
(#5) > FRHBC (#10) > CSBC (#11) > FWSBC (#4) > FWBBC
(#2) > WSBC (#3) > RHBC (#9) > WBBC (#1) > FRBBC (#8) > RBBC
(#7). On the other hand, mealworms fed with RS had the highest
digestion rate and favorable lignocellulose biodegradation rate. The
biochar from CS-fed mealworm frass also showed favorable metal
removal capabilities and demonstrated good biodegradability as a
feedstock (Table 1).
FRSBC was selected to test the effect of initial pH and pyrolysis
temperature on adsorption performance (Fig. 2B, C and 2D). The
adsorption capacities for Pb(II), Cd(II), Cu(II), and Zn(II) were
increased as pH was increased, but adsorption of Cr(VI) showed a
reversed trend (Fig. 2B). At the initial pH of 1.0, the adsorption
capabilities for Pb(II), Cd(II), Cu(II), and Zn(II) were 31.16 ± 0.53,
16.68 ± 0.42, 13.44 ± 0.34, and 10.44 ± 0.37 mg/g. When the initial
pH increased to 6.0 (or 5.0 for Cu2þ), the adsorption capabilities of
Pb(II), Cd(II), Cu(II), and Zn(II) by FRSBC reached up to 189.71 ± 3.89,
58.94 ± 2.95, 49.56 ± 1.24, and 41.98 ± 2.1 mg/g (Fig. 2B). For Cr(VI),
the respective adsorption capacities were 7.44 ± 0.26 and
19.03 ± 0.48 mg/g. The pH of the metal solutions had a significant
impact on biochar adsorption capacity. In particular, the observed
reversed capacities of Cr(VI) were likely due to the complicated
process of Cr adsorption, which involves formation of various Cr(VI)
species on surface functional groups (He et al., 2017) and oxidation
of Cr(VI) to Cr(III), which favors acidic condition (Zhang et al., 2018;
Xu et al., 2019). Stoichiometrically, three electrons are required to
reduce Cr(VI) to Cr(III) prior adsorption. The estimated electron
requirement for Cr(VI) adsorption of 19 mg/g at pH 1.0 requires
1147
electrons of 0.022 mmol or 0.176 mg as chemical oxygen demand
(COD), while 7.44 mg/g at pH 6.0 requires 0.0086 mmol electrons,
or 0.069 mg COD. The electron donor source was provided by
biochar.
Overall, FRSBC obtained at 600
C had higher adsorption ca-
pacities for all heavy metal ions than those prepared at relatively
lower pyrolysis temperatures (300 and 450
C) (Fig. 2C), suggesting
that pyrolysis of FRSBC at 600
C is a proper condition to produce
biochar for heavy metal removal.
Based on the results obtained in this study, we prefer to use RS
as supplementary feedstock, and collect frass as raw material for
biochar for metal removal.
3.3. Adsorption isotherms
Heavy metal ion adsorption isotherms were analyzed by plot-
ting the amounts of adsorbed Pb(II), Cd(II), Cu(II), Zn(II), and Cr(VI)
onto FRSBC (#6 biochar) against their equilibrium concentrations
after 12 h equilibration (Fig. 3). Langmuir and Freundlich isotherm
models were used to fit the experimental data using Eqs. (3)e(5).
The results showed that the Langmuir model fit all data better than
the Freundlich isotherm models (R2 of 0.99, 0.99, 1.00, 1.00, and 1.00
(Table 2) versus 0.32, 0.78, 0.92, 0.98, and 0.97 (Table S1)). The
Langmuir model has a better fit than the Freundlich model corre-
sponding to Pb(II), Cd(II), Cu(II), and Cr(VI) adsorption onto FRSBC
at 298.0 ± 1.0 K, which is valid for monolayer and homogeneous
adsorption on the adsorbent surface with a uniform distribution of
energy level (Huang et al., 2018). Reflected by the maximum
sorption capacities (Qm), the highest Qm values were found as
268.96, 85.74, 72.46, 52.23, and 32.59 mg/g for Pb(II), Cd(II), Cu(II),
and Cr(VI), respectively, using FRSBC (Fig. 3A). Results of adsorption
isotherm model provided the dominance of chemical adsorption in
the process of heavy metal removal onto FRSBC in this study. The
Freundlich model fit the adsorption data poorly (Table S1) and is
not considered for further application.
1148 S.-S. Yang et al. / Environmental Pollution 252 (2019) 1142e1153

Fig. 3. Adsorption model analysis using biochar from frass of mealworms fed rice straw (FRSBC). (A) Adsorption isotherms fit Langmuir models; (B) Adsorption kinetics described
using Pseudo-first order (PFO) and Pseudo-second order (PSO) models; (C) Intra-particle diffusion models (IPD) for Pb(II), Cd(II), Cu(II), Zn(II), and Cr(VI) adsorption onto FRSBC.

Table 2
Parameters of Langmuir adsorption isothermal model, Pseudo-second order kinetics, and intra-particle diffusion rate model fit the data of heavy metals Pb(II), Cd(II), Cu(II),
Zn(II), and Cr(VI) adsorbed onto FRSBC.

Biochar Langmuir Pseudo-second order Intra-particle diffusion

FRSBC-Pb Qm ¼ 268.96 mg/g qe ¼ 258.80 KP1 ¼ 13.32 KP2 ¼ 1.71 KP3 ¼ 1.61
KL ¼ 0.12 L/mg K2 ¼ 6.73 104 C1 ¼ 131.87 C2 ¼ 221.90 C3 ¼ 224.15
R2 ¼ 0.99 R2 ¼ 0.95 R2 ¼ 0.99 R2 ¼ 1.00 R2 ¼ 0.99
FRSBC-Cd Qm ¼ 85.74 mg/g qe ¼ 79.93 KP1 ¼ 3.23 KP2 ¼ 0.49 KP3 ¼ 0.23
KL ¼ 0.12 L/mg K2 ¼ 7.47 104 C1 ¼ 40.29 C2 ¼ 62.32 C3 ¼ 67.09
R2 ¼ 0.99 R2 ¼ 0.94 R2 ¼ 0.99 R2 ¼ 0.99 R2 ¼ 0.99
FRSBC-Cu Qm ¼ 72.46 mg/g qe ¼ 71.85 KP1 ¼ 5.76 KP2 ¼ 1.67 KP3 ¼ 1.12
KL ¼ 0.09 L/mg K2 ¼ 2.78 103 C1 ¼ 17.27 C2 ¼ 47.23 C3 ¼ 53.72
R2 ¼ 1.00 R2 ¼ 0.95 R2 ¼ 1.00 R2 ¼ 1.00 R2 ¼ 0.98
FRSBC-Zn Qm ¼ 52.23 mg/g qe ¼ 48.66 KP1 ¼ 3.45 KP2 ¼ 0.66 KP3 ¼ 0.52
KL ¼ 0.06 L/mg K2 ¼ 1.16 103 C1 ¼ 10.09 C2 ¼ 33.39 C3 ¼ 36.28
R2 ¼ 1.00 R2 ¼ 0.96 R2 ¼ 0.97 R2 ¼ 1.00 R2 ¼ 0.98
FRSBC-Cr Qm ¼ 32.59 mg/g qe ¼ 30.28 KP1 ¼ 2.27 KP2 ¼ 0.70 KP3 ¼ 0.42
KL ¼ 0.08 L/mg K2 ¼ 1.76 103 C1 ¼ 5.53 C2 ¼ 16.22 C3 ¼ 20.52
R2 ¼ 1.00 R2 ¼ 0.94 R2 ¼ 0.99 R2 ¼ 0.99 R2 ¼ 0.99

Note: Biochar from frass of mealworms fed rice straw (FRSBC) showed the best performance in this study.

3.4. Adsorption kinetics
The data collected was used to study adsorption kinetics of
Pb(II), Cd(II), Cu(II), Zn(II), and Cr(VI) on FRSBC are shown in Fig. 3B.
The calculated results of first-order and second-order rate equa-
tions are shown in Table 2 and Table S1. For the contact time studies
of the dynamic adsorption, the values of the regression coefficient
(R2 > 0.96) calculated based on the pseudo-second-order kinetic
model are all better than the pseudo-first-order kinetic model (R2
of 0.72e0.84), indicating that the pseudo-second-order model
could preferably describe the adsorption processes of Pb(II), Cd(II),
Cu(II), Zn(II) and Cr(VI) ions onto FRSBC. According to pseudo-
second-order model assumption, the mechanisms of Pb(II), Cd(II),
Cu(II), Zn(II), and Cr(VI) adsorption processes were limited by
bonding forces through either sharing or through ion/electrons
exchange between the adsorbate and adsorbent (Wang et al., 2018).
Results suggested that the chemical process is the rate-limiting step
in the adsorption process for heavy metal adsorption onto FRSBC in
this study.
To explore the rate-determining step in the heavy metal
adsorption mechanism, the intra-particle diffusion model with a
piecewise regression was applied to fit the experimented data, as
shown in Fig. 3C. The data fit the model well (R2 ¼ 0.97e1.00) and
indicated that the adsorption of all the five metal ions onto the
FRSBC followed three stages: the first stage at 0e60 min, the second
stage at 120e240 min, and the third stage at 360e720 min. A well-
fitted intra-particle model for all stages was obtained. For each
heavy metal ion adsorption process, the corresponding kp1, kp2, and
kp3 showed a downward trend from the first stage to the third stage,
suggesting a decrease in the driving force (i.e. the concentration of
the adsorbate) for adsorption as contact time elapsed (Sewu et al.,
2017). Additionally, values of C > 0 indicated the film diffusion was
involved as the rate-determining step in conjunction with pore
diffusion in describing the adsorption dynamics (Weber, 1984). The
increasing values from C1 to C3 in the three stages corresponded to
the increase in the thickness of the boundary layer, proving greater
contributions of the surface sorption in the rate-controlling step
(Salima et al., 2013). Among the five heavy metal ions tested, the
highest values of C1, C2, and C3 obtained for Pb2þ adsorption onto
FRSBC at each stage suggested that more mass transfer of Pb2þ
across the boundary layer was rate-determining, and further
demonstrated the highest adsorptive capacity for Pb(II) onto FRSBC.
According to the intra-particle diffusion model, a three-stage heavy
metal adsorption mechanism was achieved in this study followed
by (a) the initial rapid adsorption process controlled by the bulk
solution transport; (b) the slower adsorption process induced by
the film diffusion transport; and (c) the final equilibrium stage
caused by the saturated adsorption sites and insufficient pore
transport and adsorption (Chen et al., 2018).
3.5. Adsorption mechanism by FRSBC
The characteristics of biochar (e.g., surface area, porosity, zeta
potential, surface charge, functional groups, and element
 S.-S. Yang et al. / Environmental Pollution 252 (2019) 1142e1153 1149

components) and the main mechanism governing sorption of
Pb(II), Cd(II), Cu(II), Zn(II), and Cr(VI) by FRSBC are discussed below.
The main elemental composition, organic matter content, sur-
face elemental composition, and functional groups of the as-
prepared biochars produced at 600
C were analyzed and pre-
sented in Table 3. The yields of biochars produced from raw ma-
terials varied from 31 to 37% (w/w). The pH varied between 7.06
and 12.76. During pyrolysis, a fraction of surface functional group
elements, e.g. C, H and N, was decreased due to the loss of volatile
organic matter (Ho et al., 2017). Lower C contents in frass-based
biochars (#2, #4, #6, #8, #10, and #12) were observed when
compared with feedstock-based biochars (#1, #3, #5, #7, #9, and
#11), likely due to the conversion and digestion of complicated
organic matters in the feedstocks to CO2, H2O, and frass in the
digestive system of the larvae of T. molitor. The molar ratios of H/C
and N/C are the main parameters for carbonization degree, which is
generally used to characterize the organic compound aromaticity in
biochar (Chen et al., 2018). The H/C and N/C ratios of frass-based
biochars (#2, #4, #6, #8, #10, and #12) were lower than those of
feedstock-based biochars (#1, #3, #5, #7, #9, and #11), indicating
that aromatic structures were formed in the biochar made from
frass, resulting in stronger carbonization and higher aromaticity
that resist decomposition (Chen et al., 2014).
The pH values of aqueous solution with the biochars ranged
from 7.06 to 12.76 (Table 3) since the alkali salts were released due
to the decomposition of organic acids and formation of carbonate
during the pyrolysis process (Yuan et al., 2015). The pH of frass-
based biochars (#2, #4, #6, #8, #10, and #12) was higher than
feedstock-based biochars (#1, #3, #5, #7, #9, and #11). The differ-
ence in pH values between frass-based and feedstock-based bio-
chars was likely due to increased inorganic fraction in frass via
digestive activity in mealworms. Compared with their corre-
sponding frass from mealworms, the crop residues contained more
cellulose and hemicelluloses (Table 1) which could be decomposed
during pyrolysis, producing organic acids and phenolic substances
that lowered the pH of the products (Xu et al., 2013). The alkaline
condition is favorable for the precipitation of heavy metals. This
may explain the enhanced adsorption capabilities of frass-based
biochars (Fig. 2A). In addition, the environmental risk of heavy
metals such as Pb, Cu, Cd, and Zn leaching would be significantly
reduced with alkaline pH of the as-prepared biochar (Ho et al.,
2017).
The surface electrical characteristics of the biochars was inves-
tigated by determining Zeta potential before and after the
adsorption tests. The Zeta potential values of the FRSBC decreased
from 1.17 to 40.63 mV as pH increased from 1.0 to 6.0 (Figs. S1A
and SI), indicating that the surface charge on the biochars
became more negative as pH increased. The negative charge value
on the surface of the biochar is favorable for the active sites to
attract metal ions (Pb2þ, Cd2þ, Cu2þ, and Zn2þ) with positive
charges, resulting in electrostatic interaction (Meng et al., 2014). For
K2Cr2O7, Cr(VI) was adsorbed on the surface functional groups and
further reduced to Cr(III) using electrons provided by the biochar as
described previously (He et al., 2017; Xu et al., 2019; Zhang et al.,
2018). Hence, the cationic exchange could be a major mechanism
for propranolol sorption in addition to hydrophobic partition
(Wang et al., 2016). The lower pHpzc of 3.9 of FRSBC in aqueous
solution could increase the adsorption ability of positively charged
heavy metal ions via its surface electrostatic attractions due to the
negative potential effect (Ho et al., 2017). When pH > pHpzc, the
proton in the surface of binding sites decreased, and the negative
charge intensity on the biochar surface increased. Consequently,
the electrostatic attraction between these biochars and heavy
metal increased and thus, the adsorption capacity was enhanced
(Wang et al., 2019). Data values of the Zeta potentials of FRSBC
increased after heavy metal adsorption compared to those before
testing (Figs. S1B and SI). The increases of Zeta potentials after
cation heavy metal adsorption (Pb(II), Cd(II), Zn(II), and Cu(II))
suggested the formation of hydroxide ions (OH) on the surface of
biochar after pyrolyzing (Sewu et al., 2017). Besides, Cr(VI) in
aqueous solution is mainly in the form of oxygen-containing anions
(CrO2 2
4 , Cr2O7 ). The Zeta potential value of 1.17 mV for the FRSBC at
pH of 1.0 (Fig. S1A) indicated the formation of positive charges on
the surface of biochar. Therefore, Cr(VI) can be easily bound to its
electropositive surface through electrostatic interaction, form
complexes with its surface groups and then Cr(VI) is reduced to
Cr(III) as described previously (He et al., 2017). Biochar can supply
the electron donor source for Cr(VI) reduction to Cr(III). Results
demonstrated that electrostatic interaction was one of the major
mechanisms controlling the adsorption of heavy metal ions on
FRSBC.
The typical morphology of FRSBC obtained from pyrolysis of
frass egested from feeding raw RS showed obvious pore structures
with many regular and vertical channels (Fig. S2), exhibiting a
strong pollutant adsorption ability due to the prominent pore-
filling effect (Chen et al., 2018). Among the biochars in this study,
FRSBC had the maximal BET surface area of 221.53 m2/g and a total
pore volume of 0.117 cm3/g (Table S3), proving the pore-filling ef-
fect in FRSBC. This observation was also supported with the SEM
images, where the typical morphology of FRSBC showed obvious
pore structures with many well-formed pores and underlying
vertical channel structures (Fig. S2), also exhibiting a strong
pollutant adsorption ability due to the prominent pore-filling effect
(Zhu et al., 2014). After individual heavy metal adsorption tests,
comparison of the change in the SEM-EDX elemental mapping
confirmed the presences of Pb, Cd, Cu, Zn, and Cr-rich regions on
the surface of FRSBC (Fig. S2).
FTIR spectra of the surface functional groups of FRSBC before

Table 3
Major elements and Brunauer-Emmett-Teller (BET) of the as-prepared biochars from six crop residues and the corresponding egested frass pyrolyzed at 600
C.

Biochars Yield, % pH N, % C, % H, % N/C H/C BET surface area (m2/g) Total pore volume (cm3/g)

WBBC (#1) 31.25 7.89 4.59 71.69 2.47 0.064 0.034 37.32 0.017
FWBBC (#2) 32.76 8.81 3.12 57.69 1.69 0.054 0.029 66.76 0.032
WSBC (#3) 34.21 8.58 1.16 62.50 1.90 0.019 0.030 72.77 0.050
FWSBC (#4) 35.43 9.19 1.02 57.83 1.60 0.018 0.028 130.66 0.071
RSBC (#5) 36.38 10.89 1.88 60.98 1.97 0.031 0.032 120.49 0.068
FRSBC (#6) 36.89 12.76 1.54 55.41 1.69 0.028 0.030 221.53 0.117
RBBC (#7) 33.92 7.06 1.50 50.92 1.85 0.029 0.036 8.18 0.010
FRBBC (#8) 34.07 7.21 0.93 43.99 1.53 0.021 0.035 14.52 0.035
RHBC (#9) 35.78 8.26 1.79 57.75 1.92 0.031 0.033 87.54 0.053
FRHBC (#10) 36.11 9.74 1.45 50.03 1.48 0.029 0.030 127.60 0.092
CSBC (#11) 35.89 9.27 1.88 76.76 2.10 0.024 0.027 137.52 0.069
FCSBC (#12) 36.48 10.23 1.67 72.07 1.88 0.023 0.026 162.96 0.094
1150 S.-S. Yang et al. / Environmental Pollution 252 (2019) 1142e1153

and after heavy metal adsorption of Pb(II), Cd(II), Cu(II), Zn(II), and
Cr(VI) were compared (Figs. S3AeE). The characteristic peak as-
signments in FTIR spectra represented the existence of different
functional groups. Overall, results demonstrated qualitative differ-
ences between FRSBC surface functional groups before and after
adsorption. The band at 3200-3500 cm1 in the spectra of the
tested biochars was assigned to phenolic eOH stretching (Qiu et al.,
2008). After sorption, some changes at 3200-3500 cm1 compared
to the control FRSBC were displayed in Fig. S3. A similar observation
was reported by Xu et al. (2013), indicating the possibility of surface
adsorption through their complexation with phenolic eOH group.
The bands around 1510-1644 cm1 were attributed to the aromatic
carbonyl/carboxyl C¼O and the aromatic C¼C stretching modes (Xu
et al., 2013; Wang et al., 2017), and changes of the peak at
1600 cm1 after adsorption indicated surface complexation of
heavy metal by delocalized p electrons. Additionally, the bands at
around 1360, 1414, and 1430 cm1 were associated with OeH vi-
brations of hydroxyl groups or CeH stretching vibrations (Meng
et al., 2014; Wang et al., 2017; Huang et al., 2018). The bands be-
tween 1100 and 1000 cm1 were attributed to C¼O stretching vi-
bration of carboxyl (Zhang et al., 2015). The intensities of C¼O and
eOH groups changed after heavy metal adsorption, indicating that
the oxygen-containing groups such as eOH and eCOOH group
were involved in the adsorption process (Huang et al., 2018).
Furthermore, the typical broad bands around 1400 cm1 changed
after adsorption, indicating that ion exchange occurs between
adsorbent and adsorbate (Miller and Wilkins, 1952). The coexis-
tence of ion exchange reactions between metal ions and mineral
cations was mainly responsible for the electrostatic outer-sphere
complexation mechanism and co-precipitation/inner-sphere
complexation (Ho et al., 2017), and was therefore confirmed as
another significant chemical adsorption mechanism by FRSBC
applied in this study. The bands below 600 cm1 were due to MeX
stretching vibrations of inorganic halogen salts (such as KCl and
CaCl2) (Ment et al., 2014).
XPS analysis was employed to identify the coordination types
between heavy metal ions and these functional groups. The XPS
analyses, including Pb(II), Cd(II), Cu(II), Zn(II), and Cr(VI), were
performed to study the changes of binding energy and valence
states of heavy metal ions in FRSBC before and after adsorption.
Compared to raw FRSBC (Fig. S4A), the full-range XPS spectra of
FRSBC after Pb(II) adsorption showed new peaks (Fig. S4B). The
primary Pb 4f peaks attributed to Pb(II) were recorded at 137.7 eV
(4f7/2) and 142.5 eV (4f5/2), which is consistent with the results
reported by Bonato et al. (2012). Similarly, the Cd 3d peak area
consists of the main 3d3/2 spin-orbit components at binding en-
ergies of around 404.3 and 411.2 eV (Chang et al., 2007), respec-
tively, and the results suggest that the deconvolution of the above
peak proved the presence of Cd(II) in the form of CdO (404.3 eV)
after the adsorption of Cd(II) onto FRSBC (Fig. S4C). In the XPS
spectrum (Fig. S4D) of Cu(II) adsorption onto FRSBC, the charac-
teristic peak at 933.7 eV, which is responsible for the presence of
Cu(II), can be interpreted most likely as CuO. These results clearly
demonstrate that the deposition and chelation of Cd(II) and Cu(II)
played a significant role in the adsorption process, which is in
accordance with the study of Zhou et al. (2018). The main compo-
nent is centered at 1021 eV (Fig. S4E), ascribed to metallic Zn of the
Zn 2p3/2 peak area (Ballerini et al., 2007). In Fig. S4F, the XPS
spectrum shows two Cr 2p3/2 and Cr 2p1/2 peaks that are centered
at 575.7 and 585.2 eV, respectively, which is consistent with Cr (III)
and Cr(VI), respectively. Thus, analysis of XPS spectrum (Fig. S4F)
indicates that Cr ions are adsorbed on FRSBC as Cr(III) and Cr(VI),
which further suggests that a part of adsorbed Cr(VI) anions was
reduced to Cr(III) on the surfaces of FRSBC during adsorption
period, as described in previous reports (Hu et al., 2009; Xu et al.,
2019; Zhang et al., 2018). In this study, XPS spectra, associated
with chemical analysis, FTIR analysis, and SEM-EDX mapping
confirmed the presence of Pb(II), Cd(II), Cu(II), and Cr(VI) on the
surface of FRSBC after adsorption.
In this study, the chemisorption plays a dominant role in heavy
metal removal according to kinetic studies. Various mechanisms
including the electrostatic interaction, p-p interaction, functional
groups, hydrogen bonding, ion exchange, electrostatic outer-sphere
complexation, and co-precipitation/inner-sphere complexation
were demonstrated. Different mechanisms dominated the
sequestration of Pb (II) and Zn(II) via complexation, cation ex-
change, and precipitation; Cd and Cu via complexation, cation ex-
change, and precipitation; deposition and chelation; and Cr (VI) via
electrostatic interaction, complexation, and the reduction of Cr(VI)
to Cr(III). The adsorption or sequestration of Cr(VI) was mainly
conducted by oxygen-containing functional groups such as
carboxyl and hydroxyl groups, and subsequent Cr(III) formed was
complexed with functional groups on biochar.
3.6. Significance of the clean production approach tested in this
study
In this study, we conducted detailed tests of biochars generated
from mealworm frass for metal removal in five different cases and
proved the feasibility of our approach of clean production process.

Table 4
Comparison of the adsorption capacities of biochars from different animal wastes for different heavy metals.

Sour materials Heavy metals Biochar preparation pH value Initial Initial dosage BET (m2/ Qm (mg/g) References
conditions concentration (mg/ml) g)
(mg/L)

FRSBC Pb(II), Cd(II), Cu(II), 600
C for 1.5 h 6.0 (5.0 for 25e600 1.0 221.53 268.96, 85.74, 72.46, This study
and Cr(VI) Cu(II)) 52.23, and 32.59
Fresh and composted Cu2þ 400
C for 2 h 5.0 0.1e5 mM 5.0 93.75 and 17.71 and 21.94 Meng et al.
swine manure Cu(NO3)2,3H2O 73.49 (2014)
Swine manure Cd2þ 450
C for 1 h 4.5 0.3e100 2e160 mg into 159.3 52.45 Xu et al.
8 mL tubes (2014)
Earthworm manure Cu2þ and Cd2þ 700
C for 2 h 5.0 and 6.5 50-120 and 50- 2.0 38.28 36.56 and 29.31 Wang et al.
200 (2017)
2þ

Swine-manure Cd 250 C for 4 h 6.0 0.3e150 e 1.87 81.32 Han et al.
(2017)
Pig manure Cd2þ
700
C with a heating 5.0 ± 0.05 2e300 1.0 11.37 212.51e240.23 Wang et al.
rate of 8
C/min (2018)
Chicken-manure Cd2þ 700
C for 4 h 6.0 10e200 1.0 10.89 149.55 Huang et al.
(2018)
Pig manure Pb2þ 700
C 5.0 3.13e313 1.0 e 209.49 Wang et al.
(2019b)
 S.-S. Yang et al. / Environmental Pollution 252 (2019) 1142e1153 1151

The biochars generated from mealworm frass can be likely applied Conflicts of interest
for other purposes. However, the pyrolysis temperature, heating
rate and treatment process may be different depending on The authors declare no conflict of interest.
application.
Based on the data obtained in this study and reported in other Acknowledgments
literature, biochar has the potential for metal sorption and has
received increasing attention due to its ability to store large amounts The authors gratefully acknowledge the financial support by the
of carbon, increase crop yield, reduce soil emission of greenhouse National Natural Science Foundation of China of China (Grant No.
gases, improve soil quality, decrease nutrient leaching, reduce irri- 51708154), the Open Project of State Key Laboratory of Urban Water
gation and fertilizer requirements, enhance soil fertility for agricul- Resource and Environment (Grant No. ES201906), the State Key
tural production, and improve composting during the past decade Laboratory of Urban Water Resource and Environment (Grant No.
(Pandey et al., 2016). We compared the sorption capacities of FRSBC HC201621-01), the Key Laboratory of Research center for Eco-
(biochar from frass with fed rice straw at 600
C) for Pb(II), Cd(II), Environmental Science, Chinese Academy of Sciences (Grant No.
Cu(II), and Cr(VI) with various biochars made from animal wastes or kf2018002). Dr. W.-M. Wu appreciates the support by the Woods
manure (Table 4), including cow manure (Xu et al., 2013), chicken Institute for Environment at Stanford University (Award 1197667-
manure (Huang et al., 2018), earthworm manure (Wang et al., 2017), 10-WTAZB). The authors thank Professor Craig S. Criddle, Stanford
and swine manure (Meng et al., 2014; Xu et al., 2014; Han et al., 2017; University, for his support and suggestion during this study, and
Wang et al., 2018; Wang et al., 2019b). The biochar made from the Ms. Julia T. Wu, University of Wisconsin-Madison, Madison, and Ms.
frass of mealworms fed with rice straw showed equal to superior Andria T. Wu, DePaul University, Chicago, for their help in manu-
adsorption performance compared to others. script and figure preparation.
Among six crop residues, RS performed well as supplementary
feedstock to rear mealworms for insect biomass production and the
frass egested can be converted to biochar and be used as a high- Appendix A. Supplementary data
quality bioadsorbent for improving soil quality and enhancing
soil fertility for agricultural production. The results of our tests Supplementary data to this article can be found online at
prove our clean production design that can help mealworm https://doi.org/10.1016/j.envpol.2019.06.028.
farming achieve a low cost for feedstock while introducing the
additional valuable product biochar, which can reduce waste gen- Nomenclature
eration. This could be a simple and efficient way in rural areas to
reduce transportation costs and achieve further commercial utili- ASTM American Society for Testing and Materials
zation from crop wastes. The proposed approach in this study BET Brunauer-Emmett-Teller
shows significance potential to achieve economic, social, and C The thickness of the boundary layer (mg/g)
ecological benefits. Ce The dye concentration at equilibrium (mg/L)
CS Corn straw
4. Conclusion CSBC (#11) Biochar via pyrolysis at 600
C from corn straw (CS)
feedstock
The results have proven the feasibility of a clean production EA Elemental analysis
approach for the production of mealworm biomass by utilizing crop FTIR Fourier transform infrared spectroscopy
residues as feedstock and the egested frass as raw material to FCSBC (#12) Biochar via pyrolysis at 600
C from corn straw (CS)
generate biochar without waste residues. fed frass
Mealworms can live on different lignocellulose-rich crop resi- FRBBC (#8) Biochar via pyrolysis at 600
C from rice bran (RB) fed
dues including WS, RS, RB, CS, and RH as sole feedstock as well as frass
they can when fed with normal WB feed over a 32-day period. FRHBC (#10) Biochar via pyrolysis at 600
C from rice husk (RH) fed
Mealworms prefer to chew and ingest RS and CS, and frass
degrade cellulose, hemicellulose, and lignin in their gut. Except FRSBC (#6) Biochar via pyrolysis at 600
C from rice straw (RS) fed
for WB, the sequence of degradability of the feedstocks is frass
RS > RB > CS > WS > RH. RS, RB, and CS can serve as supplementary FWBBC (#2) Biochar via pyrolysis at 600
C from wheat bran (WB)
feedstock to rear mealworms. fed frass
Biochars generated from the frass of mealworms fed with the six FWSBC (#4) Biochar via pyrolysis at 600
C from WS fed frass
raw feedstocks performed better than those made from original FRSBC-Cd Cd adsorbed by FWSBC
feedstock materials for the removal of metals Pb(II), Cd(II), Cu(II), FRSBC-Cr Cr adsorbed by FWSBC
Zn(II), and Cr(VI). FRSBC-Cu Cu adsorbed by FWSBC
Biochar from frass of mealworms fed RS at 600
C (FRSBC) FRSBC-Pb Pb adsorbed by FWSBC
possessed the best adsorption capabilities for all the metal ions FRSBC-Zn Zn adsorbed by FWSBC
tested. The adsorption isotherms for the metals onto FRSBC fit the KL Langmuir constant (L/mg)
Langmuir model and the kinetic data fit pseudo-second order re- KF Freundlich adsorbent capacity (mg/g)
action. The heavy metal adsorption process can be well described k1 Rate constants of the pseudo-first-order rate constant
using the Intra-particle diffusion model. (min1)
Different mechanisms dominated adsorption for Pb(II), Cd(II), k2 Rate constants of the pseudo-second-order kinetic
Cu(II), and Zn(II), including electrostatic interaction, p-p interac- models (g/mg∙min)
tion, functional groups, hydrogen bonding, ion exchange, electro- kp Intra-particle diffusion rate constant (mg/g∙min0.5)
static outer-sphere complexation, and co-precipitation and inner- Mealworm The larva of Tenebrio molitor Linnaeus
sphere complexation. To remove Cr(VI), additional reduction NDF Neutral detergent fiber
transformation was involved, and biochar provided an electron nF The heterogeneity factor
donor source. Qe Adsorption capacity of dye onto adsorbents (mg/g)
1152 S.-S. Yang et al. / Environmental Pollution 252 (2019) 1142e1153
Qm Maximum adsorption capacity of dye onto adsorbents
(mg/g)
qe Adsorption capacity at equilibrium (mg/g)
qt Adsorption capacity at time t (mg/g)
RB Rice bran
RBBC (#7) Biochar via pyrolysis at 600
C from rice bran (RB)
feedstock
RH Rice husk
RHBC (#9) Biochar via pyrolysis at 600
C from rice husk (RH)
feedstock
RS Rice straw
RSBC (#5) Biochar via pyrolysis at 600
C from rice straw (RS)
feedstock
SEM Scanning electron microscopy
SEM-EDX SEM-energy-dispersive spectrometry
SR Survival rate
WB Wheat bran
WBBC (#1) Biochar via pyrolysis at 600
C from wheat bran (WB)
feedstock
WS Wheat straw
WSBC (#3) Biochar via pyrolysis at 600
C from wheat straw (WS)
feedstock
XPS X-ray photoelectron spectroscopy
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