Bioresource Technology 283 (2019) 340–349

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Bioresource Technology
journal homepage: www.elsevier.com/locate/biortech

Effect of bamboo hydrochar on anaerobic digestion of fish processing waste T

for biogas production
⁎
Ungyong Choea,b, Ahmed M. Mustafaa,c, Hongjian Lina, Jie Xua, Kuichuan Shenga,
a
College of Biosystems Engineering and Food Science, Zhejiang University, Hangzhou 310058, China
b
Faculty of Environmental Science, University of Science, Yusheng Scientist Road, Unjong District, Pyongyang 00850, Democratic People's Republic of Korea
c
Department of Agricultural Engineering, Faculty of Agriculture, Suez Canal University, Ismailia 41522, Egypt

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

Keywords: The effect of hydrothermal carbonization (HTC) temperature and bamboo hydrochar (BHC) addition on biogas
Bamboo hydrochar production in anaerobic digestion of fish processing waste (FPW) was studied. HTC temperature (200–280 °C)
Fish processing waste (FWP) had significant effects on methane yield and content, but the BHC had little effects. The maximum biogas yield
Biogas production observed with HTC at 200 °C and a BHC adding ratio of 1:2 (dry mass ratio of FPW to BHC) reached 292 L/kg
Ammonium nitrogen inhibition
volatile solids (VS), which were 64% higher than the control group with only FPW, with the maximum methane
COD decreasing
Methane content
yield of 219 L/kg-VS and highest net methane energy yield of 3410 kJ/kg-VS. The obtained results can be used to
design an efficient anaerobic digestion process for treating and effectively utilizing fish processing waste.

1. Introduction Hydrochar is a carbonaceous solid absorbent generated from hy-

China had a total fisheries production of 49.2 million tons in 2016,
which was about 62% of the global inland fishery production (FAO,
2018). Fish processing waste (FPW) is the major by-product of fish
processing, which represents more than 10% by weight of fish (Xu
et al., 2016), which means more than 4.9 million tons of fish processing
waste was generated in 2016. Traditionally, FPW is disposed of by
landfills and incineration, but those disposal methods are expensive and
cause some environmental problems. Landfills pollute groundwater by
leachate and occupy potentially arable land, while incineration emits
greenhouse gases and toxic gases (Kiran & Liu, 2015; Ren et al., 2018).
Anaerobic digestion of FPW can transform the organic substrate into
biogas, which will decrease the problems of using landfills and in-
cineration plants and produce clean energy (Xu et al., 2016). FPW
consists of various organic matter such as gill, internal organs, bone,
back fin, tail fin. Some compositions in FPW, such as lipids from fish
fats and insoluble proteins limit the anaerobic digestion and even cause
process failure of anaerobic digestion (Xia et al., 2016), because high
lipid content can inhibit the metabolism of microbial cells via the ab-
sorption of lipid derivatives (i.e., long-chain fatty acids) on cell sur-
faces, and the high nitrogen concentration of FPW can create ammonia
inhibition. Accordingly, FPW is regularly combined with other sub-
strates to reduce inhibitor concentration or improve the biogas gen-
eration (Xu et al., 2016).
drothermal carbonization (HTC) of biomass, e.g., bamboo processing
residues (Libra et al., 2011). Adding hydrochar to AD digesters raises
buffering capacity, immobilizes microbial cell, holds nutrients and
improve biogas production (Xu et al., 2018). A batch mesophile fer-
mentation experiment was carried out in 100 mL syringes found that
hydrochar addition increased the methane yield by 32% (Mumme et al.,
2014). Reza et al. (2015) found that magnetic hydrochar improved
anaerobic biofilm growth and increased biogas yield (Mumme et al.,
2014). The similar beneficial effect was identified for biochar addition
in anaerobic digestion (Fagbohungbe et al., 2016). Another improve-
ment made by biochar addition was that the addition of remediated
ammonia and fatty acids inhibition and therefore improved methane
production rate (Lü et al., 2016).
FPW is rich in protein and fats and therefore may pose substantial
inhibition to methane production in AD. However, the research of hy-
drochar addition in AD of FPW is not well documented. The objectives
of this study were therefore to (1) investigate the effect of HTC tem-
perature and BHC adding ratio on the biogas and methane yield of fish
waste; (2) evaluate the relationship between methane yield and HTC
temperature and BHC adding ratio; and (3) evaluate the hydrochars
potential for mitigation of ammonia inhibition.

⁎
Corresponding author.
E-mail address: kcsheng@zju.edu.cn (K. Sheng).

https://doi.org/10.1016/j.biortech.2019.03.084
Received 23 January 2019; Received in revised form 14 March 2019; Accepted 16 March 2019
Available online 19 March 2019
0960-8524/ © 2019 Elsevier Ltd. All rights reserved.
U. Choe, et al. Bioresource Technology 283 (2019) 340–349

2. Materials and methods at 105 °C. The dried hydrochar was stored in a plastic bag and later used
as an additive in anaerobic digestion. The yield of hydrochar was cal-
2.1. Substrate and inoculum preparation and characterization culated using the Eq. (1):

Hydrochar Dry Mass (g ) ⎞

Fish processing waste was obtained from the canteen of Zijingang Hydrochar Yield (%) = ⎜⎛ ⎟ × 100

Campus, Zhejiang University, Hangzhou, China. FPW contained the fish ⎝ Bamboo Powder Dry Mass (g ) ⎠
head, internal organs, fish fat, bladder, bone, fin, and scales. The bone, (1)
spine, and scales were removed from FPW and the processed FPW was
stored at −20 °C for further use. One day before the experiment, the
2.3. Anaerobic digestion and experiment design
frozen FPW was melted and cut off and homogenized using a blender
(CPEL-23, Shanghai Guosheng, China) to the size of 3–5 mm. The in-
The experiments were conducted in batch mode. 500-mL glass
oculum sludge was collected from the bottom settlement of anaerobic
bottles were used as vessels of the bioreactor and filled by substrate and
fermentation tank that was fed with food and kitchen waste in
inoculum. The TS content of all AD bioreactors was set to 7% by adding
Tianziling Anaerobic Fermentation Engineering operated by Hangzhou
the designated amount of tap water. Bioreactors were sealed using
Environment Group Co., Ltd.
rubber plugs and screw caps (fitted with connection tubes) and flushed
The total solids (TS) and volatile solids (VS) contents of FPW and
with nitrogen gas for 5 min to remove oxygen. Bioreactors were then
inoculum were estimated according to the APHA standard methods
incubated at 37 ± 1 °C for 36 days in a water bath (Shanghai Jinghong
(APHA, 2005). Ash content was measured by heating the samples at
Company, China), shaken manually for 1 min twice a day or before
575 ± 5 °C for two hours in a muffle oven according to ASTM D-1102.
sampling biogas. The generated biogas was trapped in a 1-L glass bottle,
The elemental determination of carbon, nitrogen, hydrogen and sulfur
loaded with a diluted hydrochloric acid solution (pH < 3 to prevent
content of the sample was carried out with a Vario EL elementary
CO2 dissolution). Biogas production was measured using the water
analyzer (Elementary Trading Shanghai Co., Ltd. China) (Carter &
displacement method where biogas produced in the bioreactor dis-
Barwick, 2011), and the oxygen content was estimated as the balance.
placed acid liquid which in turn was gathered in a 500-mL beaker
The pH was monitored with a testo 205 pH meter (Testo AG Germany).
(Mustafa et al., 2016).
The characteristics of the FPW and inoculum are listed in Table 1.
AD experiment of sixteen treatments with two duplicates was car-
Moso bamboo (Phyllostachys pubescens) supplied by China
ried out. Among them, fifteen treatments corresponded to all possible
National Bamboo Research Center in Hangzhou was harvested in Anji,
combinations of the mixing ratio of FPW to hydrochar (1:2, 1:3, and
Zhejiang. The chopped sample was dried at 60 °C overnight to a
1:4) and temperature of hydrochar preparation (200, 220, 240, 260,
moisture content less than 3%, ground to particles via a turbine grinder
and 280 °C). Another group as the control group was fed with FPW only
(XWDJ-130, Zhejiang Xinshiji grinder machine Co. Ltd, China), and
and inoculum. Substrate/inoculum VS ratio was 0.5, i.e., 1.5 g VS of the
passed through a 60-mesh screen. The prepared moso bamboo powder
substrate and 3.0 g VS of inoculum. A group of experiments containing
had an average particle size of 250–300 µm and was used as the sole
inoculum only were conducted as a blank trial to correct for biogas
feedstock for hydrothermal carbonization.
yield. The pH of all bioreactors was adjusted to approximately 7 using
1 M NaOH and 1 M HCl solutions. Biogas yield was estimated from daily
2.2. Hydrothermal carbonization measurement for the first six days, and every three days thereafter until
there was no biogas yield for five days. Biogas production was adjusted
Before the experiment, the moso bamboo powder was dried at 60 °C to standard temperature (0 °C) and pressure (1 atm) using Eq. (2) (Kafle
overnight in a beaker in an oven. 100 g of the dry powder was trans- & Kim, 2013).
ferred into a cylindrical stainless steel reactor (4848, Parr Instrument
Company, USA). Around 1 L of deionized water was weighed and VT × 273 × (760 − pw )
VSTP =
poured into the Parr stirred reactor. The experimental conditions were (273 + T ) × 760 (2)
set at 200, 220, 240, 260 and 280 °C, respectively, with an accuracy
where VSTP is the volume of biogas (L) measured at standard tem-
of ± 2 °C, a heating rate of 3 °C/min and a reaction time of 1 h. The
perature (0 °C) and pressure (1 atm), VT is the volume of biogas mea-
monitored pressure was about 15–70 bar. The content was continuously
sured at temperature T (L), pw is the water vapor pressure as a function
stirred at 90 rpm. When the hydrothermal carbonization was finished
of temperature (mm Hg). T is the temperature of the gas (°C).
and the content temperature was cooled to room temperature the gas-
eous product was then released via the gas valve, and the liquid product
was separated by vacuum filtration with 8 µm pore-size cellulose filter 2.4. Analytical methods
paper. The residue was hydrochar and was dried overnight in an oven
Biogas components (CH4, CO2, H2, and N2) were determined using a
Table 1 gas chromatograph (GC-2014, Shimadzu, Japan) equipped with a
Characteristics of fish waste and inoculum. thermal conductivity detector. The temperatures of the column oven,
injector port, and detector were 100, 120, and 120 °C, respectively.
Parameters Fish waste Inoculum
Biogas samples were taken from the bioreactors by using a special
TS (%, w.b.) 43.54 ± 0.21 8.10 ± 0.14 syringe (injection volume was 200 µL) and injected to the thermal
VS (%, w.b.) 39.20 ± 0.27 4.09 ± 0.12 conductivity detector of the gas chromatograph. Biogas composition
VS/TS (%) 90.04 ± 0.36 50.55 ± 0.32 was measured after 10 days of digestion, and then every 10 days
Total carbon (%, d.b.) 54.20 ± 0.15 26.98 ± 0.09
thereafter and carried out in three replicates.
Total nitrogen (%, d.b.) 5.06 ± 0.11 2.62 ± 0.08
H (%, d.b.) 8.35 ± 0.05 3.63 ± 0.03 After anaerobic digestion, the ammonium nitrogen content in the
S (%, d.b.) 0.51 ± 0.03 1.43 ± 0.04 digested liquid was analyzed using ammonium nitrogen (NH4-N)
O2 (%, d.b.) 31.88 ± 0.05 65.34 ± 0.02 measuring equipment (Cary 60 UV–Vis, Agilent Technologies CO., LTD,
C/N 10.72 ± 0.14 10.29 ± 0.17 China). The aqueous phase from hydrothermal carbonization was used
pH ND 7.67 ± 0.07
Ash content (%, d.b.) 2.14 ± 0.05 51.91 ± 0.04
to determine the chemical oxygen demand (COD) by dichromate oxi-
dation method (Hach, LCK 514 and Hach spectrophotometer DR/2800).
Note w.b., wet base; d.b., dry base; ND, not determined. The pH of hydrochars in the water-extractable fraction was determined
Data are mean values ± standard error of three replicates. around 4.87–5.66 (dry hydrochar mixed with deionized water at a ratio

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Table 2
Effect of hydrothermal carbonization temperature on the yield of bamboo hydrochar and hydrothermal liquid.
Parameters BHC-200 BHC-220 BHC-240 BHC-260 BHC-280

Pressure (bar,psi) 15, 220 23, 350 36, 520 49, 700 70, 940
Yield of BHC (%) 64.8 ± 1.6 54.3 ± 1.2 42.6 ± 1.3 39.3 ± 1.5 36.7 ± 0.9
Yield of HL(%) 83.7 ± 2.2 84.2 ± 1.9 84.8 ± 2.1 83.5 ± 1.8 84.6 ± 2.3
pH of HL 4.09 ± 0.14 3.90 ± 0.18 3.75 ± 0.21 3.81 ± 0.17 3.75 ± 0.19
pH of BHC 5.18 ± 0.31 5.22 ± 0.27 5.31 ± 0.29 5.40 ± 0.26 5.32 ± 0.24
Moisture(%) 1.92 ± 0.25 2.69 ± 0.36 0.82 ± 0.22 0.69 ± 0.19 0.89 ± 0.21

BHC: bamboo hydrochar; HL: hydrothermal liquid

Data are mean values ± standard error of three replicates.

Table 3
Physical and chemical characteristics of bamboo hydrochars produced at different temperatures.
Parameters BHC-200 BHC-220 BHC-240 BHC-260 BHC-280

Moisture (%) 0.96 ± 0.02 1.39 ± 0.06 1.35 ± 0.04 1.76 ± 0.08 1.10 ± 0.04
Ash (% db) 0.95 ± 0.11 1.11 ± 0.12 1.08 ± 0.14 0.99 ± 0.18 0.71 ± 0.13
VS (% db) 97.96 ± 0.94 79.29 ± 1.72 79.58 ± 1.47 55.11 ± 0.37 63.75 ± 0.92
FCa (% db) 1.09 ± 0.21 19.60 ± 0.53 19.34 ± 0.57 43.90 ± 0.73 35.54 ± 0.62
C (%) 55.96 ± 1.55 57.85 ± 1.89 66.95 ± 2.02 73.17 ± 2.43 74.58 ± 2.37
N (%) 0.42 ± 0.01 0.47 ± 0.01 0.68 ± 0.01 0.69 ± 0.01 0.81 ± 0.01
H (%) 5.97 ± 0.08 5.99 ± 0.17 5.59 ± 0.13 5.52 ± 0.15 5.37 ± 0.18
S(%) 0.02 ± 0.01 0.02 ± 0.01 0.02 ± 0.01 0.03 ± 0.01 0.03 ± 0.01
Ob (%) 37.63 ± 1.05 35.67 ± 0.98 26.76 ± 0.89 21.28 ± 0.78 19.21 ± 0.59
C/N ratio 128.3 ± 1.47 121.9 ± 1.78 98.86 ± 1.98 106.1 ± 2.01 92.48 ± 2.05

Note: All data were tested or measured on dry basis.

Data are mean values ± standard error of three replicates.
a
100 – (ash + volatile matter), FC: Fixed carbon.
b
Calculated as difference between 100 and total of C/H/N. db = dry basis.

Table 4
Specific surface areas, total pore volume and pore distribution characters of bamboo hydrochars.
Sample BET surface areas (m2/ Adsorption cumulative volume of pores (pore size Adsorption average pore Most frequent pore diameter BJH Average pore size
g) 1.70–300.00(nm) (cm3/g) size (nm) (nm) (nm)

BHC-200 9.32 ± 0.24 0.136 ± 0.017 14.75 ± 0.21 18.63 ± 0.53 8.78 ± 0.23
BHC-220 8.36 ± 0.21 0.035 ± 0.005 11.79 ± 0.18 28.21 ± 0.85 5.53 ± 0.17
BHC-240 7.63 ± 0.16 0.067 ± 0.014 11.36 ± 0.15 28.79 ± 0.93 5.20 ± 0.32
BHC-260 5.88 ± 0.14 0.034 ± 0.009 10.86 ± 0.16 30.92 ± 1.04 4.92 ± 0.29
BHC-280 5.18 ± 0.27 0.021 ± 0.008 11.30 ± 0.12 2.88 ± 0.46 4.62 ± 0.31

Data are mean values ± standard error of three replicates.

of 1:10, w/v) (Zhang et al., 2014). Specific surface areas and porosity
characteristics of hydrochars were conducted with Brunauer-Emmett-
Teller (BET) method using an automatic nitrogen adsorption analyzer
(JW-BK, Automatic Nitrogen Adsorption Equipment Co. Ltd., China)
(Yan et al., 2017).
2.5. Net energy
The total methane energy yield from dry biomass (TME, in kJ/kg)
was calculated by multiplying the total methane production (L/kg, dry
basis) and the minimum heating value of methane of 35.89 kJ
L−1(Mustafa et al., 2018; Mustafa et al., 2017; Theuretzbacher et al.,
2015). Energy for HTC temperature (%) was evaluated by dividing
energy for HTC (kJ/kg dry basis) on TME (kJ/kg dry basis). The net
methane energy (NME) yield can be calculated by subtracting the en-
ergy consumed for HTC from the total methane energy (TME).
3. Results and discussion
3.1. Impact of HTC temperature on bamboo hydrochar characteristics
Table 2 shows the yield of bamboo hydrochar (BHC) along with the
yield of hydrothermal liquid (HL), pH of BHC, pH of HL, and moisture
content. As shown, BHC yields showed a clear decreasing trend with
increasing HTC temperature, which decreased from 64.8% to 36.7%
when the temperature increased from 200 to 280 °C respectively. The
pH for BHC was ranged between 5.18 and 5.40 and for HL was ranged
between 3.75 and 4.09. Similarly, Becker et al. (2014) have reported
that the pH value of hydrothermal liquid was ranged from 3 to 4 with
pine wood feedstock, the tropical hardwoods, poplar, and wheat straw.
The physical and chemical characteristics of bamboo hydrochars
produced at different temperatures are shown in Table 3. The results
showed that the highest volatile solids content 97.96% was observed
with HTC temperature of 200 °C (BHC-200), and the fixed carbon
content was 0.95%. When the HTC temperature was above 220 °C, the
fixed carbon content showed a tendency to decrease gradually. Table 3
showed that as the hydrothermal carbonization temperature increased,
the carbon and nitrogen content also increased. The highest carbon and
nitrogen content of bamboo hydrochar was 74.58%, 0.81% with BHC-
280, and the lowest carbon and nitrogen content was 55.96%, 0.42%
with BHC-200, respectively. In contrast, the highest C/N ratio 128.31
was noticed with BHC-200, and the lowest 92.48 was observed with
BHC-280.
BET specific surface areas, total pore volumes, and pore distribution
characters of bamboo hydrochars are shown in Table 4. The highest
specific surface areas, cumulative adsorption volume of pores (pore size
1.70–300.00 nm), and adsorption average pore size of 9.32 m2/g,
0.136 cm3/g, and 8.78 nm respectively were obtained at BHC-200.

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350
BHC-200 (1:2) BHC-220 (1:2) BHC-240 (1:2)

300 BHC-260 (1:2) BHC-280 (1:2) control

Cumulative biogas yield (L/Kg VS) 250

200

150

100

50

0
0 3 6 9 12 15 18 21 24 27 30 33 36
350
BHC-200 (1:3) BHC-220 (1:3) BHC-240 (1:3)

300 BHC-260 (1:3) BHC-280 (1:3) control

Cumulative biogas yield (L/Kg VS)

250

200

150

100

50

0
0 3 6 9 12 15 18 21 24 27 30 33 36

350
BHC-200 (1:4) BHC-220 (1:4) BHC-240 (1:4)

300 BHC-260 (1:4) BHC-280 (1:4) control

Cumulative biogas yield (L/Kg VS)

250

200

150

100

50

0
0 3 6 9 12 15 18 21 24 27 30 33 36
Digestion time (days)
Fig. 1. Cumulative biogas yield during 36-day AD of mixed FPW and hydrochar (produced at 200, 220, 240, 260, and 280 °C) at mixing ratio of (a) 1:2, (b) 1:3, and
(c) 1:4.

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Table 5
Significance of the HTC temperature, bamboo hydrochar (BHC) adding ratio
and the interaction effect (HTC × BHC) for biogas and methane yield (2-way
ANOVA p < 0.05).
Parameter p-Value HTC p-Value BHC
a
Biogas yield < 0.001 0.010
Methane yield a < 0.001 0.023
Methane content% b
< 0.001 0.722
COD removal < 0.001 < 0.001
NH4-N removal < 0.001 < 0.001
NH3 content < 0.001 < 0.001
HTC: hydrothermal carbonization temperature, BHC: bamboo hydrochar
adding ratio. Bold numbers mean significant (p < 0.05).
a
Data calculated from two replicates.
b
Data calculated from three replicates.
While the lowest specific surface areas, cumulative adsorption volume
of pores, and adsorption average pore size of 5.18 m2/g, 0.021 cm3/g,
and 4.62 nm respectively were obtained at BHC-280. Furthermore, the
highest and lowest most constant pore diameter (nm) 30.96 and
2.88 nm was obtained at BHC-260 and BHC-280 respectively.
3.2. Effects of hydrochar on anaerobic digestion of FPW
3.2.1. Impacts of hydrochar on biogas production and yields
Cumulative biogas yield for the 16 (not including the blank group
which contains inoculum) AD groups during 36-day is shown in Fig. 1.
Ultimate biogas production for the mixing ratio of FPW to hydrochar as
1:2 ranged from 174 L/kg VS (BHC-240) to 292 L/kg VS (BHC-200). For
the mixing ratio of FPW to hydrochar as 1:3, the corresponding biogas
yield was 74–281 L/kg VS. For the mixing ratio of FPW to hydrochar as
1:4, the corresponding biogas yield was 84–277 L/kg VS. Fig. 1 showed
that the highest cumulative biogas production yields 292 L/kg VS were
additive BHC-200 which was the ratio of FPW to hydrochar 1:2 with
BHC-200. HTC temperature of 200 °C (at mixing ratio of 1:2, 1:3, and
1:4) improved cumulative biogas yield by 64%, 58%, and 56% re-
spectively, compared with the control group which contained FPW and
inoculum. Furthermore, the mixing ratio of BHC-260 (1:3), and BHC-
240 (1:4) decreased the cumulative biogas production by 58%, and
53% respectively, compared with the control group (178 L/kg VS). Xu
et al. (2018) mentioned that when the hydrochar amount increased
from 4 to 8 g/L, biogas yield decreased, due to the increased amount of
hydrochar adsorbed the extra VFA before the biogas production. HTC
temperature, BHC mixing ratio, and their interactive effect had a sig-
nificant effect on biogas yield at the 95% level (Table 5). As for the
impact of temperature, the highest adsorption average pore size 14.75
(nm) and highest specific surface area 9.32 m2/g (Table 4) was obtained
with hydrochar BHC-200, which also provided favorable conditions for
methanogenic bacteria and improved the biogas yield the most in this
p-Value interaction experiment and was observed in a previous study (Mumme et al., 2014;
Mustafa et al., 2016).
0.002
Table 6. Shows the impact of adding hydrochar ratio to FPW and
0.001
0.634
HTC temperature on biogas, methane yield and content, NH3 content,
< 0.001 COD and NH4-N removal after AD. As shown in Table 5, the HTC
< 0.001 temperature, BHC mixing ratio, and their interactive effect had a highly
< 0.001 significant effect on NH3 content, COD and NH4-N removal at the 95%
level. The increased biogas production yield of 292, 281, and 277 (L/kg
VS) in the BHC-200 at the different hydrochar adding ratio (1:2, 1:3,
and 1:4) can be a result of high COD removal of 1975, 2025, and 1734
(mg/L), and high NH4-N removal by additive of 115, 97, 66 (mg/g−1),
and low NH3 content of 3.4, 4.7, and 4.0 (mg/L) respectively. Reza
et al. (2015) found that all hydrochar additives for biogas production
increased NH4-N removal and the removed quantity correlated with the
specific surface area of the additive. Bai et al. (2013) have reported that
hydrochar revealed the magnitude of faster degradation than pyrochar.
Hence during the experiment, hydrochar produced at 200 °C was
showed the right degradation property for biogas production on anae-
robic digestion (Bai et al., 2013). Because degradation of feedstock and
additive were the influence of biogas production on anaerobic diges-
tion, biogas production yields were assumed to equal degradation of
hydrochar during 36 days experiment.
Cumulative biogas production yields of BHC-240(1:4) and BHC-
260(1:3) additive experimental trials were very lower than the control.
A recent study reported that organic matter in hydrochar during AD
could be used for biogas production because part of biodegradable
nutriment could be retained in low HTC temperature (220 °C) through
hydrochar preparation process (Idowu et al., 2017; Xu et al., 2018). It
was due to that the VS% in hydrochar sharply decreased from 97.96%
to 55.11% when the HTC temperature increased from 200 °C to 260 °C
(Table 2). So the biogas production using BHC-200 additive higher than
BHC-240 and BHC-260. Erdogan et al. (2015) have reported that
compounds such as phenol during hydrothermal carbonization were
found in hydrothermal liquid at 260 °C for 2 h, the amount of phenol
increased with the higher temperature. They reported that phenols are
degradation products of lignin, were detected in the aqueous phase
obtained from HTC at 260 °C for 120 min. So in the hydrothermal
carbonization products, the compounds such as phenols could inhibit
the biogas production process, and biogas production yields decreased
using BHC-260 additive. Aragón-Briceño et al. (2017) reported that the
presence of less digestible higher molecular weight organic compounds

Table 6
Impact of adding hydrochar ratio to FPW and HTC temperature on biogas, methane yield and content, NH3 content, COD and NH4 removal after AD.
Treatment Biogas Yield (L/kg- CH4 content (%) CH4 Yield L/kg- COD removal (mg/ NH4-N removal (mg/ NH4-N removal by additivea NH3 (mg/L)
VS) VS) L) L) (mg/g−1)

Control 178 54.2 97 – – – 24.5

BHC-200(1:2) 292 74.9 219 1975 383 115 3.4
BHC-220(1:2) 254 65.3 166 531 269 81 7.7
BHC-240(1:2) 174 54.8 96 1156 288 87 14.9
BHC-260(1:2) 196 56.5 110 1059 213 64 31.7
BHC-280(1:2) 251 62.4 157 1144 126 38 42.9
BHC-200(1:3) 281 76.4 215 2025 486 97 4.7
BHC-220(1:3) 268 70.9 190 1635 397 80 8.4
BHC-240(1:3) 118 51.9 61 1048 464 93 23.8
BHC-260(1:3) 74 50.7 38 734 474 95 18.8
BHC-280(1:3) 244 63.2 154 1819 348 70 7.1
BHC-200(1:4) 277 74.2 206 1734 442 66 4.0
BHC-220(1:4) 229 62.1 142 1598 421 63 6.5
BHC-240(1:4) 84 49.9 42 570 409 61 8.2
BHC-260(1:4) 204 58.7 120 1470 362 54 21.6
BHC-280(1:4) 214 60.2 129 1723 451 68 12.3

a
Calculated by difference to control in mg NH4-N per g of additive.

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BHC ratio (1:2) BHC ratio (1:2)

250 250
(a) (b)
Methane yield (mL/g-VS)

Methane yield (mL/g-VS)

200 200

150 150

100 100

50 y = -2.3101x + 666.52 50 y = 1.5739x - 287.58

R² = 0.6385 R² = 0.8202
P = 0.0565 P = 0.0129
0 0
190 200 210 220 230 240 230 240 250 260 270 280
HTC HTC
BHC ratio (1:3) BHC ratio (1:3)
250 250
(c) (d)
Methane yield (mL/g-VS)

Methane yield (mL/g-VS)

200 200

150 150

100 100

50 y = -3.8418x + 1000.5 50 y = 2.3267x - 520.66

R² = 0.8581 R² = 0.5704
P = 0.0079 P = 0.0825
0 0
190 200 210 220 230 240 230 240 250 260 270 280
HTC HTC
BHC ratio (1:4) BHC ratio (1:4)
250 250
(e) (f)
Methane yield (mL/g-VS)

Methane yield (mL/g-VS)

200 200

150 150

100 100

50 y = -4.0874x + 1029.2 50 y = 2.1656x - 466.16

R² = 0.9538 R² = 0.7575
P = 0.0008 P = 0.0241
0 0
190 200 210 220 230 240 230 240 250 260 270 280
HTC HTC

Fig. 2. Correlation between the methane yield and hydrothermal carbonization (HTC) temperature at different BHC ratio (a–b) 1:2, (b–c) 1:3 and (e–f) 1:4.

formed during the hydrothermal process at 250 °C or a higher tem-
perature could delay biogas production.
3.2.2. Impacts of hydrochar on methane production and yields
The methane content and final methane yield are shown in Table 6.
The amount of BHC additive influenced the methane content in the
biogas. The methane yield and content in BHC-200 added experimental
trials was higher than that other additives. When the feedstock to BHC-
200 ratio was 1:3, the methane contents was highest, 76.44%, which
was 20% higher than the content of 54.22% in the control group. While
the highest methane yield (219 L/kg-VS) was obtained at HTC tem-
perature of 200 °C at 1:2 for the mixing ratio of FPW to hydrochar,
which led to 127% increase in methane yield compared to the control
group with only FPW as substrate. Nyktari et al. (2017) have reported
that methane content in anaerobic fermentation using hydrothermal
carbon was 63.5–77.7%.
Then in case of mixing ratios of 1:2 and 1:4 with BHC-200, the
methane content was 74%. It was found that all added BHC-200 ad-
ditive has increased the methane content in the biogas produced on
anaerobic digestion of FPW. Shen et al. (2015) mentioned that the
increase in methane content could be due to the transformation of VFA
and ethanol to methane by the functioned groups which exist on the
surface of hydrochar and that the alkaline nature of hydrochar main-
tained the optimal pH for anaerobic digestion. Ahmad et al. (2014)
have reported that several mechanisms for CO2 removal in the digester,
including adsorption, partition and polarity attraction. As mentioned
before, the high porosity of the BHC-200 provides a large surface area
of carbonized and on-carbonized sites for CO2 adsorption and separa-
tion. So it could be assumed that methane content with BHC-200 ad-
ditives was highest than other BHC additives. With BHC-280 addition,
the mixing ratios of 1:3, 1:2 and 1:4 were corresponding to the methane
contents of 70.87, 65.34 and 60.24%, respectively, and all of them were
higher than that of the control group.
In case of all added BHC-240 and BHC-260 additives experimental
trials, the methane content was very lower than the controls (FW+In),
the lowest methane content was feedstock to BHC-240 ratio 1:4, 49.9%.
Also, the lowest methane yield (38 and 42 L/kg-VS) was obtained at
BHC-260 (1:3) and BHC-240 (1:4), which led to −58 and −53% re-
spectively, decrease in methane yield compared to the control group.
Aragón-Briceño et al. (2017) reported that the inhibitory effect of the

345
U. Choe, et al. Bioresource Technology 283 (2019) 340–349

BHC ratio (1:2) BHC ratio (1:2)

80 80

75 (a) 75 (b)

Methane content (%)

Methane content (%)

70 70

65 65

60 60

55 55

50 50
y = -0.5x + 174.97 y = 0.19x + 8.5
45 R² = 0.815 45 R² = 0.3076
P = 0.0137 P = 0.2533
40 40
190 200 210 220 230 240 230 240 250 260 270 280
HTC HTC
BHC ratio (1:3) BHC ratio (1:3)
80 80

75 (c) 75 (d)

Methane content (%)

70
Methane content (%)

70

65 65

60 60

55 55

50 50
y = -0.615x + 201.68 y = 0.285x - 18.85
45 R² = 0.8389 45 R² = 0.5315
P = 0.0103 P = 0.1001
40 40
190 200 210 220 230 240 230 240 250 260 270 280
HTC HTC

BHC ratio (1:4) BHC ratio (1:4)

80 80
75 (e) 75 (f)
Methane content (%)

70
Methane content (%)

70
65 65
60 60
55 55
50 50
y = -0.61x + 196.28 y = 0.26x - 11.333
45 R² = 0.9159 45 R² = 0.5921
P = 0.0027 P = 0.0736
40 40
190 200 210 220 230 240 230 240 250 260 270 280
HTC HTC

Fig. 3. Correlation between the methane content and hydrothermal carbonization (HTC) temperature at different BHC ratio (a–b) 1:2, (b–c) 1:3 and (e–f) 1:4.

hydrochar and the process water at 250 °C might have inhibited me-
thanogenic bacteria. Also, they have found that another factor which
might influence is the presence of less digestible higher molecular
weight organic compounds formed during the thermal process at 250 °C
temperature or other compounds that could delay methane production.
They also have reported that the presence of hydrochar affects the
consumption of organic matter by anaerobic bacteria, so BHC-240 and
BHC-260 additive on anaerobic digestion of FPW may be the role of
decreasing methane production. Aragón-Briceño et al. (2017) already
reported that although some factor that might influence is the presence
of less digestible higher molecular weight organic compounds formed
during hydrothermal carbonization process at that temperature or other
compounds that could delay methane production. It was observed that
the hydrothermal carbonization process of sewage sludge at 250 °C
resulted in a hydrochar that enhanced the net output of VFAs but de-
layed methane production (more extended lag phase). It could be ex-
plained that hydrothermal carbonization temperature at 250 °C pro-
duced some compounds maybe inhibit methanogenic bacteria.
A two-way ANOVA was conducted (Table 5) to estimate whether
the effects of HTC temperature, BHC mixing ratio and their interaction
on the methane yield and methane content were significant. The results
showed that HTC temperature had a significant effect on both methane
yield and methane content. BHC mixing ratio and the interactive effects
between HTC temperature and BHC mixing ratio had significant effect
on methane yield, but no significant effect on methane content.
Fig. 2 shows the correlation between the methane yield and hy-
drothermal carbonization (HTC) temperature at different BHC ratio.
Fig. 2(a, c and e) HTC temperature start from 200 to 240, while
Fig. 2(b, d, and f) HTC temperature start from 240 to 280. As shown in
Fig. 2(a, c and e) there is a relatively strong linear correlation
(R2 = 0.86 and 0.95) between the HTC and the methane yield for BHC
ratio 1:3 and 1:4, respectively. In comparison, the corresponding cor-
relation between HTC temperature starts from 240 to 280 (Fig. 2b, d,
and f) and methane yield was relatively poor (R2 = 0.57 and 0.76, re-
spectively). While relatively weak linear correlation (R2 = 0.64) be-
tween the HTC starts from 200 to 240 and the methane yield for BHC
ratio 1:2. In comparison, the corresponding correlation between HTC
temperature starts from 240 to 280 and methane yield was relatively

346
U. Choe, et al. Bioresource Technology 283 (2019) 340–349

450 BHC ratio (1:2) strong (R2 = 0.82).

(a)
NH4-N removal by additive (mg/g-1)

400 As shown in Fig. 3, methane yield was highest at HTC 200 °C and
350
then decreased at 240 °C and then increased again at 280 °C but was
lower than 200 °C. The reason may be due to more than 90% of
300
hemicellulose degraded at HTC 200 °C, and cellulose content in hy-
250 drochar obtained from maize silage increased to 38.7%, and when the
200 temperature increased to 250 °C the cellulose content decreased to 7.4%
150 (Reza et al., 2014). It is also known that cellulose the most important
y = -2.845x + 938.3 component in the substrate for methanogenic bacteria to produce me-
100 R² = 0.8727
thane (Mustafa et al., 2016; Mustafa et al., 2017). Furthermore, there is
50
a relatively strong linear correlation (R2 = 0.87) between HTC tem-
0 perature and the NH4-N removal by additive at BHC ratio of 1:2 (Fig. 4
190 200 210 220 230 240 250 260 270 280 290
a). As shown in Table 6, the highest NH4-N removal by additive was
HTC
115 mg/g−1 at HTC 200 °C and BHC (1:2), this may be due to in-
BHC ratio (1:3) creasing the BET surface area (9.32 m2/g) and adsorption average pore
250 size (14.75 nm) of hydrochar at 200 °C. Fig. 5.
(b) While the decline in the methane yield at HTC 240 °C may be at-
Methane yield (mL/g-VS)

200 tributed to the existence of volatile organic compounds (VOC) such as

phenol and furfural, Which consists in preparing hydrochar at tem-
150 peratures higher than 220 °C (Reza et al., 2014). The presence of phenol
often makes the hydrochar toxic for methanogenic bacteria, thus re-
100 y = 0.1379x - 68.654 ducing methane production (Libra et al., 2011). However, with the
R² = 0.9042
increase of HTC temperature, the phenol content reduces as they are
50 probably degraded into smaller materials like acids or alcohols (Reza
et al., 2014), this may explain the increase in methane yield again at a
0 temperature of 280 °C (Fig. 3). Reza et al. (2014) found that the phenol
500 750 1000 1250 1500 1750 2000 2250
concentration was 8.4 (mg/kg db) at HTC 200 °C, then increased to 27.4
COD removal (mg/L)
(mg/kg db) at 230 °C, then decreased to 16.6 (mg/kg db) at 250 °C.
BHC ratio (1:4) Furthermore, there is a linear correlation (R2 = 0.90 and R2 = 0.71)
250
between COD removal and the methane yield at BHC ratio of 1:3 and
(c) 1:4 respectively (Fig. 4b–c).
Methane yield (mL/g-VS)

200 Fig. 3 shows the correlation between the methane content and hy-
drothermal carbonization (HTC) temperature at different BHC ratio.
150 Fig. 3(a, c and e) HTC temperature start from 200 to 240 °C, while
Fig. 3(b, d, and f) HTC temperature start from 240 to 280 °C. As shown
100 in Fig. 3(a, c and e) there is a relatively strong linear correlation
(R2 = 0.82, 0.84 and 0.92) between the HTC and the methane yield for
50 y = 0.1043x - 20.249 BHC ratio 1:2, 1:3 and 1:4, respectively. In comparison, the corre-
R² = 0.7135 sponding correlation between HTC temperature starts from 240 to
0 280 °C (Fig. 2b, d, and f) and methane yield was relatively poor
500 750 1000 1250 1500 1750 2000 (R2 = 0.31, 0.53 and 0.59, respectively).
COD removal (mg/L)

Fig. 4. Correlation between (a) HTC temperature and NH4-N removal by ad- 3.3. Impact of hydrochar on the removal of COD and NH4-N
ditive at BHC ratio of 1:2, (b–c) COD removal and the methane yield at BHC
ratio of 1:3 and 1:4. Fig. 4 shows the COD and NH4-N contents after the anaerobic di-
gestion of FWP with additive BHC. The content of all the adding BHC-
200 experimental trial was lower than the other treatment, i.e.,

Fig. 5. Variation of COD and NH4-N contents after finished anaerobic digestion of FWP with additive BHC.

347
U. Choe, et al. Bioresource Technology 283 (2019) 340–349

Table 7 that the prepared hydrochar from walnut shells and olive nut had a
Effect of adding hydrochar ratio to FPW and HTC temperature on net energy surface area of 27 and 22 m2/g respectively.
yield of FPW by AD.
Treatment HTC TME Energy for Energy for NME 3.4. Effect of HTC temperature on net energy yield
Temp. Yield (kJ/ HTC Temp. HTC Temp. Yield (kJ/
(°C) kg, d.b.) (kJ/kg, d.b) (%) kg, d.b) The impact of the HTC temperature and adding ratio of hydrochar
on the net energy yields (NME) for the different treatments conditions
Control – 1878 – – 1878
BHC-200(1:2) 200 4256 846 19.9 3410 are shown in Table 7. Total methane energy yield from FPW (control)
BHC-220(1:2) 220 3231 924 28.6 2307 was 1878 kJ/kg (dry basis), 1858–4256 kJ/kg (dry basis) for different
BHC-240(1:2) 240 1858 1020 54.9 838 HTC temperature at the mixing ratio of 1:2, 733–4173 kJ/kg (dry basis)
BHC-260(1:2) 260 2148 1117 52.0 1031
for different HTC temperature at the mixing ratio of 1:3, and
BHC-280(1:2) 280 3048 1224 40.2 1824
BHC-200(1:3) 200 4173 856 20.5 3317
818–3996 kJ/kg (dry basis) for different HTC temperature at the mixing
BHC-220(1:3) 220 3697 924 25.0 2773 ratio of 1:4. The highest percentage of energy consumed for HTC
BHC-240(1:2) 240 1187 1020 86.0 167 temperature was 156% for HTC temperature 260 °C and a mixing ratio
BHC-260(1:3) 260 733 1140 155.5 −407 of 1:3, 20–55% for different HTC temperature at the mixing ratio of 1:2,
BHC-280(1:3) 280 2995 1285 42.9 1710
21–156% for different HTC temperature at the mixing ratio of 1:3, and
BHC-200(1:4) 200 3996 856 21.4 3140
BHC-220(1:4) 220 2767 924 33.4 1843 21–125% for different HTC temperature at the mixing ratio of 1:4.
BHC-240(1:4) 240 818 1020 124.7 −202 Highest net energy yield (NME) for all groups was obtained at HTC
BHC-260(1:4) 260 2331 1140 48.9 1191 temperature 200 °C and a mixing ratio of 1:2 at 3410 kJ/kg (dry basis),
BHC-280(1:4) 280 2502 1285 51.4 1217
followed by 3317 and 3140 kJ/kg (dry basis) with same HTC tem-
perature (200 °C) and mixing ratio 1:3 and 1:4 respectively.
Note: d.b., dry basis, TME – total methane energy, NME – net methane energy.
Similar results for the range of temperature 160–220 °C were also
performed by Mustafa et al. (2018) found that the fraction energy
1744 mg/L for the mixing ratio of 1:3. The highest content of COD was
consumed for hydrothermal pretreatment (HTP) was 25–37% and the
the control group, i.e., 3799 mg/L. In the case of BHC-220 as feedstock
highest net energy yield 2235 kJ/kg (dry basis) was noticed at HTP
to BHC-220 ratio with 1:2, after anaerobic digestion finished, the COD
temperature of 180 °C. Comparing to this study for the range of
content was 3268 mg/L, however in the additive BHC-220 trials added
200–220 °C, the fraction energy consumed for HTC temperature was
the amount was increased to 1:3 and 1:4, the COD content was re-
20–33% for all mixing ratios. Results with negative numbers indicate
markably decreased 2164 mg/L and 2201 mg/L, respectively. As the
that the energy consumed in heating was higher than the total energy
amount of BHC additive increased, it is more advantageous for the at-
produced by methane. Heating more than 220 °C resulted in an adverse
tachment of methanogenic bacteria to the anaerobic fermentation
result. The net energy generated was higher than the control group with
products. As a result, the decreased COD content in the fermentation
temperatures of 200–220 °C at a mixing ratio of 1:2 and 1:3, while at a
products can be evaluated as the activation of the methanogenic bac-
mixing ratio of 1:4 only HTC temperature at 200 °C improved the net
teria and the increase of the biogas production. A two-way ANOVA
methane energy. These results indicate that the use of HTC pretreat-
(Table 5) was carried out to evaluate whether the effects of HTC tem-
ment and adding hydrochar to FPW in proper temperature (200–220 °C)
perature, BHC mixing ratio and their interaction on the NH3 content,
and mixing ratio (1:2 or 1:3) can significantly improve the net energy
COD and NH4 removal were significant. The results showed that both
yield.
HTC temperature and BHC mixing ratio had a significant effect on NH3
content, COD and NH4 removal.
4. Conclusions
After the experiment finished, it was measured the NH4-N con-
centration of all experimental trials. Fig. 4 showed the variation of NH4-
This study found that in the tested range, a HTC hydrochar pre-
N concentration on anaerobic digestion of FPW after the anaerobic
paration temperature of 200 °C best promoted the biogas and methane
digestion finished. As shown in Fig. 4, after the anaerobic digestion,
production yields. Highest biogas yield (292 L/kg-VS), methane yield
additive BHC-200 experimental trials which feedstock to hydrochar
(219 L/kg-VS), and net methane energy (3410 kJ/kg, dry basis) were
ratio with 1:3, showed the lowest NH4-N concentration in the fer-
obtained at HTC temperature of 200 °C at 1:2 for the mixing ratio of fish
mented solution and the highest NH4-N level was the control of fish
processing waste to hydrochar, which led to a 64%, 127%, and 82%
processing waste added inoculum. After anaerobic digestion of FPW
increase in biogas production, methane yield, and net methane energy
was finished, the lowest content of NH4-N in the anaerobic fermenta-
compared to the control group with only FPW as substrate, respectively.
tion was 783 mg/L, and the highest experimental trial was controlled
Further addition of HTC hydrochar, i.e., the ratios of 1:3 and 1:4, did
(FPW add inoculum), 1225 mg/L. And then It was found that NH4-N
not improve biogas production and methane energy recovery.
content of all tested preliminary tests which mixing ratios of FPW and
BHC with 1:3, 1:4 was much lower than all experimental trials of
Acknowledgements
mixing ratio with 1:2. As shown in Table 6, when the amount of hy-
drochar increased in the substrate the NH4-N removal increased, this is
The authors are grateful to the China National Key R&D Program
often due to the increased surface area of the hydrochar which led to
(No. 2016YFD0800804) for financial support, and the project sup-
the adsorption of NH4-N on the surface. Xu et al. (2018) found that 1 g/
ported by a special fund for the agro-technique extension of the New
L of hydrochar from rice straw could adsorb 25 mg of NH4-N and 50 mg
Countryside Development Institute at Zhejiang University
of VFA, and Takaya et al. (2016) mentioned that 1 g/L of hydrochar
(2017ZDNT015).
from oak wood could remove 105–146 mg of NH4-N. In this study, NH4-
N removal by additive ranged between 38 and 115 mg/g−1 (Table 6).
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