Bioresource Technology Reports 18 (2022) 101033

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Bioresource Technology Reports

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Anaerobic co-digestion of cattle rumen content and food waste for biogas
production: Establishment of co-digestion ratios and kinetic studies
Newton A. Ihoeghian a, Andrew N. Amenaghawon a, *, Mike U. Ajieh b, c, Cyprian E. Oshoma d,
Abraham Ogofure d, Nosakhare O. Erhunmwunse e, Valerie I.O. Edosa f, Isioma Tongo e,
Ifeyinwa S. Obuekwe d, Ebuwa S. Isagba g, Christopher Emokaro h, Lawrence I.N. Ezemonye e,
Alfonso J. Lag-Brotons i, Kirk T. Semple i, Alastair D. Martin j
a
Department of Chemical Engineering, University of Benin, Benin City, Edo State, Nigeria
b
National Centre for Energy and Environment, Energy Commission of Nigeria, University of Benin, Benin City, Edo State, Nigeria
c
Department of Chemical and Petroleum Engineering, Faculty of Engineering, Delta State University, Oleh Campus, Oleh, Delta State, Nigeria
d
Department of Microbiology, University of Benin, Benin City, Edo State, Nigeria
e
Department of Animal and Environmental Biology, University of Benin, Benin City, Edo State, Nigeria
f
Department of Soil Science and Land Management, University of Benin, Benin City, Edo State, Nigeria
g
Department of Civil Engineering, University of Benin, Benin City, Edo State, Nigeria
h
Department of Agricultural Economics and Extension, University of Benin, Benin City, Edo State, Nigeria
i
Lancaster Environment Center, Lancaster University, Lancaster, United Kingdom
j
Department of Chemical Engineering, Lancaster University, Lancaster, United Kingdom

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

Keywords: This study investigated the batch co-digestion of cattle rumen content (CRC) and food waste (FW) for biogas
Anaerobic digestion production in different ratios (CRC:FW) to assess biogas production and process stability. The results showed that
Cattle rumen content CRC and FW possess characteristics that are desirable for biogas production as seen in their respective total solids
Food waste
(10.85 and 26.53%), volatile solids (89 and 86.83%) and carbon to nitrogen ratio (23.7 and 15.7) values. Co-
Kinetic modeling
digestion improved carbon to nitrogen ratio, biogas yield and pH of the co-substrate compared to individual
Biomethane yield
Co-digestion substrates. The 50:50 co-digestion ratio was found to be optimum as it gave the maximum cumulative biogas
yield of 320.52 ml/gVSadded. Co-digestion also improved the pH, volatile fatty acid (VFA) and total ammonia
nitrogen (TAN) characteristics during digestion. The cone model was able to adequately represent the kinetics of
the process. These findings have provided very useful insights into the co-digestion of CRC and FW.

1. Introduction this figure is approximately 60% of the total annual waste generation in
sub-Saharan Africa (Ike et al., 2018). The majority of the wastes
Nigeria is the most populous nation in Africa and her population is generated in Nigeria are not collected and properly managed as a result
growing yearly at an average rate of 2.5% (Idowu and Okedere, 2020). of poor waste management frameworks (Ezechi et al., 2017). The
The growing population of Nigeria has been put in sharp focus because organic portion of these waste streams has been estimated to be as high
of some current negative realities. For instance, Nigeria is facing serious as 60% and this represents a significant resource that provides an op­
energy crisis whereby the amount of energy generated cannot meet the portunity for Nigeria to diversify her energy mix by generating bio­
demand (Adewuyi, 2020). According to the 2019 report of the National energy from these waste materials. One of the alternatives for generating
Population Commission of Nigeria, 43.5% of Nigerians do not have ac­ energy from these wastes is anaerobic digestion.
cess to grid electricity with the majority of these people living in rural The anaerobic digestion (AD) process has been established as a
areas (Isihak et al., 2020). This has had significant negative socioeco­ sustainable way of treating organic waste. This is in addition to the value
nomic and developmental consequences. Furthermore, Nigeria gener­ added to the waste through the generation of energy in the form of
ates an estimated average of 42 million tons of solid wastes annually and biogas and organic fertilizer (digestate) (Karki et al., 2021).

* Corresponding author.
E-mail address: [email protected] (A.N. Amenaghawon).

https://doi.org/10.1016/j.biteb.2022.101033
Received 18 March 2022; Received in revised form 19 March 2022; Accepted 20 March 2022
Available online 24 March 2022
2589-014X/© 2022 Elsevier Ltd. All rights reserved.
N.A. Ihoeghian et al. Bioresource Technology Reports 18 (2022) 101033

The two key organic waste streams of focus in the current study are addition, the majority of the studies focused on the utilization cattle
food waste (FW) and cattle rumen content (CRC). Globally, food waste dung or cattle manure as feedstock for biogas production. However, this
can make up as much as 50% of municipal solid waste and a recent method is not sustainable in a country such as Nigeria where nomadic
estimate puts the annual global generation of food waste at about 2 cattle rearing is mainly favored (Ogboru and Adejonwo-Osho, 2018).
billion tons, which has been projected to rise to 2.2 billion tons in 2025 Furthermore, there are hardly any reports in the literature that consid­
(Strazzera et al., 2021); and this situation is not different in Nigeria (Ike ered co-digestion of cattle rumen content and food waste. When digested
et al., 2018). In Nigeria, the above statistic are obtained from the ever as a mono-substrate, food waste is prone to producing high amounts of
growing food vendors in the country as well as food wastage resulting VFAs and ammonium compounds which can lead to the failure of the AD
from poor harvesting and storage practices (Makanjuola et al., 2020). process when they are accumulated in high concentrations (Naran et al.,
Nigeria currently has in excess of 20 million cattle, the majority of 2016). Co-digestion of food waste with cattle rumen content could
which are slaughtered for meat in abattoirs. With the consumption of potentially alleviate this problem by nullifying VFA toxicity as well as
meat projected to double (from about 360,000 t per year) by 2050, there boosting nutrient balance. However, the optimum ratio for combining
will also be a concomitant increase in abattoir waste including a sig­ both substrates is not universal, which creates room for further inves­
nificant proportion of cattle rumen content (Odekanle et al., 2020). As a tigation (Kaur and Kommalapati, 2021). In addition, some reports show
result of the poorly regulated activities of abattoirs, their wastes are that when co-digesting organic waste streams with animal manure, some
disposed indiscriminately thereby constituting serious environmental antagonistic effect could be introduced if too much animal manure is
pollution problems. The rich organic content of these wastes makes used (Alfa et al., 2020). It is thus necessary to investigate this in the
them a valuable resource for biogas production. context of co-digestion of cattle rumen content with food waste. This
Currently, mono-feedstock digestion is favored in most AD plants. forms the major thrust of the current study which involves the estab­
However, this approach has been shown to have several limitations such lishment of co-digestion ratios of cattle rumen content and food waste
as low biogas yield per gram VS added (Zahan et al., 2018), digester for optimum biogas production and process stability.
instability (Li et al., 2018), feedstock availability (Karki et al., 2021),
nutrient imbalance resulting from improper carbon‑nitrogen (C/N) ra­ 2. Materials and methods
tios and poor microbial diversity (Kaur and Kommalapati, 2021). Co-
digestion of multiple feedstocks provides an interesting option for 2.1. Feedstock collection and preparation
overcoming the limitations of mono-feedstock digestion. The key ad­
vantages of co-digestion include improved biogas production, better Cattle rumen content from freshly eviscerated cattle was obtained
digester stability, more diversified microbial population, improved from the Vegetable Market abattoir in Benin City, Edo State, Nigeria.
nutrient balance resulting from proper C/N ratio, improved buffering Fresh food waste was collected from the food court within the University
capacity and better quality digestate which are derived from the syn­ of Benin Campus in Benin City, Edo State, Nigeria. The nonbiodegrad­
ergism introduced by the multiple feedstocks (Awosusi et al., 2021). able contaminants in the feedstocks such as metal, glass and plastics
Several researchers have investigated co-digestion of different waste were sorted out of both samples. Blending of the feedstocks was carried
streams as a strategy for improving biogas production. Awosusi et al. out as necessary using a laboratory blender (HMF-347, Hanil, Korea) to
(2021) investigated the co-digestion of animal manure and kitchen achieve a homogenized substrate. The materials were then stored at 4 ◦ C
waste for biogas production. Their findings revealed that optimum in a refrigerator before the experiments to prevent biological decom­
biogas production was recorded at a 3:1 feed ratio of kitchen waste to position before use. All reagents used were of analytical grade and were
animal manure for a retention time of 30 days. In another study, Alfa procured from Loba Chemie Ltd., Mumbai, India.
et al. (2020) investigated biogas production from a feedstock mix of cow
dung and horse dung in a 25 l cylindrical digester over a period of 37 2.2. Feedstock characterization
days. They reported that the highest daily biogas production and
maximum cumulative biogas production were recorded with a feedstock Characterization of the feedstocks was carried out according to
mix of 25% cow dung and 75% horse dung. Oladejo et al. (2020) standard methods (American Public Health Association, 2005). The tests
assessed the biogas production potential of cow dung, food waste and carried out included total solids (TS), volatile solids (VS), ash content,
piggery dung in a co-digestion set up. The highest cumulative biogas moisture content and chemical oxygen demand (COD). Elemental
production was obtained when all three feedstocks were co-digested for analysis (C, H, N, S, O) was carried out using an elemental analyzer
30 days. Several other studies have investigated the co-digestion of (Elementar Americas Inc., NY). pH was measured using a calibrated pH
organic waste streams such as food waste and chicken manure meter (HACH instruments). Total ammonia nitrogen (TAN) was deter­
(Chuenchart et al., 2020), dairy manure, meat and bone meal and crude mined following the method of Charnier et al. (2016), while total vol­
glycerol (Andriamanohiarisoamanana et al., 2018), cattle manure and atile fatty acid content was estimated from the relationship between pH
cheese whey (Bertin et al., 2013) with varying levels of success. It was and TAN as reported by Syaichurrozi et al. (2018).
generally agreed that the introduction of animal manure in the co-
substrate helped to negate the accumulation of volatile fatty acids as pH = 9.43 − 2.02 [
VFAs
( )] (1)
well as maintaining desirable moisture and nutrient balance (Karki (NH3 − N) + NH+
4 − N
et al., 2021).
The organic wastes utilized for co-digestion are made up of lipids, where (NH3 − N) + (NH4+ − N) = TAN
proteins and carbohydrates in different proportions and studies have
shown that interactions between these components can occur during the 2.3. Co-digestion studies
AD process (Astals et al., 2014; Lu et al., 2017). Because of the complex
nature of these substrates, studies on the nutrient level and how their Batch co-digestion studies were carried out in seven experimental
interactions influence the AD process are still limited. Thus, it is setups reflecting the co-digestion ratios investigated in this study. All
important to optimize the mixing ratio for combining these substrates to seven digesters were fed with co-substrates made up of cattle rumen
derive maximum synergistic benefits. content and food waste in different ratios (0:100, 20:80, 40:60, 50:50,
Within the context of the authors' search of literature, very little 60:40, 80:20 and 100:0) which were selected on the basis of previous
work has been reported on the utilization of cattle rumen content as a work (Kaur and Kommalapati, 2021; Orangun et al., 2021). Each
feedstock for biogas production (Ajieh et al., 2020; Mohammed et al., experimental setup was replicated three times. The anaerobic digestion
2019). These studies mainly focused on mono-feedstock digestion. In was carried out in different 25 l digesters constructed from redundant

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N.A. Ihoeghian et al. Bioresource Technology Reports 18 (2022) 101033

25 l gas cylinders. Two openings each for feeding and evacuating Mashad, (2013), Adanikin et al. (2017) and Owamah et al. (2021), the
digestate were introduced. A 1 ½” nonreturn or one-way valve was used models considered were first order, Fitzhugh, modified Gompertz and
for the feedstock feeding opening while a 1 ½” ball valve was used for cone models as given in Eqs. (5), (6), (7) and (8) respectively.
the digestate evacuation opening. A 1 ½” cap was used for locking the ( )
P = Pm 1 − e− kt (5)
valves. The nonreturn valve was chosen to avoid material loss during
feeding. A pressure gauge was fitted to the cylinder to monitor the gas
where P is the cumulative methane yield at any time t (ml CH4/g VS), Pm
pressure (Fig. S1 in supplementary materials).
is the simulated maximum methane yield (ml CH4/g VS) and k is the first
Each feedstock was combined in the appropriate ratio (on a wet
order rate constant (d− 1).
basis) and then mixed with clean water to form a slurry which was then
charged into the digester and occupied 50% of the digester volume in P = Pm (1 − exp( − kt)n ) (6)
order to leave sufficient head room for gas production. The digestion
{ [ ]}
process was left to run for a retention time of 42 days under ambient Rmax .e
P = Pm .exp − exp (λ − t) + 1 (7)
conditions. The contents of the digesters were manually agitated by Pm
shaking the cylinders once a day before sampling to ensure proper
mixing (Kaur and Kommalapati, 2021). The quantity of biogas produced Rmax is the maximum methane production rate (ml CH4/g VS/day), e is
was measured daily by the downward displacement of water method. the mathematical constant (2.718282) and λ is the lag phase for
The gas outlet from the digester supplied the gas into an inverted methane production (d).
measuring cylinder immersed in water (Owamah et al., 2020). Daily gas Pm
measurements were continued until the cumulative gas production for P= n
(8)
1 + (kt)−
three consecutive days was below 1% of already cumulatively produced
gas. The experimental biomethane composition was determined using a where n is a dimensionless shape factor.
Bosean biogas analyzer to establish the methane content of the biogas. It
was calibrated by using identified methane, CO2, O2 and H2S reference 2.5.2. Data analysis
gases before using it for the measurements. In the course of digestion, All the parameters in Eqs. (5) to (8) were determined via nonlinear
other parameters monitored were TS, VS, TAN, pH and VFA. regression using the Solver tool of Microsoft Office Excel 2016. The
procedure employs an iterative least square fitting routine to produce
2.4. Theoretical biomethane yield and co-digestion performance index the optimal goodness of fit between data and function. Analysis of
variance (ANOVA) and Tukey's honestly significant difference (HSD)
The theoretical biomethane yield (TMY) (ml/gVS) of each feedstock test for pairwise comparison of the mean biomethane composition ob­
and co-digested substrates was determined using the Boyle's equation tained during co-digestion were carried out using Minitab v.19 software.
with the results from the elemental analysis of the samples (Boyle, Experimental validation of the models was carried out to ensure that
1977). the predicted biogas yields were in agreement with experimental ob­
( ) ( ) servations. The assessment of the fit of the models was done using
a b 3c n a b 3c
Cn Ha Ob Nc + n − − + .H2 O→ − + + .CO2 goodness of fit statistical indicators such as coefficient of determination
4 2 4 2 8 4 8
( ) (2) (R2), adjusted R2, Akaike's information criterion (AIC) and error terms
n a b 3c
+ + − − .CH4 such as the mean square error (MSE), root mean square error (RMSE),
2 8 4 8
standard error of prediction (SEP) and mean absolute error (MAE) as
( ) shown in Eqs. (9) to (15) (Amenaghawon et al., 2021; El-Mashad, 2013).
22.4 × 4n+a− 82b− 3c × 1000
TMY = (3) ∑n
)
12n + a + 16b + 14c
P i )2
(Pi − ̂
where a, b and c and n indicate the stoichiometric number of moles of H, R2 = 1 − ni=1 ] (9)
∑( )2
̂
O, N, and C respectively. i=1
P i − Pavg
Co-digestion performance index (CPI) is an indicator of additional
[ ]
biomethane obtained from co-digesting CRC and FW. The CPI (Eq. (4)) ( ) n− 1
was used to establish and compare the efficiency of co-digestion with Adjusted R2 = 1 − 1 − R2 × (10)
n− N− 1
respect to mono-digestion of the feedstocks (Awosusi et al., 2021; Kaur
and Kommalapati, 2021). 1∑ n
MSE = P i − Pi )2
(̂ (11)
TMYi − [(TMYCRC × yCRC ) + (TMYFW × yFW ) ] n i=1
CPI = (4)
(TMYCRC × yCRC ) + (TMYFW × yFW ) √̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅
1∑ n

TMYi, TMYCRC and TMYFW are the theoretical biomethane yields of the RMSE = (P̂ i − Pi )2 (12)
n i=1
co-digestion ratio i, cattle rumen content and food waste respectively.
yCRC and yFW are the VS fractions of cattle rumen content and food waste RMSE
respectively. SEP = × 100 (13)
Pavg
According to Awosusi et al. (2021), if CPI > 1, the mixture presented
synergistic effects. If CPI < 1, the mixture presented antagonistic effects 1∑ n ⃒
( )⃒
and if CPI = 1, the effects of the mixture during co-digestion were MAE = ⃒ P̂ i − P,i ⃒ (14)
n i=1
unclear.
( )
RSS 2(N + 1)(N + 2)
2.5. Kinetics of biogas production AIC = nln + 2(N + 1) + (15)
n (n − N − 2)

2.5.1. Kinetic models where n is the number of data points, ̂P i is the estimated value, Pi is the
Biogas production was modeled using various existing models and experimental value, Pi, avg is the average experimental value, N is the
the kinetic constants were determined accordingly after fitting the number of model parameters and RSS is the residual sum of squares.
models to the experimental data. Following from the works of El-

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N.A. Ihoeghian et al. Bioresource Technology Reports 18 (2022) 101033

Table 1 35
100:0 0:100 80:20
Proximate and nutrient analysis of food waste and cattle rumen.
30 60:40 50:50 40:60

Daily biogas produced (ml/gVS)

Property Feedstock 20:80
Cattle rumen content Food waste 25

Proximate analysis 20
TS (%) 10.85 ± 0.15 26.53 ± 0.95
VS (%TS) 89.00 ± 0.50 86.83 ± 0.76 15
Moisture content (%) 89.15 ± 0.15 73.47 ± 0.95
Ash content (%TS) 10.20 ± 0.08 13.49 ± 0.16 10

Ultimate analysis 5
C 48.60 45.50
H 6.94 6.20 0
O 42.40 44.50 0 7 14 21 28 35 42
N 2.05 2.90 Retention time (days)
S 0.01 0.90
C/N 23.70 15.70 Fig. 1. Daily biogas production profile for different co-digestion ratios (CRC:
Empirical formula C27.6H47.1O18.1N C18.1H29.2O13.3N FW) [Error bars indicate standard deviations (n = 3)].

Chemical properties
pH 6.86 ± 0.01 4.12 ± 0.05 350
100:0 0:100 80:20 60:40
COD (mg/l) 13,720.00 ± 120.00 13,073.30 ± 80.8
Total ammonia nitrogen (mg/l) 6493.33 ± 172.50 5350.67 ± 576.62

Cummulative biogas produced

300 50:50 40:60 20:80

Values are the mean ± SD, n = 3. 250

(ml/gVS)
200
3. Results and discussion
150
3.1. Feedstock characterization
100
The results of the feedstock characterization are shown in Table 1. 50
The TS content of cattle rumen content and food waste were obtained as
10.85 ± 0.15 and 26.53 ± 0.95% respectively while their VS contents 0
were 89.00 ± 0.50 and 86.83 ± 0.76% respectively. The high VS values 0 7 14 21 28 35 42
are indicative of the presence of volatile organic materials in the feed­ Retention time (days)
stocks which may be readily degradable (Capson-Tojo et al., 2017).
Fig. 2. Cumulative biogas production profile for different co-digestion ratios
These values are similar to those reported for cassava pulp (93.8%) (CRC:FW) [Error bars indicate standard deviations (n = 3)].
(Glanpracha and Annachhatre, 2016), goat manure and cotton gin res­
idue (84.7% and 87.1 respectively) (Kaur and Kommalapati, 2021), and
composition was 23.70 and 15.70 for cattle rumen content and food
food waste (86.1%) (El-Mashad and Zhang, 2010). The lower VS of FW
waste respectively. Although the C/N ratio of food waste was lower than
relative to CRC directly explains its higher ash content (13.49 ± 0.16%)
that of cattle rumen content, they were however both within the rec­
as shown in Table 1.
ommended C/N range of 9 to 30 for anaerobic digestion (Orangun et al.,
The moisture content of cattle rumen content (89.15 ± 0.15%) was
2021). The C/N ratio is important in the sense that the feedstock with
higher than that of food waste (73.47 ± 0.95%). The higher moisture
the higher value makes more carbon available for biogas production.
content recorded for cattle rumen content is useful for its role in
However, if the nitrogen level is too low (i.e., very high C/N ratio), it can
ensuring desirable moisture levels during co-digestion (Karki et al.,
limit microbial activity as the microorganisms need nitrogen to maintain
2021). The values reported here are similar to those reported by Ven­
adequate growth and metabolic activity. On the other hand, low C/N
kateshkumar et al. (2019) for cow dung (86%), Parra-Orobio et al.
ratios present high nitrogen levels which can result in ammonia inhi­
(2018) for food waste (76%) and Oladejo et al. (2020) for cow dung,
bition. The co-digestion of cattle rumen content and food waste can help
food waste and pig dung (85.6%, 81.1% and 81.3% respectively).
to balance and maintain optimum C/N levels and consequently,
The pH of cattle rumen content (6.86 ± 0.01) was slightly below the
adequate nitrogen and alkalinity levels (Karki et al., 2021). A C/N ratio
neutral pH while that of food waste was in the acidic range (4.12 ±
of 17.21 was reported by Wang et al. (2014) for food waste from
0.05). The pH of the medium during anaerobic digestion is a parameter
different sources while values of 21.87, 20 and 22.69 were reported by
of significant importance because it has a direct impact on the survival of
Zahan et al. (2018), Orangun et al. (2021) and Odekanle et al. (2020) for
the microbial community (Begum et al., 2018). The reported optimum
poultry litter, goat manure and abattoir waste respectively. Overall, the
pH for anaerobic digestion is in the range of 6.8 to 7.2. The low pH
data in Table 1 indicate that both feedstocks are suitable substrates for
recorded for food waste could be attributed to the possible presence of
biogas production.
protein- and carbohydrate-containing food materials which can be
respectively converted to amino acids and monosaccharides which are
in turn converted to volatile fatty acids during the AD process (Pramanik 3.2. Co-digestion studies
et al., 2019). Zhang et al. (2018) and Shamurad et al. (2020) also re­
ported low pH values of 3.5 and 4.3 respectively for food waste. The low Daily biogas production data for different co-digestion ratios of cattle
pH value of food waste recorded in this study is however not a problem rumen content and food waste (CRC: FW) (0:100, 20:80, 40:60, 50:50,
as co-digestion of food waste with a suitable substrate is known to buffer 60:40, 80:20 and 100:0) are shown in Fig. 1. Biogas production began
the pH value to desirable levels. For instance, Zou et al. (2020) was able immediately on the first day of digestion for both the mono-digestions
to buffer the pH value of food waste from 5.2 to around 6.3–7.2 by co- (100:0 and 0:100) and co-digested substrates (20:80, 40:60, 50:50,
digestion with corn cob. 60:40, 80:20). For mono-digested CRC, the maximum daily biogas
The carbon to nitrogen ratio (C/N) determined from the elemental production was recorded as 13.20 ml/gVS on the 25th day of digestion.

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N.A. Ihoeghian et al. Bioresource Technology Reports 18 (2022) 101033

100 100:0% 0:100% 80:20% 60:40%

16000
14000 50:50% 40:60% 20:80%
80

Total VFA (mg/l)

12000
Volatile solids (%TS)

10000
60
8000

40 6000
100:0% 0:100% 80:20% 4000
20 60:40% 50:50% 40:60% 2000
20:80% 0
0 0 7 14 21 28 35 42
Retention time (days)
0 7 14 21 28 35 42
(a)
Retention time (days)
7000 100:0% 0:100% 80:20% 60:40%
Fig. 3. Volatile solids profile for different co-digestion ratios (CRC:FW) [Error 50:50% 40:60% 20:80%
6000
bars indicate standard deviations (n = 3)].
5000

TAN (mg/l)
4000
100:0% 0:100% 80:20% 60:40%
7.0 3000
50:50% 40:60% 20:80%
6.5
2000
6.0
1000
5.5
pH

0
5.0
0 7 14 21 28 35 42
4.5 Retention time (days)
4.0 (b)
3.5
Fig. 5. Time trajectory of (a) total VFA concentration and (b) total ammonia
3.0 nitrogen concentration for different co-digestion ratios [Error bars indicate
standard deviations (n = 3)].
0 7 14 21 28 35 42
Retention time (days)

Fig. 4. pH profile for different co-digestion ratios (CRC:FW) [Error bars indi­ that do not share letters are significantly different (Fig. S3 in supple­
cate standard deviations (n = 3)]. mentary materials). As indicated in the Figure, co-ratios of 80:20, 100:0,
and 60:40 all share group “B”, 60:40 and 40:60 share group “C”, while
For mono-digested FW, the maximum daily biogas production was 40:60, 20:80 and 0:100 share group “D”, all indicating there are no
recorded as 19.14 ml/gVS on the 6th day of digestion. The maximum significant differences between them. However, co-digestion ratio 50:50
daily biogas production was found to increase when both substrates (“A”) did not share a letter with any other ratio implying that it was
were co-digested with values of 27.50, 30.20, 22.07, 27.93 and 19.80 significantly different from the other co-ratios.
ml/gVS recorded for CRC:FW ratios of 50:50, 60:40, 80:20, 60:40 and The time trajectory of volatile solids in the course of digestion for the
40:60 on the 7th, 11th, 18th, 34th and 13th day of digestion mono- and co-digested substrates showed a general progressive down­
respectively. ward trend observed across all co-digestion ratios (Fig. 3). This is
Fig. 2 shows the cumulative biogas production for both mono- indicative of the conversion of the material to produce biogas. A similar
substrates and co-digested substrates. As mono-digested substrates, trend was observed for the profile of the total solids (Fig. S4 in supple­
CRC and FW yielded a total cumulative biogas production of 262.43 and mentary materials). The trend of reduction in both VS and TS correlated
222.45 ml/gVS respectively after 42 days of digestion. Across the with biogas production as shown in Fig. 2.
digestion days, it was found that biogas production increased as the The profile of pH of the digestion for the 42 days retention time is
proportion of CRC in the co-substrate increased. However, the co- shown in Fig. 4. The initial pH values of CRC and FW were 6.86 and 4.12
substrate with CRC content of 50% was seen to be optimal with a respectively. Co-digestion raised the pH of the co-substrates and this can
maximum biogas yield of 320.52 ml/gVS. In addition, increasing the be seen in the fact that at the start of digestion, co-substrates having
CRC content beyond 50% resulted in a decrease in biogas production higher proportions of CRC also had higher pH values (6.61 for 80:20)
(Fig. S2 in supplementary materials). Thus, the 50:50 ratio of CRC to FW and vice versa (4.78 for 20:80). There was an observed general drop in
could be seen to be the best ratio for maximum biogas production. pH across all co-digestion ratio for the first 21 days of digestion. This
Overall, co-digestion of CRC and FW was seen to increase biogas pro­ could be attributed to the accumulation of VFAs in the digestion medium
duction compared to mono-digestion indicating some positive synergy. from the conversion of the readily degradable materials, an observation
No previous studies have reported co-digestion of CRC and FW; how­ that is correlated by the data in Fig. 5a. However, beyond 21 days, there
ever, the maximum biogas production (320.52 ml/gVS) obtained here is was an increase and a subsequent stabilization in pH values for the
higher than that (262 ml/gVS) reported by Kaur and Kommalapati remainder of the digestion period which could indicate the conversion of
(2021) for a 20:80 co-digestion of goat manure and cotton gin trash and the VFAs to methane. The continuous production of biogas could be
250 ml/gVS reported by Alfa et al. (2020) for the 25:75 co-digestion of attributed to the acclimatization of the microorganisms to the low pH
cow dung and horse dung. conditions. This could be as a result of the fact that the microbial
The percentage methane composition for the various co-digested community in the AD system was indigenous to the feedstocks. It has
substrates was measured and the mean values were recorded. A one- been reported that methanogenic microorganisms such as Meth­
way ANOVA showed that there was a significant difference between anosarcina termofilicia, Methanosarcina barkeri, Methanosarcina mazei
the compositions with a p-value of 0.00000036. The Tukey pairwise and Methanosarcina vacuolata in natural ecosystems can produce biogas
comparison was then used to compare the mean compositions. Means at pH values as low as 3.8 (Duval and Goodwin, 2000) and 4 (Taconi

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N.A. Ihoeghian et al. Bioresource Technology Reports 18 (2022) 101033

Table 2 Table 3
Biomethane potential and co-digestion performance index of mono- and co- Parameters for kinetic models.
digested substrates. Model Parameter Value
CRC: Empirical C/N TMY CBY CMY (ml CPI
First order k (1/d) 0.0000030
FW formula (ml/ (ml/ CH4/gVS)
Pm (ml/gVS) 3,485,432.82
gVS) gVS)
Fitzhugh k (1/d) 0.028
0:100 C18.1H29.2O13.3N 18.06 427.06 216.52 112.78 – n 1.36
20:80 C18.3H30.6O13.0N 18.33 445.30 226.81 121.96 9.4 Pm (ml/gVS) 309.79
40:60 C19.3H33.5O13.1N 19.29 466.03 239.85 132.24 2.2 Modified Gompertz λ (d) 1.93
50:50 C22.5H35.9O14.8N 22.53 469.28 274.76 173.08 2.3 Rmax (ml/gVS/d) 20.30
60:40 C22.8H38.7O15.3N 22.79 472.97 247.99 148.17 1.9 Pm (ml/gVS) 274.08
80:20 C23.7H42.8O14.8N 23.65 508.82 247.47 131.53 2.0 Cone k (1/d) 0.070
100:0 C27.6H47.1O18.1N 27.65 486.15 256.36 133.05 – n 1.45
Pm (ml/gVS) 395.82
CBY = cumulative biogas yield; CMY = cumulative biomethane yield.
CBY for 50:50 ratio = 320.52 ml/gVS.

et al., 2008). These authors attributed their observations to the accli­

matization of methanogens to low pH conditions. substrates and their corresponding empirical formulas are shown in
In Fig. 5a, there was an initial increase in the total VFA concentration Table 2. The CPI was used to assess the synergistic effect of the in­
in the digestion medium during the first two weeks of digestion. This is teractions between the co-substrates during co-digestion. The CPI
because volatile fatty acids are produced from the breakdown of organic ranged from 1.9 for the 60:40 ratio to 9.4 for the 20:80 ratio of CRC to
materials during digestion. Excessive accumulation of VFAs in the FW. All the co-digestion ratios had CPI values greater than one indi­
digester can cause digester instability, which, if left unchecked, can ul­ cating beneficial synergistic effects of co-digestion. The co-digestion of
timately lead to a shutdown of the process. From the second week of food waste with cellulosic materials such as spent coffee grounds (Jinsu
digestion, the total VFA concentration began to decline. The reduction in Kim et al., 2019b) and toilet paper (Jaai Kim et al., 2019a) yielded CPI
total VFA concentration also correlated with the increase in pH recorded values in the range of 1.05 to 1.30. In comparison, Wang et al. (2019)
after the second week of digestion as shown in Fig. 4. The digester with reported a slightly higher CPI value of 1.9 for a co-substrate made up of
50% CRC and 50% FW was seen to be able to maintain system stability pig manure, corn stover and cucumber residues. The same CPI value
as it had the lowest total VFA accumulation with respect to digestion (1.9) was reported by Okoro et al. (2018) for the co-digestion of oat
time and this observation could explain the reason for the best biogas straw and cow manure. However, Kaur and Kommalapati (2021) re­
production data recorded, as shown in Fig. 2. Although the digesters ported CPI values of 8.8 and 9.8, respectively, for 60:40 and 10:90 co-
with the other co-digestion ratios recorded higher total VFA accumu­ digestion ratios of goat manure and cotton gin residue, which are
lation, biogas production was not severely inhibited as the total VFA close to that reported in this work.
accumulated for all the co-digestion ratio was less than the inhibitory
limit of 18,000 mg/l reported by Zheng et al. (2015). Some studies have
reported higher total VFA concentration as high as 20,000 mg/l with no 3.4. Kinetic modeling
inhibition when digesting feedstocks such as municipal solid waste and
vegetable waste (Aymerich et al., 2013). However, to operate at such Having established 50:50 as the optimum co-digestion ratio, the
high VFA levels and yet maintain process stability, it is necessary to biogas production data for that same ratio were fitted to four kinetic
maintain corresponding high alkalinity to prevent acidification of the models namely first order, Fitzhugh, modified Gompertz and Cone.
digester (Riggio et al., 2017). These models are commonly used for assessing the kinetics of biogas
The trend observed for total ammonia nitrogen for the different co- production from organic materials. The kinetic parameters and their
digestion ratios is shown in Fig. 5b. There was a general downward values for these models are presented in Table 3. The first order kinetic
trend for TAN in the course of digestion. Syaichurrozi et al. (2018) re­ model estimated a rate constant of 0.0000030 1/d and a predicted
ported that a substrate with more nitrogen content will potentially result biomethane yield of 3,485,432.82 ml/gVS which is very large when
in the production of more TAN. According to Rajagopal et al. (2013), a compared to the actual experimental value of 320.52 ml/gVS obtained
TAN concentration in the range of 50–200 mg/l is beneficial for mi­ for the 50:50 co-digestion ratio. This is an indication of the inability of
crobial activity. the first order equation to model biogas production. The first order ki­
However, if the TAN accumulation is too high, it can result in inhi­ netic model is useful for extracting kinetic information relating to the
bition of microbial growth and survival. Niu et al. (2013) put the upper rate of degradation and biomethane production. Despite its usefulness, it
limit of TAN concentration that can introduce nitrogen inhibition at has been reported that it might be unable to adequately model every AD
16,000 mg/l. A look at the data in Fig. 5b shows that there was no TAN process because it is only valid when the substrate surface is rate limiting
inhibition as the values of TAN during the course of the 42 days of and the formation of intermediate products is not taken into consider­
digestion were below the threshold limit. Similar observations were ation. The Fitzhugh model is an extension of the first order model with
reported by Riggio et al. (2017) for the co-digestion of animal bedding the introduction of the constant n. The Fitzhugh model predicted a rate
and food waste. The trend of TAN in over course of the 42 days of constant of 0.028 1/d and a simulated biomethane yield of 309.79 ml/
digestion was similar to that observed for total VFA (Fig. 5a). Similar to gVS which is close to the experimental value of 320.52 ml/gVS. These
VFA reported, the 50:50 co-substrate was the most stable as it consis­ values were similar to those obtained with the cone model (k = 0.070 1/
tently recorded the lowest accumulation of TAN throughout the diges­ d, Pm = 395.82 ml/gVS). In theory, a high k value is indicative of a fast
tion period. The correlation between VFA and TAN has also been degradation process. The k values obtained in this work are close to
previously reported by Niu et al. (2013). those reported by Cai et al. (2019) for a mixed substrate of vegetable
wastes. The modified Gompertz model predicted a lower biomethane
yield (274.08 ml/gVS) than the experimental value of 320.52 ml/gVS.
3.3. Biomethane yield and co-digestion performance index The constant (λ) indicates the lag phase (the time needed for the mi­
crobial community to acclimatize to the digester environment before
The theoretical biomethane yield (TMY), experimental cumulative biogas production can begin). Typically, digesters with smaller values of
biomethane yield (CMY), experimental cumulative biogas yield (CBY) λ indicate that the microbial community needed little time for adapta­
and co-digestion performance indices for the mono- and co-digested tion in the digester. On the basis of the results obtained from the

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N.A. Ihoeghian et al. Bioresource Technology Reports 18 (2022) 101033

Table 4 dairy manure and crude glycerol.

Goodness of fit statistics for kinetic models. The accuracy of the predictions of all four models was assessed using
Parameter Model statistical indicators, and the results are shown in Table 4. The desirable
situation is to have a model with an R2 and adjusted R2 value that is as
First order Fitzhugh Modified Gompertz Cone
close to unity as possible while the error terms should be as small as
R2 0.938 0.986 0.950 0.992 possible (Amenaghawon et al., 2021). Although all the models were
MSE 1068.297 116.270 438.092 62.972
RMSE 32.685 10.783 20.931 7.935
characterized by high R2 values, the cone model outperformed the
SEP 17.280 5.297 10.392 3.893 others with the highest R2 value of 0.992. In addition, the cone model
MAE 26.498 9.025 17.064 6.840 was characterized by the smallest magnitude of all the error terms used
AIC 250.858 175.790 222.218 154.328 to assess the accuracy of the models. This was followed by the Fitzhugh
model which had an R2 value of 0.986 and relatively low error values.
The first order model performed the poorest as it had the lowest R2 value
modified Gompertz model, the lag phase was 1.93 days. Cai et al. (2019)
and highest error values. On the basis of the Akaike's information cri­
reported lag times in the range of 1.1 to 4.3 days for the digestion of
terion, the performance of the models can be ranked as cone > Fitzhugh
vegetable wastes while Gu et al. (2020) reported a range of 2.7 to 4.2
> Modified Gompertz > first order.
days for co-digested food waste and sewage sludge. The relatively short
The experimental and predicted biogas yields obtained for the first
lag time recorded in this study is indicative of the fact that the microbes
order model are shown in Fig. 6a. There was a poor correlation between
in the feedstocks were able to adapt easily for the AD process to begin
the experimental and predicted biogas production data as seen in the
biogas production. This also supports the observation that biogas pro­
very significant deviation observed in the data. The same observation
duction began almost immediately after the digesters were set up
was recorded for the parity plot of Fig. 6b. In the ideal case of a perfect fit
(Fig. 1). The Rmax value of 20.30 ml/gVS/d was within the range re­
between the experimental and model predictions, all the data points in
ported by Orangun et al. (2021) for food waste and goat manure.
Fig. 6b should cluster along the 45o line indicating perfect agreement
Andriamanohiarisoamanana et al. (2018) reported Rmax values in the
between both sets of data. This was however not the case with the
range of 20 to 60 ml/gVS/d for the co-digestion of meat, bone meal,
predictions of the first order model. This situation is also supported by

400
Predicted gas production (ml/gVS)

Exp 350
350
Cumulative biogas (ml/gVS)

Model 300
300
250
250

200
200

150 150

100 100

50 50

0 0
0 5 10 15 20 25 30 35 0 40 80 120 160 200 240 280 320
Retention time (days) Actual gas production (ml/gVS)
(a) (b)
350 320
Predicted gas production (ml/gVS)

Exp 280
300 Model
Cumulative biogas (ml/gVS)

240
250
200
200
160
150 120
100 80

50 40
0
0
0 40 80 120 160 200 240 280 320
0 5 10 15 20 25 30 35
Actual gas production (ml/gVS)
Retention time (days)
(c) (d)
Fig. 6. Comparison of experimental and predicted biomethane yield (a) time trajectory for first order model (b) parity plot for first order model (c) time trajectory for
Fitzhugh model (d) parity plot for Fitzhugh model (e) time trajectory for modified Gompertz model (f) parity plot for modified Gompertz model (g) time trajectory for
cone (h) parity plot for cone model.

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N.A. Ihoeghian et al. Bioresource Technology Reports 18 (2022) 101033

350 320

Predicted gas production (ml/gVS)

Exp 280
300

Cumulative biogas (ml/gVS)

Model
240
250
200
200
160
150
120
100 80
50 40

0 0
0 5 10 15 20 25 30 35 0 40 80 120 160 200 240 280
Retention time (days) Actual gas production (ml/gVS)
(e) (f)
320
350

Predicted gas production (ml/gVS)

Exp
280
Cumulative biogas (ml/gVS)

300 Model
240
250
200
200 160
150 120
100 80

50 40
0
0 0 40 80 120 160 200 240 280 320
0 5 10 15 20 25 30 35
Actual gas production (ml/gVS)
Retention time (days)
(g) (h)

Fig. 6. (continued).

the fact that the first order model had the lowest R2 value (0.968) among conditions. The AD process can be described by the cone model with
all the models considered (Table 4). The data for the Fitzhugh model very excellent statistical metrics. Co-digested CRC and FW could serve as
(Fig. 6c) showed a significant superiority over the first order model as suitable feedstocks for sustainable biogas production.
seen in the better fit and correlation, both in terms of the time trajectory
and parity plot. Among all the models, the cone model showed the best Funding source
performance as seen in the almost perfect fit between the trends of the
experimental biogas yields and model predictions (Fig. 6g). In addition, This research work was supported by the UKRI Collective Fund
the data points comparing the experimental and model predictions in award UKRI GCRF RECIRCULATE: Driving eco-innovation in Africa:
the parity plot were almost all aligned along the 45o line, indicating Capacity-building for a safe circular water economy [Grant Ref.: ES/
excellent agreement between both sets of data (Fig. 6h). This is also P010857/1].
corroborated by the fact that the cone model had the highest R2 value
and lowest error values among all the models considered (Table 4). Availability of data and material
Thus, the cone model can be used to adequately predict biogas pro­
duction for a 50:50 co-digestion of cattle rumen content and food waste. All data generated or analyzed during this study are included in this
The excellent predictive capacity of the cone model was also reported by published article or in the supplementary material.
El-Mashad, (2013) and Karki et al. (2022).
CRediT authorship contribution statement
4. Conclusion
Newton Ihoeghian: Experiments, Data analysis, Writing. Andrew
This study has shown that a co-substrate of CRC and FW has more Amenaghawon: Conceptualization, Methodology, Writing- Original
desirable properties for AD compared to the mono-substrates. A 50:50 draft preparation, Reviewing and Editing. Mike Ajieh: Reviewing and
ratio of CRC and FW is best for biogas production. Co-digestion can Editing. Cyprian Oshoma: Reviewing and Editing. Nosakhare
stabilize the AD process with visible impacts on pH, VFA and TAN Erhunmwunse: Reviewing and Editing. Abraham Ogofure: Method­
accumulation. Biogas production is possible at low pH values as evident ology, Reviewing and Editing. Valerie Edosa: Reviewing and Editing.
in the maximum biogas yield of 320.52 ml/gVS recorded under acidic Isioma Tongo: Reviewing and Editing. Ifeyinwa Obuekwe: Reviewing

8
N.A. Ihoeghian et al. Bioresource Technology Reports 18 (2022) 101033

and Editing. Ebuwa Isagba: Reviewing and Editing. Christopher wastes. Int. J. Agric. Biol. Eng. 12, 154–159. https://doi.org/10.25165/J.
IJABE.20191203.4705.
Emokaro: Supervision, Reviewing and Editing. Lawrence Ezemonye:
Capson-Tojo, G., Rouez, M., Crest, M., Trably, E., Steyer, J.P., Bernet, N., Delgenès, J.P.,
Supervision, Reviewing and Editing. Alfonso Lag-Brotons: Reviewing Escudié, R., 2017. Kinetic study of dry anaerobic co-digestion of food waste and
and Editing. Kirk Semple: Supervision, Reviewing and Editing. Alastair cardboard for methane production. Waste Manag. 69, 470–479. https://doi.org/
Martin: Supervision, Reviewing and Editing. 10.1016/J.WASMAN.2017.09.002.
Charnier, C., Latrille, E., Lardon, L., Miroux, J., Steyer, J.P., 2016. Combining pH and
electrical conductivity measurements to improve titrimetric methods to determine
ammonia nitrogen, volatile fatty acids and inorganic carbon concentrations. Water
Declaration of competing interest Res. 95, 268–279. https://doi.org/10.1016/J.WATRES.2016.03.017.
Chuenchart, W., Logan, M., Leelayouthayotin, C., Visvanathan, C., 2020. Enhancement
of food waste thermophilic anaerobic digestion through synergistic effect with
The authors declare that they have no known competing financial chicken manure. Biomass Bioenergy 136, 105541. https://doi.org/10.1016/J.
interests or personal relationships that could have appeared to influence BIOMBIOE.2020.105541.
the work reported in this paper. Duval, B., Goodwin, S., 2000. Methane production and release from two New England
peatlands. Int. Microbiol. 3, 89–95.
El-Mashad, H.M., 2013. Kinetics of methane production from the codigestion of
Acknowledgment switchgrass and Spirulina platensis algae. Bioresour. Technol. 132, 305–312.
https://doi.org/10.1016/J.BIORTECH.2012.12.183.
El-Mashad, H.M., Zhang, R., 2010. Biogas production from co-digestion of dairy manure
The authors gratefully acknowledge the assistance of the staff of the and food waste. Bioresour. Technol. 101, 4021–4028. https://doi.org/10.1016/J.
Vegetable Market abattoir at Airport road in Benin City, Nigeria for BIORTECH.2010.01.027.
Ezechi, E.H., Nwabuko, C.G., Enyinnaya, O.C., Babington, C.J., 2017. Municipal solid
providing the cattle rumen content used in this study. waste management in Aba, Nigeria: challenges and prospects. Environ. Eng. Res. 22,
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Appendix A. Supplementary data Glanpracha, N., Annachhatre, A.P., 2016. Anaerobic co-digestion of cyanide containing
cassava pulp with pig manure. Bioresour. Technol. 214, 112–121. https://doi.org/
10.1016/J.BIORTECH.2016.04.079.
Supplementary data to this article can be found online at https://doi. Gu, J., Liu, R., Cheng, Y., Stanisavljevic, N., Li, L., Djatkov, D., Peng, X., Wang, X., 2020.
org/10.1016/j.biteb.2022.101033. Anaerobic co-digestion of food waste and sewage sludge under mesophilic and
thermophilic conditions: focusing on synergistic effects on methane production.
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