Journal of Hazardous Materials xxx (xxxx) xxxx

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Journal of Hazardous Materials

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

Effects of microbial culture and chicken manure biochar on compost

maturity and greenhouse gas emissions during chicken manure composting
Hongyu Chena,e,1, Sanjeev Kumar Awasthia,1, Tao Liua, Yumin Duana, Xiuna Rena,
Zengqiang Zhanga, Ashok Pandeyc,d,**, Mukesh Kumar Awasthia,b,*
a
College of Natural Resources and Environment, Northwest A&F University, Yangling 712100, PR China
b
Swedish Centre for Resource Recovery, University of Borås, 50190 Borås, Sweden
c
Centre for Innovation and Translational Research, CSIR-Indian Institute of Toxicology, Lucknow 226 001, India
d
Department of Civil and Environmental Sciences, Yonsei University, Seoul, South Korea
e
Institute of Biology, Freie Universität Berlin Altensteinstr. 6, 14195 Berlin, Germany

G R A P H I C A L A B S T R A C T

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

Editor: Deyi Hou The effects of chicken manure biochar (CMB) and chicken manure integrated microbial consortium (CMMC) as
Keywords: co-amendments were assessed on compost maturity and reduction of greenhouse gases and ammonia (NH3)
Greenhouse gases emissions during chicken manure composting. Composting was conducted using six combinations of CMB and
Ammonia CMCC (0 % CMB + 0 % CMMC, 0 % CMB + 10 % CMMC, 2 % CMB + 10 % CMMC, 4 % CMB + 10 % CMMC, 6
Chicken manure biochar % CMB + 10 % CMMC, 10 % CMB + 10 % CMMC added on a dry weight basis) in six polyvinyl chloride
Chicken manure composting composting reactors for 42 days under an aerobic environment. Co-amendment of CMB and CMMC extended the
thermophilic stage and promoted compost maturity. The release of greenhouse gases [nitrous oxide (N2O) and
methane (CH4)] and NH3 from treatments co-amended by CMB and CMMC were reduced by 19.0–27.4 %,
9.3–55.9 % and 24.2–56.9 %, respectively, compared with the control. In addition, a redundancy analysis

Abbreviations: C/N ratio, carbon to nitrogen ratio; CH4, methane; CM, chicken manure; CMB, chicken manure biochar; CMMC, chicken manure integrated microbial
consortium; CO2, carbon dioxide; EC, electrical conductivity; GHG, greenhouse gases; GI, germination index; GWP, global warming potential; N2O, nitrous oxide;
NH3, ammonia; OM, organic matter; RDA, redundancy analysis; TK, total potassium; TKN, total kjeldahl nitrogen; TNa, total sodium; TOC, total organic carbon;
TOM, total organic matter; TP, total phosphorus; WS, wheat straw
⁎
Corresponding author at: College of Natural Resources and Environment, Northwest A&F University, Yangling 712100, PR China.
⁎⁎
Corresponding author at: Centre for Innovation and Translational Research, CSIR-Indian Institute of Toxicology, Lucknow 226 001, India.
E-mail addresses: zhangzq58@126.com (Z. Zhang), ashokpandey1956@gmail.com (A. Pandey), mukesh_awasthi45@yahoo.com (M.K. Awasthi).
1
Equally contributing authors.

https://doi.org/10.1016/j.jhazmat.2019.121908
Received 24 June 2019; Received in revised form 4 November 2019; Accepted 15 December 2019
0304-3894/ © 2019 Elsevier B.V. All rights reserved.

Please cite this article as: Hongyu Chen, et al., Journal of Hazardous Materials, https://doi.org/10.1016/j.jhazmat.2019.121908
H. Chen, et al.
showed that the C/N ratio and temperature had a significant relationship with greenhouse gases and NH3
emissions among all physiochemical characteristics.
1. Introduction
With the sustained, stable, and rapid development of the livestock
farming industry in China, the large-scale standardization and in-
dustrialization of the livestock industry is accelerating, and the pro-
duction capacity is being constantly improved. However, this devel-
opment is accompanied by a concomitant increase in pollution and
other environmental problems (Chen et al., 2018; Xiao et al., 2019).
Currently, in China, approximately 3.8 billion tons of livestock and
poultry wastes are produced annually, of which about 1.5 billion tons
are livestock manure, accounting for nearly 39.5 % of the total waste
(National Bureau of Statistics of China, 2017). As a type of organic solid
waste, livestock manure is also an important fertilizer resource in
agricultural production because it is rich in organic matter (OM) and
nutrients such as nitrogen, phosphorus, and potassium (Neslihan,
2019).
However, the improper disposal of livestock manure can easily be-
come an agricultural non-point pollution source; meanwhile, mal-
odorous and greenhouse gases such as NH3 and hydrogen sulfide re-
leased from livestock manure can also seriously damage the air quality
and aggravate the global greenhouse effect. Related research studies
have proven that animal husbandry is the main emission source of
methane (CH4) and nitrous oxide (N2O), accounting for approximately
37 % of CH4 and 65 % of N2O globally (IPCC: Climate Change 2014,
2014). The research also showed that CH4 and N2O released from an-
imal husbandry accounted for 80 % of agricultural non-carbon-dioxide
greenhouse gas emissions, which comprised 12 % of global anthro-
pogenic GHG emissions. CO2, CH4, and N2O are three major GHGs
produced by livestock manure. An Intergovernmental Panel on Climate
Change (IPCC) report showed that the global warming potential (GWP)
of CH4 is 28 times that of CO2, while the GWP of N2O is 265 times that
of CO2 (IPCC: Climate Change 2014, 2014). Related studies also showed
that the contribution rates of CH4 and N2O produced by livestock
manure to the total global CH4 and N2O emissions are 5–10 % and 7 %,
respectively, which should not be ignored (Awasthi et al., 2019; Ussiri
and Lal, 2017).
Aerobic composting has proven to be an effective method to convert
livestock manure into high-quality organic fertilizer and can also realize
the goals of reduction, harmlessness, and resource utilization of live-
stock manure (Ravindran et al., 2019). However, with the degradation
and humification of OM during the aerobic composting, a large amount
of ammonia and greenhouse gases will be released. This can lead to
serious pollution to the atmosphere and environment, and will cause
the loss of nitrogen and carbon during composting. Thus, it will affect
the quality of the final products of composting. Biochar is type of a
highly aromatic and insoluble solid material produced by the pyrolysis
of biomass under a high temperature and incomplete or complete an-
oxic conditions (Qiu et al., 2019). Therefore, biochar generally pos-
sesses excellent properties such as highly stable characteristics, devel-
oped pore structures, and abundant surface functional groups. Thus,
biochar could be an excellent potential bulking agent for aerobic
composting because it can adjust the moisture and porosity of the
composting and provide a suitable living environment for micro-
organisms (Akdeniz, 2019). Related research studies have shown that
exogenous additives such as microbial agents or biochar can effectively
alleviate and mitigate nitrogen loss and the emission of greenhouse
gases during aerobic composting. This has important practical sig-
nificance for the optimization of aerobic composting and control of
environmental pollution (Agyarko-Mintah et al., 2017a).
A study by Agyarko-Mintah et al. (2017a) showed that green waste
2
Journal of Hazardous Materials xxx (xxxx) xxxx
and poultry litter biochar can significantly decrease the total nitrogen
(51 %) and NH3 (60 %) losses and enhance the fertilizer value of final
composting products. Chen et al. (2017a,Chen et al., 2017b studied the
effects of 10 % cornstalk, bamboo, woody, layer manure, and coir
biochar on layer manure composting. Among them, cornstalk biochar
had the best inhibitory effect on NH3 and CH4 volatilization, which
were reduced by 38.5 % and 22.2 %, respectively, compared with the
control (0 %). The inhibitory effect of biochar on ammonia and GHG
emissions during composting is related to raw materials and their sur-
face properties.
Although many studies have focused on the effects of biochar as an
additive to the GHG and NH3 emissions during composting, no study
has reported on the influence of chicken manure biochar (CMB) com-
bined with chicken manure integrated microbial consortium (CMMC) as
a co-amendment to Chicken manure (CM) composting, especially with
regard to nitrogen fixation, GHG emissions, and composting maturity.
In this study, since biochar as an amendment in composting could
provide a suitable breeding and metabolic environment for the main
contributor of composting (microorganisms), a microbial consortium
cultured by raw material (chicken manure) was added to composting
with biochar to study the specific effects of biochar on composting and
the influence on internal microbial activities. The purpose of this study
was to detect the dynamic changes of GHG and NH3 emissions, evaluate
the influence of CMB combined with CMMC as additive to the maturity
of CM composting, and study the correlation between them.
2. Materials and methods
2.1. Collection and preparation of raw materials
Fresh CM was purchased form a local chicken farm (Yangling,
Shanxi Province, China). Part of the CM was flattened on the ground for
2 weeks (and regularly turned during this time). Then, the dried CM
was crushed into a small size by a mechanical crusher. The biochar was
prepared from CM biomass via slow and dry pyrolysis at a temperature
of 550–600 °C at atmospheric pressure for 24 h, which was initiated by
the pyrolysis of feedstock from the bottom of the kiln. The some basic
properties of the biochar are shown in Table 1, and the BET surface area
(678.46 m2 g−1), the pore volume (0.18 cm3 g−1) and the pore size
(4.98 nm), S (0.15 ± 0.02 %), O (13.4 ± 0.08 %) and H (2.38 ± 0.04
%), which were determined by standard methods (Qiu et al., 2019). To
develop an effective bacterial consortium for CM composting, CMMC
was cultivated at 55 ℃ by shaking (200 rpm) for 72 h in a modified
basal-salt medium according to a study by Ronald (1995). Wheat straw
(WS) was collected from an agricultural experimental station (Yangling,
Shaanxi Province, China) and cut into 1-cm3 blocks by a mechanical
chopper to ensure regular mixing of the raw materials. The
Table 1
Characteristics of composting materials used in the present experiments.
Parameters CM WS CMB
Moisture content (%) 78.56 ± 0.12 9.23 ± 0.11 1.04 ± 0.02
TKN (%) 2.39 ± 0.04 4.59 ± 0.03 0.45 ± 0.01
Organic matter (%) 69.74 ± 0.89 90.96 ± 1.12 78.82 ± 1.50
C/N ratio 29.18 ± 1.86 19.82 ± 1.02 175.16 ± 3.49
pH 6.77 ± 0.01 7.11 ± 0.01 9.32 ± 0.05
EC (μS/cm) 6280 ± 25 2860 ± 18 1476 ± 0.21
CM - Chicken manure, WS - Wheat straw, CMB - Chicken manure biochar, EC -
Electrical conductivity, TKN - Total kjeldahl nitrogen, C/N ratio: Carbon to
nitrogen ratio. Results are the average of three repeats ± standard deviation.
H. Chen, et al.
characteristics of each composting material are listed in Table 1.
2.2. Experimental design
The composting experiment was performed at the research base of
Northwest A&F University by using 100-L polyvinyl chloride (PVC)
reactors. The structure and operation of the composting reactors were
presented in our previous studies (Awasthi et al., 2017a). Six treatments
(T1–T6) were designed in this experiment. CM and WS were regularly
mixed together in the ratio of 5:1 (dry weight basis) for all treatments.
Different amounts of CMB were added in different treatments: [0 %
(T1), 0 % (T2), 2 % (T3), 4 % (T4), 6 % (T5), and 10 % (T6) on a dry
weight basis]. Expect for the control treatment (T1), the treatments had
10 % CMCC added on a dry weight basis. The C/N ratio of mixed raw
materials was adjusted to 25 by adding 22 kg of CM and 4.7 kg of WS.
For each treatment, 500-g plastic beans were added to each composter
to achieve a bulk density of 0.5 kg/L, and 1.52 L of deionized water was
added to each mixture to maintain a moisture content of 60 %. After
being fully mixed, each mixture was placed in the reactor and com-
posted for 42 days. The air was pumped from the bottom of the reactor
by an air blower, and the flow rate was controlled at 0.5 L h−1 kg−1 dry
weight. The compost was mixed thoroughly prior to the collection of
samples at 0, 3, 7, 14, 21, 28, 35, and 42 days. The samples collected
were divided into two parts: one portion was stored in a refrigerator at
4 °C for the determination of the fresh sample, and the other was air-
dried and sieved through a 0.1-mm sieve for subsequent determination
of physicochemical parameters.
2.3. Analysis
The temperature of the environment and each composting system
was monitored simultaneously using a thermometer every 12 h. NH3,
GHGs (N2O, CH4, and CO2) and physicochemical parameters [pH,
moisture content, electrical conductivity (EC), total kjeldahl nitrogen
(TKN), and total organic carbon (TOC)] were measured via standard
methods (Zucconi et al., 1981; TMECC (Test Methods for the
Examination of Composts and Composting), 2002). All analyses were
repeated three times to ensure the accuracy and reliability of all data.
Meanwhile, data were subjected to a one-way analysis of variance
(ANOVA), and multiple comparison tests were performed to compare
the least significance difference (LSD) for p = 0.05 values using the
SPSS 13.0 software package (SPSS for Windows, Version 13.0, USA).
Redundancy analyses (RDA) were performed by using the Canoco 5
software package to identify the correlation between the NH3, GHG
emissions, and physiochemical properties.
Fig. 1. The change of temperature (a) and pH (b) during the composting process of all treatments. CMB: Chicken manure biochar, CMMC: Chicken manure integrated
microbial consortium. Value are the average of three repeats and error bars indicates the standard deviation.
3
Journal of Hazardous Materials xxx (xxxx) xxxx
3. Results and discussion
3.1. Changes in temperature and pH during composting
Temperature, as one of the crucial criteria for evaluating whether
aerobic composting successfully achieves maturity, is an important in-
dicator that can intuitively reflect the composting process and microbial
activity during composting (Duan et al., 2019a). The dynamic changes
in temperature for all treatments in this study are shown in Fig. 1a. As
can be seen from the figure, the dynamic trends are consistent with
those of most aerobic composting studies (Ussiri and Lal, 2017) and
usually have three typical stages: mesophilic, thermophilic, and mature
(Qiu et al., 2019). After the initiation of the experiment, the tempera-
ture for all treatments rapidly increased and reached the thermophilic
stage (> 50 °C) during the first 2 days. Among all treatments, the
treatments with the addition of CMB (T3, T4, T5, and T6) reached the
thermophilic stage on the first day of composting, while T1 (control)
and T2 arrived at the thermophilic stage one day later. The thermo-
philic stage of all treatments lasted for more than 5 days, which meant
that pathogenic microorganisms and weed seeds in the mixture were
effectively eliminated, and thus all treatments met the standards of
harmless composting (Jain et al., 2018). The temperature peaks of all
treatments (T1–T6) were 57.3 (day 7), 65.25 (day 6), 66.05 (day 4),
66.2 (day 3), 69.5 (day 4), and 72.5 ℃ (day 4). Compared with the
control, the addition of CMB could significantly promote rapid warming
and increase the temperature peak for CM composting. This may be
owing to the special characteristics of CMB that make the concentration
and distribution of oxygen more uniform and sufficient. Meanwhile,
CMB can also provide favorable habitats and environmental conditions
for microbial reproduction and metabolism, thus promoting the de-
gradation of OM and rapidly increasing the temperature in the early
stage of composting (Qiu et al., 2019; Awasthi et al., 2017a). Moreover,
the thermophilic stage of each treatment lasted for 6 (T1), 8 (T2), 9
(T3), 10 (T4), 10 (T5), and 11 (T6) days. Addition of CMB significantly
(p < 0.05) prolonged the thermophilic period of chicken manure
composting, which is more conducive to the maturity of the compost.
These results are similar to those of the studies by Chen et al. (2018)
and Awasthi et al. (2017b), who studied the effects of biochar and clay
as additives to chicken manure. At the end of the thermophilic period,
the OM in the mixture gradually depleted, and the temperature of each
treatment gradually decreased and stayed consistent at room tem-
perature at the end of composting. Notably, the temperature of the
control (T1) increased on the 15th day and lasted for about 1 week; this
may have occurred because of the incomplete degradation of OM
during the thermophilic period of T1. Continuous degradation of OM
H. Chen, et al.
during this period resulted in an increase in temperature and lasted for
1 week. The above results indicate that the addition of CMB can sig-
nificantly (p < 0.05) promote a rapid increase in temperature and
prolong the thermophilic period; of all CMB compositions, 10 % CMB
showed the most effective increase. Vandecasteele et al. (2016) and
Agyarko-Mintah et al. (2017b) found similar results in the co-com-
posting of pig manure, struvite, and medical stone.
Very high or very low composting pH decreases the decomposition
rate of OM. In particular, excessive pH results in more nitrogen loss in
the form of NH3 volatilization, thus causing an increase in nitrogen loss
and a reduction in fertilizer efficiency (Chan et al., 2016). As shown in
Fig. 1b, addition of CMB can significantly (p < 0.05) increase the
initial pH of the mixture and the pH of the final products, while the
addition of CMMC has no significant influence on the initial pH of the
compost. Czekala et al. (2016) found similar results; the pH of the
composting products was higher than that of the control in chicken
manure and wheat straw co-composting that was amended with bio-
char. The initial pH of each treatment (T1–T6) was 6.77, 6.70, 6.85,
6.9, 7.12, and 7.44, respectively, with increase in the added CMB. In the
early stage of composting, the pH of each treatment increased rapidly
with increase in temperature. Among them, the pH of T1 and T2 peaked
on the 14th day and then gradually decreased, while for treatments
amended with CMB (T3, T4, T5, and T6) it peaked on day 7. The in-
crease of pH in first few days may have been caused by the rapid de-
gradation of OM, leading to the accumulation of a large amount of
ammonia. The subsequent decline in pH may be related to the volati-
lization of NH3 and emission of CO2. At the maturity stage, the pH of
each treatment had a different degree of recovery; this may be due to
the decomposition of organic acids. Then, as ammonization gradually
weakened, nitration caused a slight decrease in pH (Liu et al., 2017). At
the end of composting, the pH of T1-T6 were 7.85, 7.94, 7.83, 8.05,
8.20, and 8.24, respectively.
The results of this study indicate that the addition of CMB (which is
alkaline) can significantly increase the pH of the mixture. This is con-
sistent with the studies of Liu et al. (2017) and Duan et al. (2019b), who
studied the effects of biochar on poultry manure composting. There was
no significant difference in the pH of treatments T1 and T2, which in-
dicated that the addition of CMMC had no effect on the changes in pH.
Research by Zhang et al. (2018), who added 0–15 % biochar to pig
manure composting, saw no increase in pH. Li et al. (2015) arrived at
the same conclusion that the addition of biochar did not affect the pH of
the sludge compost. It can be seen that the results of current research
studies regarding the effects of biochar on pH during composting are
not consistent. This may be related to the characteristics of the biochar
itself and the changes in the mixture during composting that occur
because the properties of biochar produced by different raw materials
Fig. 2. The change of electrical conductivity (a) and the ratio of carbon to nitrogen (b) during the composting process of all treatments. CMB: Chicken manure
biochar, CMMC: Chicken manure integrated microbial consortium. Value are the average of three repeats and error bars indicates the standard deviation.
4
Journal of Hazardous Materials xxx (xxxx) xxxx
are considerably different (Sanchez-Monedero et al., 2018).
3.2. Changes in electrical conductivity and ratio of carbon to nitrogen
during composting
The electrical conductivity (EC) can directly reflect the salt content
of the composting mixture, and to a certain extent, can also determine
whether the final composting products will cause phytotoxicity or in-
hibit plant growth (Zucconi et al., 1981; Bernal et al., 2009). Fig. 2a
shows the dynamic changes in EC. Each treatment showed a similar
trend: a rapid increase at the beginning of composting, a gradual de-
crease from day 14, and stabilization at the end of composting; the
range was 2515–5915 μS·cm−1. At the beginning of composting, with a
rapid increase in temperature, organic materials in the composter were
rapidly degraded by microorganisms producing large quantities of
small molecular-free substances. Decline in moisture content in the
compost caused by high temperatures and aeration resulted in an en-
richment in the concentration water soluble nutrients (Zhang et al.,
2016). Therefore, the EC of each treatment increased rapidly during
composting in the first 14 days. The EC values of all treatments reached
their peaks on the 14th day and were 5730, 5840, 5790, 5710, 5400,
and 5910 μS·cm−1.
The addition of CMB improved the aeration and porosity of the
composter and created a more suitable environment for the propagation
and metabolic activities of microorganisms, thereby accelerating the
OM degradation during composting and causing a rapid increase in the
EC (Chen et al., 2018). As composting progresses, small chain organic
acids and various ions gradually form stable humus under the action of
microorganisms (Bernal et al., 2009). The EC of each treatment gra-
dually decreased and stabilized after the 14th day. At the end of com-
posting, the EC of each treatment (T1–T6) was 3235, 3120, 2980, 2955,
2925, and 2800 μS·cm−1, respectively. The ECs of the treatments
amended with CMB were significantly lower than that of the control,
and the final EC of each treatment decreased with an increase in the
CMB proportion. This may be because the addition of CMB accelerated
compost maturation, and itself absorbed a substantial amount of salt
ions because of its structural characteristics (Chan et al., 2016). In
general, composting products can be safely applied to the soil as or-
ganic fertilizers only when the EC of the products is less than 4000
μS·cm−1. Therefore, all the final composting products in this study met
the standards of application.
The suitable initial ratio of carbon to nitrogen (C/N ratio) is a key
factor to ensure the success of composting. The optimum C/N ratio of
the mixed raw materials is generally considered to be between 25:1 and
35:1. When the C/N ratio is too low, microbial activity is inhibited
owing to insufficient carbon sources. This results in slow and
H. Chen, et al.
incomplete decomposition of mixed materials. When the C/N ratio is
too high, it leads to an insufficient supply of nitrogen, which also limits
microbial metabolism. The C/N ratio is also an important indicator to
measure composting and the maturity of the final products. Fig. 2b
shows the changes in the C/N ratio during CM composting. The C/N
ratio increased in first three days and peaked on the 3rd day, which may
be owing to the loss of nitrogen caused by the large amount of ammonia
volatilization during this period. Subsequently, with the degradation of
OM, the C/N ratio of each treatment gradually decreased until the end
of composting. Finally, the C/N ratio of all treatments reached the
standard for composting products (< 25). As an additive to the chicken
manure compost, CMB is rich in carbon, which causes certain changes
in the C/N ratio of the composting mixture and impacts aerobic com-
posting. However, as most of the carbon in biochar is very stable, its
impact on changes in the C/N ratio are negligible (Zhou et al., 2019).
The RDA showed that the C/N ratio of the composting materials is
positively correlated with the emission of N2O during composting.
3.3. Emissions of ammonia and greenhouse gases during chicken manure
composting
NH3 emissions are the main form of nitrogen loss during composting
and pollute the air environment; these are also responsible for the low
quality of final composting products (Chen et al., 2017a; Chan et al.,
2016).The NH3 emissions of all treatments in this study are shown in
Fig. 3a. The trends of all treatments are basically consistent with those
of traditional aerobic composting. In the initial stage of composting,
with the rapid degradation of OM and a quick increase in temperature,
the emissions of large quantities of NH3 were observed for all treat-
ments (Yang et al., 2015; Jiang et al., 2016a). It is obvious that com-
pared with the treatments amended by CMB and CMCC, the control
(T1) and the treatment only amended by CMCC (T2) had significantly
(p < 0.05) higher NH3 emissions and reached their emission peaks on
Fig. 3. Ammonia (a), nitrous oxide (b), carbon dioxide (c) and methane (d) emission from different treatments during composting. CMB: Chicken manure biochar,
CMMC: Chicken manure integrated microbial consortium.
5
Journal of Hazardous Materials xxx (xxxx) xxxx
the 3rd and 2nd days, respectively. The other treatments (T3–T6)
reached their peaks on days 4–5. The emission peaks of each treatment
(T1–T6) were 2472.11, 2180.37, 1681.91, 1367.46, 1066.72 and
1060.26 mg/d, respectively. After each treatment reached its peak, the
emission rate gradually decreased with further progress in composting
and dropped to zero at the end of composting. However, a secondary
peak was observed on day 9 in some treatments (T1, T3, and T5); the
emission rate then decreased and tended toward zero until the end of
composting. This may be owing to the degradation of some of the or-
ganic materials.
Compared to the control, the NH3 emissions were significantly
lower in the treatments amended by CMB; the higher the CMB pro-
portion, the better the emission reduction effect. Among them, the T6
treatment reduced NH3 by 56.9 %; followed byT5, T4, and T3 -amended
treatments caused 56.8 %, 47.3 %, and 32.8 % NH3 reduction, re-
spectively. The cumulative NH3 emissions (data not shown) of T2–T6
were reduced by 21.8 %, 24.2 %, 37.8 %, 39.3 %, and 41.4 %, as
compared to the control. Chen et al. (2017) and López-Cano et al.
(2016) observed similar results in studies of biochar as additives to
sheep manure and layer manure composting. Related studies indicated
that owing to the characteristics of biochar (such as porosity and high
specific surface area), it can effectively adsorb NH3 and ammonium
ions, thereby reducing NH3 emissions during chicken manure com-
posting (Chan et al., 2016; Li et al., 2015). Anions attached to the
surface of biochar are also beneficial for ammonia adsorption (Awasthi
et al., 2016). In this study, the addition of CMB and CMCC increased the
oxygen uptake rate and promoted the reproductive and metabolic ac-
tivities of microorganisms, which all had a certain inhibitory effect on
NH3 release. The RDA analysis showed that the NH3 emissions had a
significantly (p < 0.05) higher correlation with temperature and C/N
(Fig. 4).
N2O emission is a major form of nitrogen loss during composting
having serious impact on the global atmospheric environment in terms
H. Chen, et al.
Fig. 4. Redundancy analyses of the correlation between the physiochemical properties, greenhouse gases and ammonia emission. CMB: Chicken manure biochar,
CMMC: Chicken manure integrated microbial consortium.
of aggravating the global greenhouse effect (Jiang et al., 2016a). The
emission of N2O during composting is a function of the activity of mi-
croorganisms and involves incomplete nitrification and denitrification.
Owing to the uneven distribution of oxygen inside the compost, ni-
trification on the surface of the compost and denitrification inside the
compost produces N2O. Ammonium and nitrate nitrogen (data not
shown) are substrates for microbial nitrification and denitrification,
and the production and emission of N2O are largely influenced by these
two substrates (Li et al., 2015).
The N2O emission trends of each treatment are shown in Fig. 3b. In
the early and middle stages of composting, the emission of N2O in all
treatments was at a relatively low level. López-Cano et al. (2016) ob-
served similar regulations in pig manure composting and olive-branch
waste composting. This might be attributed to the inhibition of the
activity of nitrifying bacteria due to high temperature and high pH
during this period. In addition, the high concentration of ammonium
ions (data not shown) was also responsible for the low release of N2O in
the early stage of composting (Jiang et al., 2016b). From the 10th day,
the emission rate of N2O gradually increased, and all treatments
reached their emission peaks on the 35th day, which from T1-T6 were
7.00, 6.30, 5.49, 5.67, 5.46, and 5.27 mg/day, respectively. Apparently,
with an increase in the amount of CMB amended to the compost, the
emission peak of each treatment decreased successively, and the cu-
mulative emission of N2O for each treatment also decreased
(p < 0.05). This may be because the addition of CMB promoted de-
nitrification, reduced NO3− to N2, and thereby reduced the production
of intermediate N2O. The large amount of N2O released in the later
stages may be owing to the decrease in the temperature of the heap and
increase in nitrate concentration. A large amount of N2O was generated
in all treatments at the end of the composting, which may be owing to
the decrease in the temperature of the compost and an increase in ni-
trate concentration. Compared to the control, the N2O emissions were
significantly lower in the treatments amended by CMB: the higher the
proportion, the better the emission reduction effect. Among them, the
T6 treatment reduced the NH3 by 27.4 %, CMB at 6 % 4 %, and 2 %
caused NH3 reduction by 22.0 %, 21.5 %, and 19.0 %, respectively. The
cumulative N2O emissions (data not shown) of T2-T6–were reduced by
44.5 %, 21.0 %, 18.2 %, 15.2 %, and 9.0 %, respectively, compared to
6
Journal of Hazardous Materials xxx (xxxx) xxxx
the control. This result is similar to that of a study by Li et al. (2015),
who added 3 % biochar to cow manure and wheat straw and found that
the N2O emissions were reduced by 54.1 % compared to the control. He
et al. (2018) found that the addition of biochar to pig manure compost
effectively reduced the total N2O emissions. Related studies showed
that biochar as an additive could directly or indirectly affect N2O
emissions during composting (Chan et al., 2016), based on the char-
acteristic of the strong adsorption of biochar itself that can reduce the
concentration of NO3−-N during composting. Meanwhile, biochar is
generally alkaline, which can increase the pH of the compost, thus in-
hibiting the production and release of N2O.
The production and emission of CO2 during aerobic composting are
mainly caused by the metabolic activities of the degradation of OM by
microorganisms. Therefore, the emission rate of CO2 can directly reflect
the activity of microorganisms and the degradation and mineralization
rate of OM during composting (He et al., 2018). The CO2 emission
trends for each treatment are shown in Fig. 3c. The dynamic changes for
each treatment are basically similar, rapidly rising and peaking in the
early stage of composting, and then gradually decreasing until the end.
All treatments reached their emission peaks on day 5; the values for
T1–T6 being 29.75, 33.67, 39.44, 44.16, 49.37, and 51.84 g/d, re-
spectively. Compared with the control, the addition of CMB sig-
nificantly (p < 0.05) increased the CO2 emission rate and cumulative
emissions.
This may have occurred because of the porous properties of CMB,
which greatly improved the aeration and optimized the supply and
distribution of oxygen inside the compost. In addition, the large specific
surface area further promoted the metabolism and reproduction of
microorganisms. After the thermophilic period, the intensity of micro-
bial activity gradually decreased. The CO2 emission rates of all treat-
ments evenly decreased and finally stabilized at a very low level at the
end of composting, which also indicated the completion of the process.
It is worth noting that the emission rate of CO2 in the control showed a
rebounding tendency on the 15th day; this phenomenon corresponded
to the dynamic change in the temperature. This might be attributed to
the easily degradable OM in T1 not being completely decomposed at
the early stage; its continuous degradation increased the CO2 emission
rate and temperature on day 15. The above results show that the
H. Chen, et al. Journal of Hazardous Materials xxx (xxxx) xxxx

addition of CMB can effectively promote the metabolic activities of chemical properties such as pH, C/N, and total organic carbon are in-
microorganisms in chicken manure compost and strengthen OM de- dicative of the composting efficiency and the feasibility of promoting
gradation. the application of organic agricultural composts.
CH4 is one of the main greenhouse gases released by aerobic com-
posting and is mainly produced by the deoxidation of CO2/hydrogen
3.5. Mass balance and nutrient content
and acetic acid under anaerobic conditions by methanogens. Therefore,
the emission of CH4 during composting indicates that parts of the
The content of different nutrients and the physicochemical char-
composter are insufficiently supplied with oxygen. As shown in Fig. 3d,
acteristics of the final compost products in this study are listed in
CH4 emissions from all treatments in this study were mainly con-
Table 2. As can be seen from the table, the addition of CMB promoted
centrated in the early stage of composting. This is similar to the results
the degradation of TOM and had a positive effect on the nutrient con-
of research on sludge and pig manure composting by Awasthi et al.
tent. The germination index (GI), EC, C/N, pH, and other physico-
(2017b) and Wang et al. (2013).
chemical indicators all met the maturity standards. In particular, the GI
At the beginning of composting, the CH4 emission rate for each
values of all treatments were greater than 0.8, which is an important
treatment increased rapidly and reached the emission peak on the 2nd
indicator of nontoxicity and harmlessness (Bernal et al., 2009). The
day. This may have occurred because during this period, the degrada-
results showed that the final compost product could be safely applied as
tion of a large amount of OM consumed most of the oxygen in the
organic fertilizer to the soil. Meanwhile, the variation ranges of nu-
compost. This caused a part of the reactor to experience an anaerobic
trients, including TKN, TP, TK, and TNa were 1.14–1.49 %, 0.68–0.94
state, thereby promoting the activity of methanogens. Subsequently, as
%, 1.06–1.43 %, and 2.07–3.14 %, respectively.
the degradation rate of OM gradually decreased, the internal environ-
In this study, the addition of CMB combined with CMMC sig-
ment of the compost also gradually stabilized. The CH4 emission rate
nificantly reduced the total carbon and nitrogen loss from CM compost
for all treatments decreased rapidly and gradually tended to zero at the
(Table 3). More specifically, the higher the content of CMB added, the
end of composting. Compared with the control, CH4 emissions in
lower the carbon and nitrogen loss. Among all treatments, the addition
treatments T2–T6 were reduced by 9.3 %, 27.1 %, 38.2 %, 47.7 % and
of 10 % CMB + 10 % CMMC (T6) was the most effective treatment for
55.9 %, and respectively. The addition of CMB significantly reduced
both carbon and nitrogen fixation in CM composting, and reduced the
CH4 emissions during composting. The results of this study are con-
nitrogen and carbon losses by 17.1 % and 20.9 %, respectively, com-
sistent those of de la Rosa et al. (2014), who indicated that the addition
pared with the control. This was followed by T5 (: 14 % nitrogen loss
of biochar can reduce the activity of methanogens (and thereby CH4
and 15.4 % carbon loss, T4: 11.6 % nitrogen loss and 13.4 % carbon
production) during composting and increase the activity of methane-
loss, and T3: 7.94 % nitrogen loss and 10 % carbon loss. Compared with
oxidizing bacteria (CH4 oxidation).
the control, the addition of CMB and CMMC significantly reduced CH4
emissions; however, CO2 emissions were the main form of carbon loss.
Meanwhile, the release of NH3 accounted for the majority of nitrogen
3.4. Redundancy analysis
loss.
In this study, the correlation between the emissions of NH3 as well
as greenhouse gases and physical and chemical properties was revealed 4. Conclusion
through a redundancy analysis (RDA) (Fig. 4). The results of the RDA
show that the maximum correlation of all parameters was 69.34 % as The addition of CMB and CMCC can accelerate the degradation of
found in T6, followed by T4 (68.28 %), T2 (66.81 %), T5 (65.56 %), T3 CM, reduce the loss of nutritive elements, and decrease the release of
(65.44 %), and T1 (59.35 %). The relatively low correlation observed GHGs and NH3. The treatments co-amended by CMB and CMMC all
for the control may be owing to its low efficiency of OM degradation achieved the standard of compost maturity in advance. Among them,
and degree of humification. The RDA percentage between the emissions the co-addition of 10 % CMB and 10 % CMCC reduced the GHG and
of NH3, CO2, C/N, and temperature could indicate a close relationship NH3 emissions to the highest extent. The RDA showed significant cor-
between the overall gas emissions and maturity of the composting relation between the physiochemical characteristics, GHGs, and NH3
products, and reflect a positive effect on the reduction of gas emissions emissions. Considering the low cost and wide sources of CM, this study
during composting. The research of Awasthi et al. (2016) and Chen showed that CMB can be used as an effective amendment in composting
et al. (2018) showed that gas emissions, temperature, and physical and practices. In particular, 10 % CMB can achieve nitrogen retention,

Table 2
Physicochemical characteristics of composting final products (dry weight basis).
Parameters T1 T2 T3 T4 T5 T6 FAI (FAI TMECC (TMECC (Test Methods for the
(2007)) Examination of Composts and Composting), 2002)
CCME (CCME (2005))

Moisture content 40.6 ± 0.6 40.1 ± 0.2 39.0 ± 0.2 38.5 ± 0.3 37.5 ± 0.5 36.5 ± 0.4 35-55 35-45
(%)
pH 7.85 ± 0.05 7.94 ± 0.03 7.83 ± 0.03 8.05 ± 0.03 8.20 ± 0.02 8.24 ± 0.04 6.5-8.5 5.5-8.5
EC (μS/cm) 3.24 ± 0.04 3.11 ± 0.01 3.02 ± 0.02 3.04 ± 0.02 2.91 ± 0.01 2.86 ± 0.02 2-6 ≥4
TOM (%) 38.2 ± 1.13 35.1 ± 2.14 34.6 ± 1.64 34.4 ± 2.21 32.2 ± 1.03 32.6 ± 1.06 > 30 ≤ 40
TKN (%) 1.21 ± 0.16 1.14 ± 0.04 1.19 ± 0.04 1.24 ± 0.01 1.49 ± 0.14 1.33 ± 0.18 1.0-3.0 –
TP (%) 0.79 ± 0.04 0.94 ± 0.05 0.68 ± 0.03 0.85 ± 0.01 0.78 ± 0.01 0.72 ± 0.02 0.4-1.1 –
TK (%) 1.43 ± 0.27 1.30 ± 0.07 1.16 ± 0.12 1.06 ± 0.09 1.09 ± 0.19 1.41 ± 0.17 0.6-1.7 ≥4
TNa (%) 2.53 ± 0.13 2.07 ± 0.09 3.01 ± 0.21 2.56 ± 0.16 3.14 ± 0.08 2.25 ± 0.06 NA ≥4
C:N ratio 18.3 ± 1.13 17.9 ± 0.97 16.8 ± 2.13 16.0 ± 1.04 12.5 ± 1.14 14.2 ± 0.88 < 25 < 25
GI (%) 0.93 ± 0.05 1.09 ± 0.06 1.11 ± 0.05 1.43 ± 0.04 1.52 ± 0.02 1.71 ± 0.08 ≥ 0.8 ≥ 0.8

T1: 0 % CMB + 0 % CMMC, T2: 0 % CMB + 10 % CMMC, T3: 2 % CMB + 10 % CMMC, T4: 4 % CMB + 10 % CMMC, T5: 6 %CMB + 10 % CMMC, T6: 10 %
CMB + 10 % CMMC. EC - Electrical conductivity, TOM: Total organic matter, TKN - Total kjeldahl nitrogen, TP: Total phosphorus, TNa: Total sodium, TK: Total
potassium, GI: Germination index. Results are the average of three repeats ± standard deviation. FAI: Fertilizer Association of India; TMECC: Test Methods for the
Examination of Composts and Composting; and CCME: Canadian Council of the Ministers of the Environment.

7
H. Chen, et al. Journal of Hazardous Materials xxx (xxxx) xxxx

Table 3
Mass balance of carbon and nitrogen.
Treatments Carbon balance (%) Nitrogen balance (%)

CH4-C Total C losses NH3-N N2O-N Other N losses Total N losses

T1 0.41 55.2 ± 0.32 30.5 2.37 2.31 ± 0.02 35.18 ± 0.24

T2 0.39 52.6 ± 0.25 29.1 2.32 1.44 ± 0.01 32.86 ± 0.25
T3 0.31 45.2 ± 0.19 23.5 2.21 1.53 ± 0.01 27.24 ± 0.19
T4 0.26 41.8 ± 0.20 19.7 2.18 1.74 ± 0.03 23.62 ± 0.21
T5 0.20 39.8 ± 0.18 18.3 2.06 0.82 ± 0.02 21.18 ± 0.14
T6 0.15 34.3 ± 0.15 15.1 1.97 1.01 ± 0.01 18.08 ± 0.16

T1: 0 % CMB + 0 % CMMC, T2: 0 % CMB + 10 % CMMC, T3: 2 % CMB + 10 % CMMC, T4: 4 % CMB + 10 % CMMC, T5: 6 % CMB + 10 % CMMC, T6: 10 %
CMB + 10 % CMMC.

deodorize the compost, as well as improve the quality of the compost.
Declaration of interest statement
There is no conflict of interest in this work.
Acknowledgements
The authors are grateful for the financial support from the Research
Fund for International Young Scientists from the National Natural
Science Foundation of China (Grant No. 31750110469), China; the
Shaanxi Introduced Talent Research Funding (A279021901), China and
the Introduction of Talent Research Start-up Fund (No. Z101021803),
from the College of Natural Resources and Environment, Northwest A&
F University, Yangling, Shaanxi Province 712100, China. We are also
thankful to all our laboratory colleagues and research staff members for
their constructive advice and assistance.
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