Science of the Total Environment 842 (2022) 156957

Contents lists available at ScienceDirect

Science of the Total Environment

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

Mitigating gas emissions from poultry litter composting with waste

vinegar residue
Chunjing Liu a,b,1, Xinxing Zhang a,1, Weitao Zhang c, Shanshan Wang a, Yujing Fan a, Jianzhi Xie a,b,
⁎ ⁎
Wenhua Liao a,b, , Zhiling Gao a,b,
a
College of Resources and Environmental Sciences, Hebei Agricultural University, Baoding, PR China
b
Key Laboratory for Farmland Eco-Environment of Hebei Province, Baoding, PR China
c
General Husbandry Station of Hebei Province, Shijiazhuang 050000, PR China

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

• Suitability of vinegar residue and poultry

litter co-composting was evaluated.
• Amendment of vinegar residue reduced
NH3 and GHG emissions from poultry lit-
ter composting.
• Inhibition on the composting can be alle-
viated by the addition of lime/biochar.
• Waste vinegar residue can be recycled
through co-composting with poultry litter.

A R T I C L E I N F O A B S T R A C T

Editor: Pavlos Kassomenos The composting process is important in the recycling of organic wastes produced in agriculture, food, and municipal
waste management. This study explored the suitability of using waste vinegar residue (WVR) as an amendment in poul-
Keywords: try litter (PL) composting. Four treatments, including poultry litter (CK), poultry litter+vinegar residue (VR), poultry
Vinegar residue
litter+vinegar residue+lime (VR_Ca) and poultry litter+vinegar residue+biochar (VR_B), were conducted. During a
Poultry litter
42-day composting period, the dynamics of carbon dioxide (CO2), ammonia (NH3), nitrous oxide (N2O) and methane
Co-composting
Ammonia
(CH4) emissions, as well as the physicochemical properties and abundances of the bacteria and fungi of the feedstock
Greenhouse gas were tracked to examine the potential barriers in the co-composting of WVR and PL. Compared to those of the CK,
Biochar using a WVR amendment lowered the pH, increased the electrical conductivity significantly at the early stage, resulted
in a strong inhibition of bacterial and fungal growth and delayed the thermophilic period of poultry litter composting
while significantly reducing NH3 and N2O and GHG (CO2-e) emissions. A preadjustment of the WVR with alkaline bio-
char or lime lengthened the thermophilic period and increased the germination index (GI) by alleviating the inhibitory
effect of the WVR on bacterial and fungal growth during composting. However, such preadjustment might reduce the
mitigation effect on NH3. In conclusion, WVR can be recycled through co-composting with poultry litter, and the addi-
tional mitigation of N losses and N conservation can be achieved without halting compost quality.

1. Introduction
⁎ Corresponding authors at: College of Resources and Environmental Sciences, Hebei
Agricultural University, 2596 Lekai south street, Baoding, Hebei 071000, PR China.
E-mail addresses: liaowenhua@hebau.edu.cn (W. Liao), zhilinggao@hebau.edu.cn
Composting is considered to be an important strategy for recycling ani-
(Z. Gao). mal waste due to its various advantages, such as lowering waste density and
1
The first two authors equally contributed to this research. volume (Peng et al., 2015), reducing the environmental impacts of manure-

http://dx.doi.org/10.1016/j.scitotenv.2022.156957
Received 12 April 2022; Received in revised form 28 May 2022; Accepted 21 June 2022
Available online 24 June 2022
0048-9697/© 2022 Published by Elsevier B.V.
C. Liu et al.
borne antimicrobials (e.g., ionophores) and other hazardous substances,
such as noxious odors, toxins and pathogens (Munaretto et al., 2016), and
stabilizing the waste product prior to land application. Nonetheless, great
challenges are associated with this process, e.g., large nitrogen losses (up
to 37 % of the total nitrogen) due to alkaline pH and elevated temperatures
have led to various environmental issues and have impeded the wide appli-
cation of composting (Luo et al., 2014).
Poultry litter has a high N concentration (35.5–50.0 g/kg), low C/N
ratio (7.9–9.8) and high pH (8.7–9.0) as reported by Agyarko-Mintah
et al. (2017), Arikan et al. (2016) and Steiner et al. (2010). The large
amount of N loss through ammonia (NH3 ) during composting
(Kithome et al., 1999; Reece et al., 1979) indicates that it has a reduced
value as an N fertilizer (Tiquia and Tam, 2002) and is hazardous to the
atmospheric environment (Tolvanen et al., 1998; Turan et al., 2007;
Turan et al., 2009; Cao et al., 2020a, 2020b). Strategies to reduce such
N loss, including optimizing the process parameters (aeration rate, turn-
ing frequency, and bulk density) (Wang et al., 2013) and ultilizing addi-
tives (zeolite, biochar, bentonite, and vermiculite) (Agyarko-Mintah
et al., 2017; Cole et al., 2012; He et al., 2018; Janczak et al., 2017;
Steiner et al., 2010) have been investigated. The main mechanisms be-
hind these strategies for alleviating NH3 emissions include the promo-
tion of NH3/NH+ +
4 assimilation, the increase in the NH4 and NH3 ratio
(decreasing the pH), and the immobilization of NH+ 4 (Pan et al., 2018;
Wang and Zeng, 2018).
The amendment of acidic materials, including superphosphate, ni-
tric acid, sulfuric acid, phosphoric acid, and olive pomace, to feedstock
can minimize NH3 emissions by lowering the pH and increasing the
ratio of NH+ 4 and NH3 during composting (Yu and Huang, 2009; Tong
et al., 2019; Cao et al., 2020a, 2020b). For instance, the use of alum
and phosphoric acid can reduce NH3 volatilization from poultry litter
composting by up to 54–76 % and help retain more N in compost
(Delaune et al., 2004; Moore et al., 1996). Meanwhile, the organic
material of lactic acid produced by bacterial fermentation has also been
confirmed to be able to reduce NH3 emissions from composting as an
acidulant by continuously releasing H+ to combine with NH3 in the early
stage of composting (Nie et al., 2020; Chopin, 2010; Hofvendahl and
Hahn-Hgerdal, 2000).
Currently, approximately three million tons of waste vinegar residue
(WVR) — a typical agro-industrial byproduct in the vinegar production
process — is produced per year in China. Potential environmental issues
can be raised because of its acidic quality (a pH value <4) as well as the
fiber, protein, fat, and inorganic salt (Tian et al., 2017) that it contains.
Therefore, realizing the resource utilization of WVR has become a hot
issue in the vinegar brewing industry. Attempts to use windrow-
composting processes (Sun et al., 2017), biogas (Wang et al., 2015; Feng
et al., 2013), substrates for phytase production from Aspergillus ficuum
NTG-23 (Wang et al., 2011), and feed components for laying hens
(Song et al., 2012) have been made. However, incineration, landfilling
and open discharge are still the main practices for WVR management
(Feng et al., 2013).
Thus, it was hypothesized that the application of WVR may have the
potential to reduce NH 3 emissions during poultry litter composting.
However, according to the literature review (Cao et al., 2020a,
2020b), there have been few efforts to explore its suitability as an
acidulant in poultry litter composting to reduce NH3 emissions. It has
been indicated that composting could be halted given an unreasonable
amendment of acidic materials due to the suppression of microorganism
activity once the pH of the compost pile falls below 6 (Wang and Zeng,
2018). Therefore, this study explored the suitability of using WVR as an
amendment in poultry litter composting by tracking the dynamics of gas
emissions, the physicochemical properties and the abundances of bacte-
ria and fungi in compost and examined the potential barriers to poultry
litter composting by modifying the acidity of WVR with alkaline lime
and biochar. This study will be novel and helpful for the simultaneous
achievement of the WVR recycling in agroecosystems and the mitiga-
tion of N loss in manure composting.
2
Science of the Total Environment 842 (2022) 156957
2. Materials and methods
2.1. Experimental design
Poultry litter was collected from a commercial operation of laying hens
in Baoding, China. As shown in Table 1, the pH, total organic carbon (TOC),
total nitrogen (TN) and water content were 7.33, 37.43 %, 2.84 % and 68.6
%, respectively. A sawdust with TOC of 50.03 %, TN 0.11 %, water content
7.7 % was used. The WVR (pH 3.72, TOC 46.84 %, TN 1.38 %, water con-
tent 62.4 %) was produced with solid fermentation, and the solid–liquid
separation of the residue was undertaken to reduce water content prior to
use.
Four treatments were conducted (Table 2), including CK (chicken
litter + sawdust), VR (chicken litter + sawdust + vinegar residue),
VR_Ca (chicken litter + sawdust + vinegar residue + lime) and VR_B
(chicken litter+ sawdust +vinegar residue + biochar), with three repli-
cates. In comparison with CK, the VR treatment demonstrated the impact
on N losses of composting processes, as previous studies indicated that low
pH could halt composting with a lagged temperature increase. The impact
of raising the pH of WVR on gas emissions and composting temperature by
mixing WVR with lime (VR_Ca) or with alkaline biochar (pH 10.23, TOC
30.79 %, TN 0.26 %, water content 4.0 %) (VR_B) were investigated. The
preparation of pH-adjusted WVR was subjected to an ensemble pH of
approximately 7.0. Table 2 showed the compositions of the feedstocks of
4 treatments expressed with ratios (w/w) of the components, with the com-
positions that were pre-examined, similar water contents and C/N ratios for
the feedstocks of all treatments were ensured.
2.2. Composting and gas measurement
A self-designed facility for composting was used, which consisted of a
central control unit, flow-rate regulators, and a stainless composting con-
tainer (Tong et al., 2019). The CO2, NH3, N2O and CH4 concentrations of
the inlet and outlet of the composting container were measured using
Innova 1412i (Lumasense, Denmark), and the concentrations were re-
corded per minute. Sensors were equipped for monitoring temperature
and flow rate through air. In this study, the prepared feedstocks of 17 kg
were loaded in a stainless steel composting container, and they were well
isolated from the ambient surroundings (Fig. 1). During the experiment,
feedstock core temperatures were recorded every hour. Feedstocks were
aerated continuously (~2 L/min), and were manually mixed every 4 days
to collect samples to analyze nutrient contents and water content and to
examine the germination index, DNA extraction and PCR amplification.
2.3. Sample analysis
The water content, pH, EC, total organic carbon (TOC), total N, total am-
monia N (TAN), nitrate and germination index (GI) of the compost samples
at different composting times were analyzed. The water contents of the
samples were measured under oven-dried conditions (105 °C). The pH
and EC values of the samples were determined at a ratio of 1:10 (w/v) for
the sample and distilled water with a pH meter (Starter 3C-Ohaus,
America) (Li et al., 2012). The potassium dichromate volumetric method
for measuring TOC (referring to NY 525–2012 organic fertilizer) was
used. The total N of the samples was determined by digesting them with
H2SO4-H2O2 and then titrating them with diluted H2SO4. The US EPA
method 350.2 was used for measuring TAN. NO− 3 -N was determined by
Table 1
Physical and chemical properties of raw materials for the second composting.
Terms pH TOC(%) TN(%) Water content(%)
Chicken litter 7.33 37.43 2.84 68.6
Vinegar residue 3.72 46.84 1.38 62.4
Sawdust – 50.03 0.11 7.7
Biochar 10.23 30.79 0.26 4.0
C. Liu et al. Science of the Total Environment 842 (2022) 156957

Table 2 2.4. Calculation of gas emission rates

Initial properties of the materials of different treatments.
Treatments Composition(w/w) TOC TN C/N Water content With the CO2, NH3, N2O and CH4 concentrations of the inlet and outlet
(g/kg) (g/kg) (%) of the composting container, the emissions rates at the ith measurement
CK 100a:18b:0c:0d:0e 464.75 18.78 24.7:1 62.0 were calculated using the following equation:
VR 100a:18b:15c:0d:0e 471.09 19.13 24.6:1 63.0
VR_Ca 100a:18b:15c:0.004d:0e 476.29 17.84 26.7:1 63.0
100a:0.3b:15c:0d:33e
ðCoutlet −Cinlet Þ  v  273:15  P
VR_B 608.82 22.49 27.1:1 60.0 Fi ¼ ð1Þ
a
S  ð273:15 þ T Þ  1013:25
Chicken litter.
b
Sawdust.
c
Vinegar residue. where F represents the gas emission rate during measurement (mg/kg/h)
d
Lime. under standard conditions (i.e. 273.15 K and 1213.25 hPa); Coutlet and Cinlet
e
Biochar. represent the concentrations at the inlet and outlet of the composting con-
tainer (mg/m3), respectively; v represents the air flow rate (m3/h) through
the headspace of the composting container; S represents the initial weight
diluting the sample with 2 mol/L KCl solution (1:10, w/v) and measured of feedstock (kg); and P and T represent the actual pressure (hPa) and tem-
with a continuous flow analyzer (SEAL AutoAnalyzer 3, Germany). The ger- perature (°C) of the headspace of the container, respectively.
mination index (GI) of samples was determined by using the same diluted The level of cumulative gas emissions during the composting period was
solution that was used for pH measurement, extracting 5 mL of the diluted calculated using the following equation:
solution into a culture dish with 9 cm filter paper at the bottom, placing 10
cucumber seeds into the culture dish and setting the dish in a 25 °C incuba-
tor for 48 h (Liu et al., 2021). The GI was calculated with the germination X ð F i þ F iþ1 Þ
Q¼  ðt iþ1 −t i Þ ð2Þ
rates of seeds and the root lengths. 2

Fig. 1. Illustration of the composting facility and measurement systems (size not scaled).

3
C. Liu et al.
where Q represents the total gas emissions of interest during the
composting period, Fi represents the gas emission rate at the ith measure-
ment event, and ti represents the time of the ith measurement event.
From the CO2 emissions during composting, it can be seen that only part
of the carbon flow of the feedstock is represented; therefore, it is only
used to distinguish the composting progress of different treatments. In
this case, the total greenhouse gas (GHG) emissions in terms of CO2 equiv-
alents (CO2-e), including the contributions of CH4, N2O and indirect N2O
from NH3 loss during composting, are calculated as follows (IPCC, 2014):
E CO2 eq ¼ 28ECH4 þ 265ðE N2 O þ 0:01E NH3 −N  44=28Þ ð3Þ
where ECO2eq represents the total GHG emissions (g CO2-e kg−1), ECH4 rep-
resents the cumulative emissions of CH4 (g/ kg), EN2O represents the cumu-
lative emissions of N2O (g/ kg), and ENH3−N represents the cumulative
emissions of NH3-N (g/ kg).
2.5. DNA extraction, quantitative polymerase chain reaction (Q-PCR)
Microbial community genomic DNA was extracted from compost sam-
ples using the E.Z.N.A.® soil DNA Kit (Omega Bio-Tek, Norcross, GA, U.S.)
according to the manufacturer's instructions. The DNA extract was checked
on a 1 % agarose gel, and DNA concentration and purity were determined
with a NanoDrop 2000 UV–vis spectrophotometer (Thermo Scientific,
Wilmington, USA). The hypervariable region of the bacterial 16S rRNA
gene, namely V3-V4, was amplified with the primer pairs 338F (5′-ACTC
CTACGGGAGGCAGCAG-3′) and 806R (5′-GGACTACHVGGGTWTCTAAT-
3′) by an ABI GeneAmp® 9700 PCR thermocycler (ABI, CA, USA). The fun-
gal ITS rRNA gene was amplified with the primer pairs ITS1F (5′-CTTGGT
CATTTAGAGGAAGTAA-3′) and ITS2R (5′-GCTGCGTTCTTCATCGATGC-3′).
The PCR amplification of the 16S rRNA gene was performed as follows:
initial denaturation at 95 °C for 5 min, denaturing at 95 °C for 30 s, followed
by 35 cycles of annealing at 58 °C for 30 s and extension at 72 °C for 60 s.
The PCR mixtures contained 4 μL of 5 × TransStart FastPfu buffer, 2 μL
of 2.5 mM dNTPs, 0.8 μL of forward primer (5 μM), 0.8 μL of reverse primer
(5 μM), 0.4 μL of TransStart FastPfu DNA Polymerase, 10 ng of template
DNA, and up to 20 μL of ddH2O. PCRs were performed in triplicate. The
Fig. 2. Temperature (a) and water content (b) during the composting.
4
Science of the Total Environment 842 (2022) 156957
PCR product was extracted from a 2 % agarose gel, purified using the
AxyPrep DNA Gel Extraction Kit (Axygen Biosciences, Union City, CA,
USA) according to the manufacturer's instructions and quantified using a
Quantus™ Fluorometer (Promega, USA). Standard curves were obtained
through serial dilutions of known copy numbers of plasmids containing
16S rRNA gene fragments. Amplification efficiency and correlation coeffi-
cient of the standard curve in a range from 90 to 110 % and above 0.90
were employed.
2.6. Statistical analysis
All data were analyzed using SPSS 17.0 for Windows. One-way ANOVA
in SPSS 17.0 was used to determine the significance of the difference in the
mean values (α = 0.05).
3. Results
3.1. The evolution of temperature during composting
As shown in Fig. 2a, the evolution of temperature in different treatments
varied greatly. For example, the temperature in CK increased quickly to ap-
proximately 60 °C in the first four days, and a similar pattern in VR_Ca treat-
ment was observed; however, the temperature of VR and VR-B increased
slowly and was constantly lower than those of CK and VR_Ca in the first
week. Therefore, the amendment of vinegar residue might have delayed
the composting process at the beginning, but the addition of lime partly re-
duced this delay. However, the addition of biochar did not improve the
composting process when WVR was amended. It was also found that in
the later composting period of Days 18–42, the temperature of the CK
started declining and approached approximately 30 °C, but that the thermo-
philic composting in the treatments with WVR amendment continued for
almost a week, started declining on Day 24 and eventually reached approx-
imately 30 °C. In Fig. 2b, the water content of the composting material de-
clined from approximately 55–60 % at the beginning of the experiment to
38–42 % at the end.
C. Liu et al.
3.2. The dynamics of some chemical indices
Fig. 3 shows the changes in pH, EC and GI of the composting material
during composting. Different behaviors of pH can be observed in Fig. 3a,
where the pH of VR_B and VR_Ca were greater than those of CK and VR, in-
dicating a strong effect of the addition of lime and alkaline biochar. During
the period of Days 7–25, the pH of the CK was consistently greater than
those of the WVR-amended treatments, but they approached a similar
value afterward.
In Fig. 3b, large differences in the EC values of different treatments can
also be seen. In comparison with those of CK, the amendment of WVR
strongly increased the EC values at the beginning, and the addition of bio-
char and lime reduced the EC to some extent, but after Day 17, similar EC
values for all treatments were observed.
In addition, the germination indices of the different treatments are
shown in Fig. 3c. These results indicate that before Day 25, the GI of the
treatments with WVR was much lower than that of the CK; however,
since Day 25, the VR_B and VR_Ca treatments showed greater GI than did
the CK, while the VR and CK treatments showed a similar GI after Day
32. The results showed that the application of biochar or lime improved
the co-composting of poultry manure and WVR.
3.3. The dynamics of gas emissions during composting
Fig. 4a shows the CO2 emissions of different treatments, and it can be
seen that major differences existed. The CO2 emissions of the CK treatment
increased much faster than those of the other treatments, and the maximum
value reached 1600 mg C kg−1 d−1 on Day 9 and declined slowly after-
ward. On the other hand, the CO2 emissions of VR, VR_Ca and VR_B were
a
pH
b
EC (mS cm -1)
c
GI (%)
Time (day)
Fig. 3. Dynamics of pH (a), electrical conductivity (b) and germination index (c) during the composting.
5
Science of the Total Environment 842 (2022) 156957
very low at rates of 150 mg C kg−1 d−1, reached 500 mg C kg−1 d−1 on
Day 4 and then declined very slowly. Overall, constantly lower CO2 emis-
sions from the WVR treatments, especially during the period of days 1–18
were observed. Therefore, the amendment of the WVR reduced the CO2
emissions of poultry litter composting.
In addition, large differences occurred in NH3 emissions among the dif-
ferent treatments (Fig. 4b). For example, the NH3 emissions of the CK, VR-B
and VR-Ca increased much faster than those of the VR, and the significant
emission in the VR started from Day 14. It was also found that the NH3 of
VR_Ca treatment differed from that of VR_B during days 9–17. This result
indicated that the alkalinity of the lime might have neutralized the acids
that were stocked in WVR or generated in the composting process and pro-
moted NH3 production and emission, while the greater buffering capacity
of VR_B in alkalinity had a relatively weak impact on NH3 emissions. Fur-
thermore, in the late period of composting, it was found that WVR treat-
ments, especially VR, showed much stronger NH3 emissions, made a great
contribution to total N losses and required great attention when materials
such as acidic WVR were used for co-composting.
Furthermore, significant but lower N2O emissions occurred (Fig. 4c).
Among the different treatments, the emission rates of CK were consistently
greater than those of the other treatments. Meanwhile, among the treat-
ments using WVR, during the period of Days 2–6, the VR_B treatment had
higher N2O emission rates than those of the other treatments. During
days 7–15, greater emissions were observed in the VR_B and VR_Ca than
in the VR. Meanwhile, the emission rates of the VR treatment were higher
during days 16–42. From the above comparisons, the WVR amendment
showed a strong influence on the N2O emissions from poultry litter
composting, and that adjusting the pH of WVR with biochar and lime also
played an important role in N2O emissions under such conditions.
C. Liu et al.
Fig. 4. CO2-C (a), NH3-N (b), N2O-N (c) and CH4-C (d) emissions during composting.
Methane emissions from composting were observed during days 1–13
(Fig. 4d), during which no significant CH4 emissions in VR_Ca were ob-
served, and the high emission periods in VR_B and VR appeared earlier
than those in CK.
3.4. Dynamics of nutrient values
As shown in Fig. 5a, the TOC of the CK treatment declined similarly to
those of the VR and VR_Ca treatments and was slightly higher than that
of VR_B but reached the lowest value after Day 25. Meanwhile, the total
N of the CK was similar to that of the VR_B treatment but constantly
lower than those of the VR and VR_Ca treatments. In addition, the total
6
Science of the Total Environment 842 (2022) 156957
ammoniacal N of all treatments increased during the first 10 days and
started to decline afterward. During days 15–28, the VR had greater TAN
than the others, but it eventually approached similar values as the others.
As expected, the NO− 3 -N of all treatments increased during composting,
but greater NO− 3 -N contents were observed in the treatments using VR.
Overall, the greater N retention of the WVR treatments demonstrated the
potential for N conservation in the composting of chicken litter.
3.5. Evolution of the microbial community during composting
As shown in Fig. 6a, compared with the CK, the WVR amendment
strongly reduced the abundance of bacteria at the beginning of composting,
C. Liu et al.
a
TN (g kg-1)
TOC (%)
c d
NO3--N (g kg-1)
TAN (g kg-1)
Time (day)
Fig. 5. Dynamics of the feedstocks parameters during the composting period. a, total organic carbon; b, total nitrogen; c, total ammoniacal N; d, NO−
especially during the first 5 days, which corresponds to the low temperature
of the feedstock during the first days as shown in Fig. 2a, indicating a neg-
ative impact on poultry litter composting. The comparable abundance of
bacteria in the VR_B treatment was found to be similar to that in the CK,
whereas the application of lime in combination with VR showed a positive
impact on the abundance of bacteria, which also agreed with the evolution
of composting temperature in Fig. 2a.
Meanwhile, significant differences in the abundance of fungi in the dif-
ferent treatments were observed; the WVR-amended treatment had the
lowest fungal abundance, and the application of biochar with VR moder-
ately increased its fungal abundance, while the application of lime kept
the abundance comparable to the CK despite a faster decline during the
last 10 days. It is inferred that the application of alkaline materials such
as lime or biochar plays an important role in the co-composting of poultry
litter and WVR.
3.6. The evaluation of the co-composting
From Fig. 7a, the total CO2 emissions from VR, VR_B and VR_Ca during
42 days were approximately 51 %, 46 % and 38 % of that in CK, respec-
tively, which shows a significant mitigation effect. In addition, according
to Fig. 4b, a large difference in NH3 emissions between the CK and VR treat-
ments existed especially during the first 20 days, and thus indicating a re-
duction 4–18 % (Fig. 7b). Similarly, strong impacts of the VR treatments
on emissions N2O-N were found and total reductions were 50–58 %
(Fig. 7c); and the CH4-C reduction of 38–80 % from VR and VR_Ca were ob-
served though a CH4-C increase of 45 % from the VR_B was found (Fig. 7d).
In general, the application of WVR or the combination of WVR and bio-
char/lime significantly reduced the CO2, CH4 and NH3 emissions during
the composting period (Fig. 7), except for the increased CH4 emissions
from VR_B. Moreover, it was estimated that the VR, VR_B and VR_Ca re-
duced the total GHG by 45 %, 46 % and 56 %, respectively. Therefore,
7
Science of the Total Environment 842 (2022) 156957
b
Time (day)
3 -N.
using the amendment with WVR has the potential to mitigate N loss
through NH3, N2O emissions as well as the GHG emissions.
3.7. Evaluation of the composting duration
Based on the results in Fig. 3c, the composting process can usually be
considered complete when the GI, according to the standard for organic fer-
tilizers, is constantly over 70 %. Therefore, estimating the N losses and
other gas emissions across the entire composting period could provide bi-
ased suggestions. From this point, the total emissions during composting
were calculated based on two different periods of 28 days and 42 days,
and the relative reductions of the WVR amendment to the CK are shown
in Fig. 7. In general, with the extension of the composting period, the differ-
ences in NH3, N2O, CO2 and CH4 emissions among the different treatments
decreased. For example, the NH3 loss of the VR was 31 % (p < 0.05) lower
than that of the CK in the 28-day period, while it was approximately 11 %
lower when evaluated at 42 days. Similarly, the reduction of CO2, N2O and
CH4 of the VR, in comparison with those of the CK, decreased from 55 %,
56 % and 41 % to 49 %, 50 % and 38 %, respectively. The GHG reductions
of the VR, R_B and VR_Ca were 52 %, 44 % and 55 %, respectively. The
above analysis confirmed that terminating the composting process is very
important for the evaluation of composting technology.
4. Discussions
4.1. The impact on the maturity of co-composting
It was found that the temperature of the feedstock followed a typical
pattern, e.g., the initiated with mesophilic, via thermophilic and eventually
curing phases, which indicated that the bioavailable organic matter was
exhausted; thus, the temperature gradually decreased until the end of the
composting period with the stabilization of the compost. However, the lon-
ger thermophilic period with the amendment of WVR might be partly
C. Liu et al.
Gene copies of bact eria (copi es 1011 g-1)
a
Gene copies of fungi (copi es 108 g-1)
Time (day)
Fig. 6. Evolution of bacterial (a) and fungal (b) abundances of different treatments during the composting.
attributed to the available C sources of the WVR that could be used by mi-
croorganisms to release metabolic heat (Wang et al., 2018; Wu et al., 2015).
In addition, the observed higher EC values of the VR treatments over the
CK treatments might be attributable to the high amount of acids in the WVR
(corresponding to the low pH and NH3 emissions). The addition of Ca or
biochar considerably lowered the EC values compared to those of the CK;
however, the EC of the VR treatment approached the CK after Day 25 and
eventually became lower than the threshold of 4 mS cm−1, which is consid-
ered tolerable by plants of medium sensitivity (Lasaridi et al., 2006; Silva
et al., 2009).
The initial GI values of all the treatments were quite low (Fig. 1c), which
could be attributed to the release of toxic ammonia and the presence vola-
tile fatty acids of low molecular weight (Chen et al., 2010; Jiang et al.,
2016b). At the end of the experiment, the GI values of the VR_B and
VR_Ca treatments were higher than those of the CK (over 80 %, suggested
by (Lasaridi et al., 2006)). The positive role of biochar to the GI might be
partly attributable to the high adsorption to NH+ 4 or NH3 and water-
soluble salts, or to the better stabilization of the composts (Agyarko-
Mintah et al., 2017; Awasthi et al., 2020; Sánchez-García et al., 2015;
Wong et al., 2009). This is similar to the findings of Li et al. (2015) and
Lopez-Cano et al. (2016), who discovered that biochar could improve the
maturation of PL and sheep manure during composting.
4.2. pH of co-composting
During the early stages of composting, the pH value of the CK quickly
rose as temperatures increased. This increase in pH may have resulted
from the production and accumulation of ammonia (Chen et al., 2010;
8
Science of the Total Environment 842 (2022) 156957
Jiang et al., 2016a), but no subsequent decreases in pH occurred due to
the volatilization of NH3 and nitrification-released H+ (Chikae et al.,
2006; Lin, 2008).
In general, the feedstock pH of the VR treatment during the period of
day 1 to 25 was constantly lower than the values in the CK especially. The
low pH (e.g. 5.63–6.89 during day 1 to 16) of the VR treatment were appar-
ently lower than the optimal pH 7.0–8.0 for efficient composting demon-
strated in previous studies (Chan et al., 2016; Ermolaev et al., 2014;
Nakasaki et al., 1993; Szanto et al., 2007; Wong et al., 2009). This is similar
to the decreased pH in food waste composting at the early stage that is due to
the abundance of decomposable material and the subsequent release of or-
ganic acids (Awasthi et al., 2016c; Villasenor et al., 2011; Wong et al.,
1995; Yang et al., 2013). Such acidification of the feedstock may strongly
limit microorganism activity and the activities of amylase, cellulose, prote-
ase and phosphates for the composting because the thermophilic community
does not tolerate acids. (Sundberg et al., 2004; Wang et al., 2016).
To reduce the acidic inhibition of low pH generated during composting,
the introduction of alkaline materials such as NaAc, lime, and biochar
(Yu and Huang, 2009), or pH buffer agents such as K2HPO4/MgSO4 and
KH2PO4/MgSO4 (Li et al., 2013a), may alleviate this situation. However,
the former practice may lead to increased NH3 volatilization, but the latter
results in less NH3 emissions. This study used biochar and lime to adjust the
initial pH values of the compost matrices, which accords with previous
studies by Li et al. (2015) and Awasthi et al. (2016a), who used biochar
to improve nutrient transformation during PM composting.
Moreover, a significant increase in pH values in VR treatments during
the curing phase was found, possibly due to the decomposition of organic
acids and NH3 release from mineralization (Chan et al., 2016; Li et al.,
C. Liu et al.
a b
Relat ive r educti on (%)
c d
Relat ive r educti on (%)
Treatments
Fig. 7. Reductions of CO2 (a), NH3 (b), N2O (c) and CH4 (d) emissions of the VR, VR_B and VR-Ca relative to control.
2015; Wang et al., 2018). The similar pH of all treatments during curing
demonstrated that the addition of vinegar residue had no significant effect
on the final pH compared to that of the CK.
4.3. Impacts on gas emissions
With the comparable maturity of different treatments, the WVR addi-
tion strongly suppressed CO2 emissions (Fig. 6), which might be attributed
to the inhibited microbiological activity (Sundberg et al., 2004; Wang et al.,
2016). Meanwhile, the weak impact of biochar amendments on CO2 was
similar to previous studies, despite a relatively greater bacterial abundance
(Chen et al., 2010; Kim et al., 2016; Xu et al., 2016), whereas the slightly
enhanced mitigation of the VR_Ca treatment could partly be attributed to
CaO implementation that may capture CO2 to produce CaCO3 precipitate
or to the promotion of CO2 fixation by the substantially greater bacterial
abundance as shown in Fig. 6a (Yan et al., 2021).
Of the varied patterns of CH4 emissions from different treatments, the
delayed CH4 emissions from the CK could be derived from greater water
content (Fig. 2) or from the settling of the compost matrix during the
early phase of composting, which led to limited oxygen diffusion and thus
formed a partially anaerobic environment for CH4 emissions (Chowdhury
et al., 2014; Luo et al., 2013; He et al., 2000; Li et al., 2013b). The findings
regarding the increased CH4 emissions from the VR_B treatments during the
initial stages of composting might have been due to lower pH and abundant
acids in the compost substrate may favor methanogenic bacteria (Sánchez-
García et al., 2015; Santos et al., 2016; Yang et al., 2013). It is in line with
the study by Liu et al. (2021), indicating that the application of biochar
could increase CH4 emissions through: (1) shortening the lag phases of H2
and CH4 production, and enhancing volatile fatty acid (VFA) formation in
the H2 phase and VFA degradation in the CH4 phase (Sunyoto et al., 2016)
and (2) lowering the free NH3 that could inhibit methanogenic microorgan-
isms and result in low CH4 production (Chen et al., 2021; Yu et al., 2020);
9
Science of the Total Environment 842 (2022) 156957
Treatments
In this study, N2O emissions mainly occurred during the thermophilic
phase, and this emission pattern is similar to those previously reported by
El Kader et al. (2007) for farm manure composting, by Yang et al. (2013)
for kitchen waste composting, by Maulini-Duran et al. (2014) for OFMSW
composting and by Lopez-Cano et al. (2016) and Wolter et al. (2004) for
PM and olive mill wastes. Meanwhile, the amendment of WVR strongly sup-
pressed bacterial and fungal abundances as shown in Fig. 6 and decreased
the N2O emission substantially compared to the CK. Therefore, the low
abundances of nitrifying and denitrifying microbes (in accordance with
low bacterial and fungal abundances) and the initially low concentrations
of nitrate in all the treatments could be responsible for the low N2O emis-
sions (Awasthi et al., 2016b; Sommer and Møller, 2000). In addition,
slightly less reduction of N2O in the VR_B and VR_Ca compared to VR
(Fig. 7) might be attributable to the alleviated stress on microbial abun-
dance due to the application of lime and biochar.
The initially high NH3 emissions in the CK could have been due to
rapid degradation of organic nitrogen and a higher temperature and pH
(Chan et al., 2016; Li et al., 2015). Amendment with WVR significantly
(p < 0.05) lowered NH3 compared to that of CK, likely because WVR
contained a certain amount of organic acids that could react with ammonium
ions and reduce ammonia production (Chen et al., 2010; Wang et al., 2018).
However, adding biochar to the WVR-amended treatment increased NH3
emissions, which does not agree with many previous studies (Awasthi
et al., 2016a; Awasthi et al., 2016b; Cole et al., 2012; Lopez-Cano et al.,
2016). This might be related to (1) the better porosity of feedstock material
for NH3 transport as bulking agents (Maulini-Duran et al., 2014) and (2) to
the biochar's alkaline property responsible for the increase in feedstock pH
and low NH+ 4 /NH3 ratio (Wang et al., 2013). This result indicated that
these positive factors favoring NH3 emissions may have suppressed the ad-
sorption of NH3 by biochar. In contrast, little effect on NH3 emission was
found when lime was added to the WVR treatment. The similar bulking pH
values (approximately 7.0) of the preadjusted WVR, the different pH values
at the early stage of composting and the different behaviors regarding NH3
C. Liu et al.
emissions could all be due to the evenness of the mixing process, which is de-
rived from the sizes of the biochar and lime particles.
4.4. Implication of the composting of poultry litter with vinegar residue
Previous studies have shown that high water content and strong acidity
can strongly limit the composting of vinegar residue (Awasthi et al., 2016c),
thus a long composting period over 40 days for WVR is needed to reach sta-
bilization with a GI of over 80 %. This agrees with our study that confirmed
a low bacterial abundance during the mesophilic period (Fig. 6). To im-
prove the composting of WVR, special bacteria, such as nitrogen-fixation
bacteria combined with cellulose-decomposing bacteria or the combination
of bacillus acidocaldarius, rhizopus stolonifer and trichoderma viride, are
usually inoculated into the feedstock to improve the temperature of mate-
rials at the initial stage (Zhao et al., 2010; Zhou et al., 2014). Meanwhile,
the high C/N ratio of the WVR often requires other materials with low C/
N, such as rapeseed meal, to be included (Feng et al., 2014).
This study revealed a shortcut that WVR, as an acidic material, may play
an important role in poultry litter composting. It could hold the feedstock
pH at a relatively low level during the first 3 weeks and played an important
role in the mitigation of NH3 losses in comparison with CK. In addition, the
low activity of the bacteria during the first 2 weeks may also play an impor-
tant role in the breakdown of organic N into NH+ 4 . However, as shown in
Fig. 4b, a fast increase in NH3 emission after approximately 12 days
indicated that the inhibitory effect of the residue might vanish with the
decomposition of organic acids. Therefore, employing the potential of
vinegar residue via co-composting with low C/N ratio material such as
poultry litter might be a good strategy to achieve the aforementioned
double targets.
Furthermore, the preadjustment of WVR with lime can largely alleviate
the inhibitory effect of VR on composting. According to this study, a 10 %
ratio (W/W) of WVR with a pH of 7.0 (adjusted with lime) to poultry litter
seems to be appropriate for the reduction of N losses and the recycling of
vinegar residue. However, the enhancement of N losses during later
composting should be considered when using WVR as an additive of co-
composting.
5. Conclusions
This study evaluated the effect of vinegar residue amendments on chicken
litter composting and nitrogenous and greenhouse gas emissions. The co-
composting of vinegar residue and poultry litter delayed the thermophilic
phase of composting mainly due to the strong inhibition of bacterial and fun-
gal growth caused by lowered pH and increased EC at the early stage. How-
ever, this is beneficial, showing significant reductions in nitrogen losses
through NH3 and N2O by 31 % and 45 %, respectively, and GHG (CO2-e) re-
duction by 52 %. The preadjustment of the WVR with alkaline biochar or
lime played a positive role in the composting duration and germination
index by reducing the inhibitory effect of the WVR on the bacterial and fungal
growth during composting. However, a potential adverse effect is reduced
NH3 mitigation from 31 % to 3–20 %. In conclusion, WVR can be recycled
through co-composting with poultry litter with the additional mitigation of
N losses and N conservation without halting compost quality.
Declaration of competing interest
The authors declare that they have no known competing financial inter-
ests or personal relationships that could have appeared to influence the
work reported in this paper.
Acknowledgement
This research was financially supported by the Key Research and
Development Program of Hebei Province (21327303D and 20327306D),
and National Natural Science Foundation of China (NSFC: Grant nos.
41675151).
10
Science of the Total Environment 842 (2022) 156957
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://doi.
org/10.1016/j.scitotenv.2022.156957.
References
Agyarko-Mintah, E., Cowie, A., Zwieten, L.V., Singh, B.P., Smillie, R., Harden, S., Fornasier,
F., 2017. Biochar lowers ammonia emission and improves nitrogen retention in poultry
litter composting. Waste Manag. 61, 129–137. https://doi.org/10.1016/j.wasman.
2016.12.009.
Arikan, O.A., Mulbry, W., Rice, C., 2016. The effect of composting on the persistence of four
ionophores in dairy manure and poultry litter. Waste Manag. 54, 110–117. https://doi.
org/10.1016/j.wasman.2016.04.032.
Awasthi, M.K., Wang, M., Chen, H., Wang, Q., Zhao, J., Ren, X., Li, D., Awasthi, S.K., Shen, F.,
Li, R., Zhang, Z., 2016a. Heterogeneity of biochar amendment to improve the carbon and
nitrogen sequestration through reduce the greenhouse gases emissions during sewage
sludge composting. Bioresour. Technol. 224, 428–438. https://doi.org/10.1016/j.
biortech.2016.11.014.
Awasthi, M.K., Wang, Q., Huang, H., Li, R., Shen, F., Lahori, A.H., Wang, P., Guo, D., Guo, Z.,
Jiang, S., Zhang, Z., 2016b. Effect of biochar amendment on greenhouse gas emission and
bio-availability of heavy metals during sewage sludge co-composting. J. Clean. Prod. 135
(nov.1), 829–835. https://doi.org/10.1016/j.jclepro.2016.07.008.
Awasthi, M.K., Wang, Q., Huang, H., Ren, X., Lahori, A.H., Mahar, A., Ali, A., Shen, F., Li, R.,
Zhang, Z., 2016c. Influence of zeolite and lime as additives on greenhouse gas emissions
and maturity evolution during sewage sludge composting. Bioresour. Technol. 216,
172–181. https://doi.org/10.1016/j.biortech.2016.05.065.
Awasthi, M.K., Duan, Y., Awasthi, S.K., Liu, T., Zhang, Z., 2020. Influence of bamboo biochar
on mitigating greenhouse gas emissions and nitrogen loss during poultry manure
composting. Bioresour. Technol. 303, 122952. https://doi.org/10.1016/j.biortech.
2020.122952.
Cao, Y., Hu, H., Guo, H., Butterly, C., Bai, M., Zhang, Y., Chen, D., He, J., 2020. Lignite as ad-
ditives accelerates the removal of antibiotic resistance genes during poultry litter
composting. Bioresour. Technol. 315. https://doi.org/10.1016/j.biortech.2020.123841.
Cao, Y., Wang, X., Liu, L., Velthof, G.L., Misselbrook, T., Bai, Z., Ma, L., 2020. Acidification of
manure reduces gaseous emissions and nutrient losses from subsequent composting pro-
cess. J. Environ. Manag. 264, 110454. https://doi.org/10.1016/j.jenvman.2020.110454.
Chan, M.T., Selvam, A., Wong, J.W.C., 2016. Reducing nitrogen loss and salinity during
‘struvite’ food waste composting by zeolite amendment. Bioresour. Technol. 200,
838–844. https://doi.org/10.1016/j.biortech.2015.10.093.
Chen, Y.X., Huang, X., Han, Z., Huang, X., Hu, B., Shi, D., Wu, W., 2010. Effects of bamboo
charcoal and bamboo vinegar on nitrogen conservation and heavy metals immobility dur-
ing pig manure composting. Chemosphere 78 (9), 1177–1181. https://doi.org/10.1016/
j.chemosphere.2009.12.029.
Chen, M., Liu, S., Yuan, X., Li, Q.X., Wang, F., Xin, F., Wen, B., 2021. Methane production and
characteristics of the microbial community in the co-digestion of potato pulp waste and
dairy manure amended with biochar. Renew. Energy 163, 357–367. https://doi.org/
10.1016/j.renene.2020.09.006.
Chikae, M., Ikeda, R., Kerman, K., Morita, Y., Tamiya, E., 2006. Estimation of maturity of com-
post from food wastes and agro-residues by multiple regression analysis. Bioresour.
Technol. 97 (16), 1979–1985. https://doi.org/10.1016/j.biortech.2005.09.026.
Chopin, A., 2010. Organization and regulation of genes for amino acid biosynthesis in lactic
acid bacteria. FEMS Microbiol. Rev. 12 (1–3), 21–37. https://doi.org/10.1016/0168-
6445(93)90056-F.
Chowdhury, M.A., Neergaard, A.D., Jensen, L.S., 2014. Potential of aeration flow
rate and bio-char addition to reduce greenhouse gas and ammonia emissions
during manure composting. Chemosphere 97, 16–25. https://doi.org/10.1016/j.
chemosphere.2013.10.030.
Cole, D.P., Smith, E.A., Lee, Y.J., 2012. High-resolution mass spectrometric characterization of
molecules on biochar from pyrolysis and gasification of switchgrass. Energ. Fuel. 26 (6),
3803–3809. https://doi.org/10.31274/etd-180810-3894.
Delaune, P.B., Moore, P.A., Daniel, T.C., Lemunyon, J.L., 2004. Effect of chemical and micro-
bial amendments on ammonia volatilization from composting poultry litter. J. Environ.
Qual. 33 (2), 728–734 PMID: 15074826.
El Kader, N.A., Robin, P., Paillat, J.M., Leterme, P., 2007. Turning, compacting and the addition
of water as factors affecting gaseous emissions in farm manure composting. Bioresour.
Technol. 98 (14), 2619–2628. https://doi.org/10.1016/j.biortech.2006.07.035.
Ermolaev, E., Sundberg, C., Pell, M., Jönsson, H., 2014. Greenhouse gas emissions from home
composting in practice. Bioresour. Technol. 151, 174–182. https://doi.org/10.1016/j.
biortech.2013.10.049.
Feng, L., Li, Y., Chen, C., Liu, X., Xiao, X., Ma, X., Zhang, R., He, Y., Liu, G., 2013. Biochemical
methane potential (BMP) of vinegar residue and the influence of feed to inoculum ratios
on biogas production. Bioresources 8 (2), 2487–2498. https://doi.org/10.15376/biores.
8.2.2487-2498.
Feng, R.Z., Wei, Q., Zhou, W.H., Wang, T., Yang-Bo, L.I., 2014. Study on the vinegar dregs
compost with high temperature. Food Ferment. Ind. 40 (6), 81–84. https://doi.org/10.
13995/j.cnki.11-1802/ts.2014.06.041.
He, Y.W., Inamori, Y., Mizuochi, M., Kong, H., Iwami, N., Sun, T., 2000. Measurements of
N2O and CH4 from the aerated composting of food waste. Sci. Total Environ. 254 (1),
65–74. https://doi.org/10.1016/S0048-9697(00)00439-3.
He, Z.H., Lin, H., Hao, J., Kong, X., Tian, K., Bei, Z., Tian, X., 2018. Impact of vermiculite on
ammonia emissions and organic matter decomposition of food waste during composting.
Bioresour. Technol. 263, 548–554. https://doi.org/10.1016/j.biortech.2018.05.031.
C. Liu et al.
Hofvendahl, K., Hahn-Hgerdal, B., 2000. Factors affecting the fermentative lactic acid produc-
tion from renewable resources 1. EnzymeMicrob. Technol. 26 (2–4), 87–107. https://doi.
org/10.1016/S0141-0229(99)00155-6.
IPCC, 2014. In: Pachauri, R.K., Meyer, L.A. (Eds.), Climate Change 2014: Synthesis Report.
Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Inter-
governmental Panel on Climate Change. IPCC, Geneva, Switzerland 151 pp.
Janczak, D., Malińska, K., Czekała, W., Cáceres, R., Lewicki, A., Dach, J., 2017. Biochar to reduce
ammonia emissions in gaseous and liquid phase during composting of poultry manure with
wheat straw. Waste Manag. 66, 36–45. https://doi.org/10.1016/j.wasman.2017.04.033.
Jiang, T., Ma, X., Tang, Q., Yang, J., Schuchardt, F., 2016a. Combined use of nitrification in-
hibitor and struvite crystallization to reduce the NH3 and N2O emissions during
composting. Bioresour. Technol. 217, 210–218. https://doi.org/10.1016/j.biortech.
2016.01.089.
Jiang, T., Ma, X., Yang, J., Tang, Q., Yi, Z., Chen, M., Li, G., 2016b. Effect of different struvite
crystallization methods on gaseous emission and the comprehensive comparison during
the composting. Bioresour. Technol. 217, 219–226. https://doi.org/10.1016/j.biortech.
2016.02.046.
Kim, E., Lim, K., Lee, T., Ha, K., Han, D., Nam, J., Choi, N., Cho, I., Yip, A.C.K., Choi, J.,
2016. Mono-dispersed DDR zeolite particles by seeded growth and their CO2, N2,
and H2O adsorption properties. Chem. Eng. J. 306, 876–888. https://doi.org/10.
1016/j.cej.2016.08.025.
Kithome, M., Paul, J.W., Bomke, A.A., 1999. Reducing nitrogen losses during simulated
composting of poultry manure using adsorbents or chemical amendments. J. Environ.
Qual. 28 (1), 194–201. https://doi.org/10.2134/jeq1999.00472425002800010023x.
Lasaridi, K., Protopapa, I., Kotsou, M., Pilidis, G., Manios, T., Kyriacou, A., 2006. Quality as-
sessment of composts in the Greek market: the need for standards and quality assurance.
J. Environ. Manag. 80 (1), 58–65. https://doi.org/10.1016/j.jenvman.2005.08.011.
Li, R.H., Wang, J.J., Zhang, Z., Shen, F., Zhang, G., Qin, R., Li, X., Xiao, R., 2012. Nutrient
transformations during composting of pig manure with bentonite. Bioresour. Technol.
121, 362–368. https://doi.org/10.1016/j.biortech.2012.06.065.
Li, S., Huang, G.H., An, C.J., Yu, H., 2013a. Effect of different buffer agents on in-vessel
composting of food waste: performance analysis and comparative study. J. Environ. Sci.
Health A 48 (7), 772–780. https://doi.org/10.1080/10934529.2013.744637.
Li, Y.B., Li, W.G., Wu, C.D., Wang, K., 2013b. New insights into the interactions between car-
bon dioxide and ammonia emissions during sewage sludge composting. Bioresour.
Technol. 136, 385–393. https://doi.org/10.1016/j.biortech.2013.03.061.
Li, R., Wang, Q., Zhang, Z., Zhang, G., Li, Z., Wang, L., Zheng, J., 2015. Nutrient transformation
during aerobic composting of pig manure with biochar prepared at different temperatures.
Environ. Technol. 36 (5–8), 815–826. https://doi.org/10.1080/09593330.2014.963692.
Lin, C., 2008. A negative-pressure aeration system for composting food wastes. Bioresour.
Technol. 99 (16), 7651–7656. https://doi.org/10.1016/j.biortech.2008.01.078.
Liu, M.L., Liu, C., Liao, W., Xie, X., Zhang, X., Gao, Z., 2021. Impact of biochar application on
gas emissions from liquid pig manure storage. Sci. Total Environ. 771, 145454. https://
doi.org/10.1016/j.scitotenv.2021.145454.
Lopez-Cano, I., Roig, A., Cayuela, M.L., Alburquerque, J.A., Sanchez-Monedero, M.A., 2016.
Biochar improves N cycling during composting of olive mill wastes and sheep manure.
Waste Manag. 49, 553–559. https://doi.org/10.1016/j.wasman.2015.12.031.
Luo, Y., Li, G., Luo, W., Schuchardt, F., Jiang, T., Xu, D., 2013. Effect of phosphogypsum and
dicyandiamide as additives on NH3, N2O and CH4 emissions during composting.
J. Environ. Sci. 25 (7), 1338–1345. https://doi.org/10.1016/S1001-0742(12)60126-0.
Luo, W.H., Yuan, J., Luo, Y., Li, G., Nghiem, L.D., Price, W.E., 2014. Effects of mixing and cov-
ering with mature compost on gaseous emissions during composting. Chemosphere 117,
14–19. https://doi.org/10.1016/j.chemosphere.2014.05.043.
Maulini-Duran, C., Artola, A., Font, X., Sanchez, A., 2014. Gaseous emissions in municipal
wastes composting: effect of the bulking agent. Bioresour. Technol. 172, 260–268.
https://doi.org/10.1016/j.biortech.2014.09.041.
Moore, P.A., Daniel, T.C., Edwards, D.R., Miller, D.M., 1996. Evaluation of chemical amend-
ments to reduce ammonia volatilization from poultry litter. Poult. Sci. 75 (3), 315–320.
https://doi.org/10.3382/ps.0750315.
Munaretto, J.S., Yonkos, L., Aga, D.S., 2016. Transformation of ionophore antimicrobials in
poultry litter during pilot-scale composting. Environ. Pollut. 212, 392–400. https://doi.
org/10.1016/j.envpol.2016.01.066.
Nakasaki, K., Yaguchi, H., Sasaki, Y., Kubota, H., 1993. Effects of pH control on composting of
garbage. Waste Manage. Res. 11 (2), 117–125. https://doi.org/10.1006/wmre.1993.1013.
Nie, E.R., Gao, D., Zheng, G.D., 2020. Effects of lactic acid on modulating the ammonia emis-
sions in co-composts of poultry litter with slaughter sludge. Bioresour. Technol. 315,
123812. https://doi.org/10.1016/j.biortech.2020.123812.
Pan, J.T., Cai, H., Zhang, Z., Liu, H., Li, R., Mao, H., Awasthi, M.K., Wang, Q., Zhai, L., 2018.
Comparative evaluation of the use of acidic additives on sewage sludge composting qual-
ity improvement, nitrogen conservation, and greenhouse gas reduction. Bioresour.
Technol. 270, 467–475. https://doi.org/10.1016/j.biortech.2018.09.050.
Peng, S., Wang, Y., Zhou, B., Lin, X., 2015. Long-term application of fresh and composted ma-
nure increase tetracycline resistance in the arable soil of eastern China. Sci. Total Environ.
506–507, 279–286. https://doi.org/10.1016/j.scitotenv.2014.11.010.
Reece, F.N., Bates, B.J., Lott, B.D., 1979. Ammonia control in broiler houses. Poultry Sci. 58
(3), 754–755. https://doi.org/10.3382/ps.0580754.
Sánchez-García, M., Alburquerque, J.A., Sánchez-Monedero, M.A., Roig, A., Cayuela, M.L.,
2015. Biochar accelerates organic matter degradation and enhances N mineralisation
during composting of poultry manure without a relevant impact on gas emissions.
Bioresour. Technol. 192, 272–279. https://doi.org/10.1016/j.biortech.2015.05.003.
Santos, A., Bustamante, M.A., Tortosa, G., Moral, R., Bernal, M.P., 2016. Gaseous emissions and
process development during composting of pig slurry: the influence of the proportion of cot-
ton gin waste. J. Clean. Prod. 112, 81–90. https://doi.org/10.1016/j.jclepro.2015.08.084.
Silva, M.E., Lemos, L.T., Cunha-Queda, A.C., Nunes, O.C., 2009. Co-composting of poultry ma-
nure with low quantities of carbon-rich materials. Waste Manag. Res. 27 (2), 119–128.
https://doi.org/10.1177/0734242X08096693.
11
Science of the Total Environment 842 (2022) 156957
Sommer, S.G., Møller, H.B., 2000. Emission of greenhouse gases during composting of deep
litter from pig production – effect of straw content. J. Agric. Sci. 134 (3), 327–335.
https://doi.org/10.1017/S0021859699007625.
Song, Z.T., Dong, X.F., Tong, J.M., Wang, Z.H., 2012. Effects of waste vinegar residue on nu-
trient digestibility and nitrogen balance in laying hens. Livestock Sci. 150 (1–3), 67–73.
https://doi.org/10.1016/j.livsci.2012.08.004.
Steiner, C., Das, K.C., Melear, N., Lakly, D., 2010. Reducing nitrogen loss during poultry litter
composting using biochar. J. Environ. Qual. 39 (4), 1236–1242. https://doi.org/10.
2134/jeq2009.0337.
Sun, D., Zhao, Q., Tian, X., 2017. Study on the suitable condition of vinegar residue windrow-
composting. Agri Tech Equip. 335 (11), 4–9. https://doi.org/10.3969/j.issn.1673- 887X.
2017.11.001.
Sundberg, C., Smars, S., Jonsson, H., 2004. Low pH as an inhibiting factor in the transition
from mesophilic to thermophilic phase in composting. Bioresour. Technol. 95 (2),
145–150. https://doi.org/10.1016/j.biortech.2004.01.016.
Sunyoto, N.M., Zhu, M., Zhang, Z., Zhang, D., 2016. Effect of biochar addition on hydrogen
and methane production in two-phase anaerobic digestion of aqueous carbohydrates
food waste. Bioresour. Technol. 219, 29–36. https://doi.org/10.1016/j.biortech.2016.
07.089.
Szanto, G.L., Hamelers, H.V.M., Rulkens, W.H., Veeken, A.H.M., 2007. NH3, N2O and CH4
emissions during passively aerated composting of straw-rich pig manure. Bioresour.
Technol. 98 (14), 2659–2670. https://doi.org/10.1016/j.biortech.2006.09.021.
Tian, B., Zhao, S., Zhang, J., Yongjian, Y.U., 2017. Research advance on utilization of vinegar
residue. China Brew. 36 (3), 1–4. https://doi.org/10.11882/j.issn.0254-5071.2017.03.
001.
Tiquia, S.M., Tam, N., 2002. Characterization and composting of poultry litter in forced-
aeration piles. Process Biochem. 37 (8), 869–880. https://doi.org/10.1016/S0032-9592
(01)00274-6.
Tolvanen, O.K., Hanninen, K.I., Veijanen, A., Villberg, K., 1998. Occupational hygiene in
biowaste composting. Waste Manage. Res. 16 (6), 525–540. https://doi.org/10.1177/
0734242X9801600604.
Tong, B.X., Wang, X., Wang, S.Q., Ma, L., Ma, W.Q., 2019. Transformation of nitrogen and car-
bon during composting of manure litter with different methods. Bioresour. Technol. 293,
122046. https://doi.org/10.1016/j.biortech.2019.122046.
Turan, N.G., Akdemir, A., Ergun, O.N., 2007. Emission of volatile organic compounds during
composting of poultry litter. Water Air Soil Pollut. 184 (1–4), 177–182. https://doi.org/
10.1007/s11270-007-9406-0.
Turan, N.G., Akdemir, A., Ergun, O.N., 2009. Removal of volatile organic compounds by nat-
ural materials during composting of poultry litter. Bioresour. Technol. 100 (2), 798–803.
https://doi.org/10.1016/j.biortech.2008.07.010.
Villasenor, J., Rodriguez, L., Fernandez, F.J., 2011. Composting domestic sewage sludge with
natural zeolites in a rotary drum reactor. Bioresour. Technol. 102 (2), 1447–1454.
https://doi.org/10.1016/j.biortech.2010.09.085.
Wang, S.G., Zeng, Y., 2018. Ammonia emission mitigation in food waste composting: a re-
view. Bioresour. Technol. 248, 13–19. https://doi.org/10.1016/j.biortech.2017.07.050.
Wang, Z.H., Dong, X., Zhang, G., Tong, J., Zhang, Q., Xu, S., 2011. Waste vinegar residue as
substrate for phytase production. Waste Manage. Res. 29 (12), 1262–1270. https://doi.
org/10.1177/0734242X11398521.
Wang, C., Lu, H., Dong, D., Deng, H., Strong, P.J., Wang, H., Wu, W., 2013. Insight into the
effects of biochar on manure composting: evidence supporting the relationship between
N2O emission and denitrifying community. Environ. Sci. Technol. 47 (13), 7341–7349.
https://doi.org/10.1021/es305293h.
Wang, Z.B., Shao, S., Zhang, C., Lu, D., Ma, H., Ren, X., 2015. Pretreatment of vinegar residue
and anaerobic sludge for enhanced hydrogen and methane production in the two-stage
anaerobic system. Int. J. Hydrogen Energy 40 (13), 4494–4501. https://doi.org/10.
1016/j.ijhydene.2015.02.029.
Wang, Q., Wang, Z., Awasthi, M.K., Jiang, Y., Li, R., Ren, X., Zhao, J., Shen, F., Wang, M.,
Zhang, Z., 2016. Evaluation of medical stone amendment for the reduction of nitrogen
loss and bioavailability of heavy metals during pig manure composting. Bioresour.
Technol. 220, 297–304. https://doi.org/10.1016/j.biortech.2016.08.081.
Wang, Q., Awasthi, M.K., Ren, X., Zhao, J., Li, R., Wang, Z., Wang, M., Chen, H., Zhang, Z.,
2018. Combining biochar, zeolite and wood vinegar for composting of pig manure: the
effect on greenhouse gas emission and nitrogen conservation. Waste Manag. 74,
221–230. https://doi.org/10.1016/j.wasman.2018.01.015.
Wolter, M., Prayitno, S., Schuchardt, F., 2004. Greenhouse gas emission during storage of pig
manure on a pilot scale. Bioresour. Technol. 95 (3), 235–244. https://doi.org/10.1016/j.
biortech.2003.01.003.
Wong, J.W.C., Li, S.W.Y., Wong, M.H., 1995. Coal fly-ash as a composting material for
sewage-sludge: effects on microbial activities. Environ. Technol. 16 (6), 527–537.
https://doi.org/10.1080/09593331608616294.
Wong, J.W.C., Fung, S.O., Selvam, A., 2009. Coal fly ash and lime addition enhances the rate
and efficiency of decomposition of food waste during composting. Bioresour. Technol.
100 (13), 3324–3331. https://doi.org/10.1016/j.biortech.2009.01.063.
Wu, Q., Zhang, S., Hou, B., Zheng, H., Deng, W., 2015. Study on the preparation of wood vin-
egar from biomass residues by carbonization process. Bioresour. Technol. https://doi.
org/10.1016/j.biortech.2014.12.026.
Xu, X., Kan, Y., Zhao, L., Cao, X., 2016. Chemical transformation of CO2 during its capture by
waste biomass derived biochars. Environ. Pollut. 213, 533–540. https://doi.org/10.
1016/j.envpol.2016.03.013.
Yan, H., Niu, Q., Zhu, Q., Wang, S., Meng, Q., Li, G., Li, X., Ma, C., Li, Q., 2021. Biochar rein-
forced the populations of cbbL-containing autotrophic microbes and humic substance for-
mation via sequestrating CO2 in composting process. J. Biotechnol. 333, 39–48. https://
doi.org/10.1016/j.jbiotec.2021.04.011.
Yang, F., Li, G.X., Yang, Q.Y., Luo, W.H., 2013. Effect of bulking agents on maturity and gas-
eous emissions during kitchen waste composting. Chemosphere 93 (7), 1393–1399.
https://doi.org/10.1016/j.chemosphere.2013.07.002.
C. Liu et al.
Yu, H., Huang, G.H., 2009. Effects of sodium acetate as a pH control amendment on the
composting of food waste. Bioresour. Technol. 100 (6), 2005–2011. https://doi.org/10.
1016/j.biortech.2008.10.007.
Yu, Q., Sun, C., Liu, R.H., Yellezuome, D., Zhu, X.P., Bai, R.F., Liu, M.Q., Sun, M.Z., 2020.
Anaerobic co-digestion of corn stover and chickenmanure using continuous stirred tank
reactor: the effect of biochar addition and urea pretreatment. Bioresour. Technol. 319,
124197. https://doi.org/10.1016/j.biortech.2020.124197.
12
Science of the Total Environment 842 (2022) 156957
Zhao, Q., Li, P., Wang, J., Zhu, Y., Sun, D., 2010. Technology and effect of vinegar residue
windrow composting. Trans. CSAE 26 (7), 255–259. https://doi.org/10.3969/j.issn.
1002-6819.2010.07.044.
Zhou, W.H., Wei, Q., Wang, T., Feng, R., Du, Y., Pang, J., 2014. Effect of inoculating microbes
on composting of vinegar dregs. FoodFerment.Ind. 40 (10), 11–15. https://doi.org/10.
13995/j.cnki.11-1802/ts.2014.10.047.