Biomass and Bioenergy 141 (2020) 105693

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Biomass and Bioenergy

journal homepage: http://www.elsevier.com/locate/biombioe

Biogas production from chicken manure at different organic loading rates

in a mesophilic full scale anaerobic digestion plant
Linas Jurgutis, Alvyra Slepetiene, Jonas Volungevicius, Kristina Amaleviciute-Volunge *
Institute of Agriculture, Lithuanian Research Centre for Agriculture and Forestry (LAMMC), Instituto al.1, LT-58344, Akademija, Kedainiai Distr., Lithuania

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

Keywords: The objective of this work was to determine the potential of using chicken manure (CM) as a sole feedstock for
Biogas renewable biogas production under anaerobic conditions before spreading the digested chicken manure biomass
Chicken manure on the fields as an organic biofertilizer. The chicken manure samples from four different locations of Lithuania
Digestate
were analysed and compared in order to better understand the chemical composition of the locally generated
Energy
Nitrogen
biomass resource. The annual quantities of chicken manure produced were investigated allowing estimation of
Inhibition the biogas potential if such biomass was treated anaerobically. Laboratory biomethane potential (BMP) tests
performed indicated the biogas potential of methane – 508 mL CH4 g− 1 VS added and this result was compared
to biogas yields obtained in full scale anaerobic digestion plant using manure as a core substrate. Fermentation
process data analysis of anaerobic digestion performance indicates that the system is able to adapt even if the
same operational conditions, such as organic loading rate and retention time are applied. Once adapted, the
performance of biogas plant fermenter was able to deliver 93% of chicken manure biogas potential with an OLR
of 3.14 kg VS L− 1d− 1 and TAN concentration of 5.5 g L− 1. The results indicated that it is possible to digest
chicken manure as a stand-alone feedstock if ammonium concentration was carefully controlled via optimized
fresh water dilution process.

1. Introduction technology for the waste treatment approach.

In Lithuania, the national energy sector development strategy was
approved in 2018 with 35% of locally sourced electricity production by
2020 and approaching 100% by 2050 [1]. Biogas is expected to play a
ponderable role in reaching these electricity production targets. Due to
base load electricity production, abundance of local resources suitable
for anaerobic digestion (AD) process and advanced technology devel­
opment level, biogas power plants have the potential to expand
significantly.
Agricultural anaerobic digestion serves not only in electricity and
heat production, but also in production of nutrient rich digestate stream,
that is the side product of anaerobic digestion plant. As a side product for
energy produced (in the form of biogas), anaerobic digestion facilities
generate significant quantities of collateral biomass known as digestate
which is often recycled to soil as fertilizer [2,3]. Such holistic approach
when anaerobic digestion process is considered as both energy pro­
duction and quick release biofertilizer generation technology should
make the agricultural anaerobic digestion process the dominant
The national interest in biogas has resulted in 10 new agricultural
biogas plants in Lithuania since 2015. However, there are still many tons
of biomass suitable for biogas production unutilized in Lithuania.
Currently, chicken manure is not used at any biogas plant in Lithuania.
The literature suggests that digestate quality, which is comparable to
that of the raw substrate, has a lower total solids (TS) content than the
original substrate. However, this depends on the total solids content of
the original substrate [4]. It was found that treatment of chicken manure
under diluted anaerobic digestion conditions can produce biogas and
does not reduce biofertilizer value.
By 2017 there were 40 biogas plants operating in Lithuania, 30% of
them were agricultural biogas plants [5,34]. Only one biogas plant in
Lithuania was partially using chicken manure as the feedstock for the
limited time period and has switched to other feed stocks recently. The
feedstock portfolio change has been made due to the increased chicken
manure feedstock price, large amount of water needed for dilution and
other high operational expenses associated with chicken manure
digestion.

* Corresponding author.
E-mail address: kristina.amaleviciute-volunge@lammc.lt (K. Amaleviciute-Volunge).

https://doi.org/10.1016/j.biombioe.2020.105693
Received 24 January 2020; Received in revised form 2 July 2020; Accepted 23 July 2020
Available online 17 August 2020
0961-9534/© 2020 Elsevier Ltd. All rights reserved.
L. Jurgutis et al.
Increasing poultry breeding industry produces extensive amounts of
manure waste. In line with increasing intensive chicken farming, large
amounts of chicken manure biomass are being produced. It has been
estimated that world produces around 20 708 million tons, Asia pro­
duces 11 514 million tons and Europe produces about 2039 million tons
of chicken manure annually and only 30–40% to this manure is con­
verted into biogas by anaerobic degradation [6]. The technological
barriers of chicken manure limit its broader utilization for the renewable
energy generation purpose. It is due to the fact that chicken manure is
difficult to degrade into biogas efficiently [7]. According to EUROSTAT
data production of poultry in the EU-28 in 2018 was as follows: Poland –
16.8%, UK – 12.9%, France – 11.4%, Spain – 10.7%, Germany – 10.4%,
Italy – 8.5%, Hungary – 3.5% [8]. In China, about 155 million tons of
chicken manure are produced annually and this has the potential to
produce 3×1014 KJ energy [13].
The most common methods for managements of chicken manure
include the applications of this biomass for soil (land spreading of un­
processed manure, production of fertilizers and soil improvers) and for
production of biogas through anaerobic digestion [10]. The ideal con­
tent of C:N:P in fertilizer shall be 100:10:1. Therefore, utilization of
chicken manure as soil fertilizer require an additional source of carbon,
which would result in avoidance of nitrogen and phosphorus leaching.
Furthermore, mineral components potentially available to plants are
released gradually over 2–3 years, therefore, chicken manure cannot be
spread to given soil every year [10].
Treatment of chicken manure is important as phosphorus run off into
water bodies, nitrate leaching into ground water, green house gases and
release of pathogenic microbes are the main problems if chicken manure
was used without anaerobic digestion treatment as a fertilizer in
different crops [11]. However, the technological barriers of chicken
manure limit its broader utilization for the renewable energy generation
purpose. It is due to the fact that chicken manure is difficult to degrade
into biogas efficiently [7]. Moreover, ammonium inhibition resulting
due to increase ammonium in manure and limited techno-economic
viability of techniques used to remove it are an important aspect of
only one third of annual chicken manure bioenergy potential is pro­
duced via anaerobic fermentation [10].
Therefore, anaerobic digestion of chicken manure is an important
process to proper degradation when stabilizing organic matter along
with biogas production from chicken manure [10]. In this way this
biogas can be used for conversion of renewable heat and electricity and
the remaining organic matter produced after anaerobic degradation is
then sustainably applied as an agricultural fertilizer [12]. The organic
fraction of chicken manure is deemed to be a high biogas yielding
feedstock and so the anaerobic digestion of chicken manure is consid­
ered as a priority option to treat such waste and produce renewable
energy at the same time. Anaerobic digestion is a sustainable solution for
chicken manure management technology from the energy recovery,
biofertilizer production and greenhouse gas management points of view.
However, anaerobic digestion of chicken manure as the dominant sub­
strate in the biogas plant reactor feedstock mix has been problematic
due to its high nitrogen content [13,14], causing inhibition of anaerobic
digestion process when high organic loading rate is applied to the di­
gesters. Chicken manure has a higher nitrogen content than food waste,
cow manure, pig slurry or waste activated sludge [15].
Anaerobic digestion is a biological process which results in biogas
production and digestate generation. The dominant component of
biogas is methane gas. During anaerobic fermentation, methane is pro­
duced through two major metabolism pathways: acetate decomposition
or acetate oxidation and hydrogenotrophic methanogenesis. The effi­
ciency of those two pathways can be affected by the various stress fac­
tors such as ammonia inhibition. For example, it was reported that with
increasing total ammonium nitrogen (TAN) values in the digester
Methanoculleus was replaced by the genus Methanosarcina [13]. The
dominance of Methanosarcina under high TAN conditions may indicate
that it has higher tolerance under such stressed conditions. The authors
2
Biomass and Bioenergy 141 (2020) 105693
concluded that acetate oxidation and hydrogenotrophic methanogenesis
pathway dominant when chicken manure was digested at high free
ammonia nitrogen (FAN) and high organic loading rate (OLR) condi­
tions responding to the shift in the microbial community [13].
In recent years, researchers focus on enhancement of chicken manure
mass usage as the biogas production feedstock. The major methods
found in the recent publications of chicken manure digestion are co-
digestion with other organic feedstocks, chicken manure pre-treatment
and digestate post-treatment for the sake of ammonia stripping. In
terms of co-digestion, the suitable co-substrates for chicken manure
digestion is carbon rich biomass such as lignocellulosic biomass [6,16,
17]. However, due to the seasonality, local availability and the feedstock
market price, other wastes are still being sought that could be processed
together with chicken manure [8].
The effect of introducing external additives, such as microelements
[10,13] or activated carbon [11] was also studied. For example [10],
found that 280 mg/L Fe2+ and 2 mg/L Ni2+ supplements on chicken
manure addition demonstrated biomethane yield of 0.241 L gVS− 1
compared to reference digester of 180 L CH4 gVS− 1. Molaey et al., 2018
[13] researched Ni+2, Co+2, Mo+6, Se+4,W+6 impact for biogas yield as
chicken manure was digested as mono-substrate. Se+4 was identified as
the critical trace element for the stable anaerobic digestion of chicken
manure [13]. They also found that without trace element supplemen­
tation, severe acetic and propionic acid accumulation occurred, causing
the CH4 yield to decrease below 0.12 m3 kg− 1 of VS added [13].
Another promising method of effective chicken manure digestion is
dilution of manure feedstock through liquid digestate recirculation.
However, the ammonium nitrogen concentration should be reduced in
the recirculation stream and this is often done via ammonia stripping
process. Described in literature, efforts to mitigate the accumulation of
ammonia result in 0.250 L CH4 g− 1 of VS added production at total
ammonium nitrogen (TAN) concentration 5800 mg L− 1 and 0.187 L CH4
g− 1 of VS added production at TAN concentration 6800 mg L− 1 [18].
Niu et al., 2015 [19] demonstrated the process temperature impact
for chicken manure digestion. It was found that the tolerance of ther­
mophilic reactor on TAN was 8000 mg L− 1 with free ammonia 2000 mg
L− 1 compared to 16000 mg L− 1 (FAN 1500 mg L− 1) of mesophilic
reactor. biomethane production was 0.29 L g− 1 VSin. Furthermore,
mesophilic reactor was successfully recovered from seriously inhibition
of TAN 16 000 mg L− 1. In contrast, thermophilic reactor recovery was
failed. Mesophilic reactor was dominated by acetoclastic methanogens
compared with the thermophilic reactor. The functional bacteria com­
munity has a less diversity in the thermophilic reactor makes it more
susceptible to sudden changes in ammonia loading condition [19]. Such
results indicate that mesophilic temperature is more favourable for the
chicken manure digestion resulting in more stable fermentation process.
Some research has been focused on sole digestion of chicken manure
and detailed process analysis was made. Bayrakdar et al. 2017demon­
strated laboratory scale chicken manure digestion and stable biogas
production performance with the total ammonium nitrogen (TAN)
concentration maintained below 4.0 g L− 1 when operating with organic
loading rate of 3.56 g VSL− 1d− 1 [6]. The chicken manure co-digestion
and dilution with water were applied in order to control TAN levels in
the fermentation media. Another researcher increased the OLR to 5.3 g
VSL− 1d− 1 reaching free ammonia nitrogen (FAN) concentration of 770
mgL− 1 in the fermentation media and producing 390 mL g− 1 VS biogas
with biogas yield descending as OLR was increased further [20]. Bi et al.,
2019 [21] studied the temperature and OLR effect on biogas production
efficiency for chicken manure digestion and demonstrated that ther­
mophilic digestion caused ammonia inhibition influenced methane
production of 220 mL CH4 g− 1 TS for OLR of 1.6 g VSL− 1d− 1 and 94 mL
CH4 g− 1 TS for OLR of 2.5 kg VS m− 3 d− 1. Table 4 summarizes recent
results of chicken manure anaerobic digestion approach.
The strategies to overcome the ammonium inhibition recommended
in the literature are co-digestion, technical ammonium-ammonia strip­
ping and trace element addition [25]. Another strategy to dilute the
L. Jurgutis et al.
chicken manure with process water is often applied in full-scale anaer­
obic digesters. All of the above-mentioned strategies are effective and
mitigate the ammonia inhibition problem; however, they increase the
process complexity and significantly raise biogas plant operational
expenses.
Long term full scale mono digestion data of chicken manure is scarce.
Few information is available about full scale mono fermentation of
chicken manure in order to understand how to effectively manage the
chicken manure digestion process. Typically, as the anaerobic digestion
process disturbance resulting in (temporary) biogas production slow
down and methane composition drop happens, full scale biogas plant
operators apply re-inoculation strategy or over dilute the process with
fresh water stream. Such approach does not ensure fermentation media
adaptation to increased TAN environment and adaptation is postponed.
Furthermore, only few articles demonstrated recovery strategies and
system adaptation behaviour once reactor inhibition occurred.
The objective of this study was to evaluate chicken manure biogas
potential and to explore the full scale biogas plant digestion perfor­
mance in order to better understand the stability of chicken manure
digestion process and full scale anaerobic digestion system recovery
strategy.
2. Materials and methods
2.1. Chicken manure quality parameters
During 2018, chicken manure was collected from several chicken
farms located in Lithuania. The farm size ranged from small scale (1–50
chicken heads), to medium scale (150 000–250 000 chicken heads), up
to large scale (900 000–1 000 000 chicken heads). Before the biogas
potential analysis tests were performed, chicken manure (CM) samples
were measured in terms of total solids (TS), volatile solids (VS), Total
Kjeldahl nitrogen (TKN), Phosphorus (P), Potassium (K), organic carbon
(OC), pH and ammonium nitrogen (N–NH4). CM samples were homog­
enized with a laboratory blender while mixing the biomass deionized
water to 15% TS. The samples were stored at 5 ◦ C and further used for
biogas potential analysis experiments.
2.2. Batch biogas potential experiments
The biochemical methane potential of the seven CM samples was
determined by the Automatic Methane Potential Test System (AMPTS II,
Bioprocess control, Sweden). The inoculum digested sludge was used
from full scale biogas plant co-digesting pig slurry with ensiled beet root
pulp biomass. The total reactor volume was 500 mL while working
volume was 400 mL. The chosen inoculum to substrate ratio was 2 on g
VS basis. The inoculum was stored at ambient temperature and incu­
bated at 35 ◦ C before the batch biogas tests launch. The reactors were
adjusted with distilled water in order to have the same test volumes. The
headspace of reactors was flushed with nitrogen gas. The tests were
carried out in triplicates and operating temperature was set at meso­
philic conditions (35 ± 1 ◦ C). The incubation period was set to 40 days.
Biogas produced passed through gas flow meter counter (Ritter TG 05
miligas counter, Ritter Apparatebau GmbH & Co., Germany) and then
CO2 was removed by passing through sodium hydroxide solution.
Methane yield was determined by AMPTS system’s gas flow meter.
2.3. Full scale anaerobic digestion experiment
Valuable data were obtained during full scale anaerobic digestion of
chicken manure in 400 kW power capacity biogas plant located in
eastern part of Lithuania. A single digestion tank reactor with a working
volume of 2500 m3 was operated continuously at 35 ± 1 ◦ C with four
mixers stirring once every hour for 15 min mixing interval. The duration
of the experiment was 217 days. The experiment was started after the
digester had been running under stable conditions. The biogas plant
3
Biomass and Bioenergy 141 (2020) 105693
operator did not indicate the exact origin of chicken manure since it was
delivered from 4 chicken farms located in Lithuania. Chicken manure
feedstock was delivered at the same quantities and was fed once mixed
with the same proportions during all the experimental period. The
experiment could not be continued further since the biogas plant oper­
ator changed the feeding mix to other biomass partly replacing CM as a
mono substrate due to a cheaper feedstock identified on the market.
2.4. Chicken manure analyses
The total solids (TS) of the CM samples were evaluated after drying
to a constant weight at 105 ◦ C. Volatile solids (VS) were determined by
loss on ignition at 550 ◦ C for 24 h. The pH of CM was measured by
homogenization followed by deionized water extract (1:5 w/v) appli­
cation. Ammonium nitrogen was measured by a spectrophotometer at a
wavelength of 550 nm with the cuvette test LCK 302 (HACH Lange,
Germany) using the standard procedure. The total Kjeldahl nitrogen
content was evaluated in the fresh chicken manure samples.
The organic carbon content was determined after wet-combustion by
a spectrophotometric measurement at a wavelength of 590 nm using
glucose as the standard according to the Nikitin-modified Tyurin
method (Nikitin, 1999) [26].
The total phosphorus concentrations were quantified spectrophoto­
metrically by a colour reaction with an ammonium molybdate vanadate
reagent at a wavelength of 430 nm on a Cary 60 UV–vis spectropho­
tometer (Varian Inc., USA), and the total potassium content was deter­
mined using the flame atomic absorption spectrometry measurement on
Analyst 200 (PerkinElmer, USA) after the wet digestion process with
sulfuric acid.
2.5. Anaerobic digestion process analyses
Digestates from full scale anaerobic digestion process were centri­
fuged at 10 000 rpm at 10 ◦ C for 10 min (16R H. Megafuge, Thermo
Scientific, USA) and the supernatant was used for volatile fatty acids
(VFA) analysis. VFA/TAC analyses were made by automatic titration
with 0.1 mol L− 1 H2SO4 to pH 5.00, 4.30, 4.00 using a Titrator T90
(Mettler Toledo International Inc., Switzerland) according to the to the
method [27].
VFA were calculated:
( ) NH SO NH SO
VFA = 131340 × VpH4.00 − VpH5.00 × 2 4 − 3.08 × 1000 × VpH 4.30 × 2 4
VPR VPR
− 10.9
VPR – centrifuged sample volume, mL
NH2SO4 – normality of the acid, mol L− 1
VpH X – volume of acid needed to endpoint pH x, mL
FAN is the concentration of free ammonia nitrogen in the digester in
g L− 1. FAN was calculated:
⎛ ⎞
⎜ 10− pH ⎟
FAN = TAN × ⎝1 + ⎠
10− ( 0.09018 + 2729.92
T(K)
1
TAN – concentration of N–NH4, g L−
T (K) – temperature, Kelvin
The ratio of full scale CH4 yield to biomethane potential yield was
used to determine the performance caused by industrial operational
conditions. The following formula was used for efficiency calculations:
%CH4 × Vbiogas
η, % =
BMPCM × mCM
L. Jurgutis et al.
% CH4 – methane content in the biogas
Vbiogas – volume of biogas produced, m3 d− 1
BMPCM– biomethane potential determined in this research, m3 CH4
t− 1
mCM – chicken manure fed daily to the digester, t
2.6. Gas volume and composition analysis
Gas composition was measured during a fixed hour on a daily basis.
The concentration of CH4 was measured using a Sewerin Multitec 540
device, allowing measurement of methane (0.0–100%), carbon dioxide
(0–100%), oxygen (0.0–25%), hydrogen sulphide (0–2000 ppm), and
carbon monoxide (0–500 ppm). Gas composition measurement was
measured every week using standard etalon gases provided by a Lithu­
anian company with a standard mixture of 65% CH4 and 35% CO2.
Volumetric biogas production was registered by a Kohne OPTISONIC
7300 Biogas flow meter.
3. Results and discussion
3.1. Chicken manure quantity and quality
The number of chicken birds farmed in Lithuania increased by 86%
from 2000 to 2019 (Table 2).
Scarlat et al., 2017 [29] estimated the 9.5 million chicken birds in
Lithuania in 2013.
According to Juška (2017) [30], it is estimated that feeding per day is
about 0.115–0.1177 kg of feed and about 13% of the feed’s nutrient
conversion yields to product. The amount of excrement produced per
day is 0.158 kg. This number is higher than that reported by other au­
thors in literature [31] 0.11 kg day-1, while Food and Agriculture Or­
ganization (FAO) [32] estimates of the manure excreted by 1 bird per
Fig. 1. Amounts of chicken manure accumulated in Lithuania in 2019.
4
Biomass and Bioenergy 141 (2020) 105693
day (based on average daily live weights during the birds’ production
cycle) are approximately 0.12 kg for layer chickens, 0.08 kg for meat
chickens. Additionally, personal communications of the biggest layer
chicken farm in Lithuania indicated the daily manure production of
0.082 kg per single bird. Therefore, the annual manure production
estimation of 29.2 kg was used in this research paper. The abundance of
available Lithuanian chicken manure makes this biomass an attractive
feedstock for biogas energy production.
The latest data of chicken manure quantities and their distribution
according to the counties are shown on the map (Fig. 1). According to
logically reasonable chicken manure transportation distances, it is most
advantageous to use chicken manure in the anaerobic digestion power
plants operating in Vilnius, Šiauliai, Panevėžys districts. The largest
quantities of chicken manure are concentrated closer to the Vievis
anaerobic digestion power plant.
The uneven distribution of chicken manure in municipalities is
determined by the territorial differentiation of poultry farming in
Lithuania. The system of poultry farming consists of small breeders of
poultry, poultry farms and poultry yards. Small poultry breeders
specialize in the production of different species of poultry, while the vast
majority of poultry farms are focused on hen production. Poultry yards
are also involved in hen production. Large poultry yards are located near
the largest cities of Lithuania (Vilnius, Kaunas, Panevėžys, Šiauliai,
Alytus), therefore the greatest amounts of chicken manure are generated
in these and the adjacent municipalities. Most of the chicken manure is
concentrated closer to the Vievis anaerobic digestion power plant (BP1).
Next to it, there are three large poultry yards, which collectively
generate 50 %of the total amount of chicken manure produced in
Lithuania per year (17957 t). The location of this plant is also favourable
from the geo-ecology viewpoint. The surrounding municipalities are
dominated by eroded soils (approx. 15–25% of the total agricultural
land) and, as a side product of chicken manure processing, digestate
becomes a valuable resource to be used for increasing soil organic matter
L. Jurgutis et al. Biomass and Bioenergy 141 (2020) 105693

and improving soil fertility. Table 2

The characteristics of seven different chicken manure samples are The number of chicken birds in Lithuania at the beginning of each year. Data
given in Table 1. from [28].
The variation of chemical parameters of the seven chicken manure County 2000 2005 2010 2015 2019
samples analysed indicates that chicken manure is an chemically un­ Vilnius 2 177 3066 3 280 3569 179 2 836
stable feedstock. The total solids and organic matter deviation can be 932 293 369 428
explained due to different bedding material used at the farms. Another Alytus 462 930 231 605 576 449 473 946 1 472
factor affecting TS, VS and other chemical parameters might be the 420
Kaunas 1 245 1919 2 380 3385 792 3 486
storage conditions as well as storage time of the chicken manure.
035 845 088 264
Chickens are uricotelic animals and they excrete uric acid as the nitro­ Klaipėda 580 179 635 624 447 991 391 835 571 408
gen removal channel. Once released into the atmosphere, uric acid is Marijampolė 306 247 212 946 182 989 77 072 71 033
gradually converted into ammonium via enzymatic transformations Panevėžys 287 796 665 950 616 018 1 029 1093 801
[37]. As uric acid to ammonium conversion occurs gradually, other 257
Šiauliai 409 851 433 410 371 862 218 249 839 275
biochemical metabolisms take place resulting in differences in manure Tauragė 151 288 153 613 144 763 56 063 217 175
chemical composition depending on the manure biomass age and Telšiai 377 755 646 004 708 146 644 132 737 582
environmental conditions. Utena 209 506 262 511 316 738 247 582 236 700
In total for 6 208 8227 9 025 10 093 11 562
Lithuania 519 801 413 107 086
3.2. BMP tests

The biomethane potential (BMP) test of the seven CM samples show

the variation of specific methane product within the range of 275–350 L Table 3
CH4 kg− 1 VS added. The results of BMP tests are reported in Table 3. It is Average biogas and biomethane production of seven chicken manure samples.
obvious that chemical composition of chicken manure affects BMP po­ Farm size, L biogas L CH4 % CH4 L biogas
tential significantly, resulting in the biogas production per quantity of thousand chicken kg− 1 VS kg− 1 VS kg− 1 FM
heads added added
fresh mass (FM) with 145 ± 57 L biogas kg− 1 FM). However, once the
BMP results were evaluated in terms of volatile solids fed into the biogas CM1 0.001–0.05 442 ± 8 275 ± 12 62.2 ± 166 ± 11
reactor, the methane production is similar between each CM tested 1.2
CM2 750–1000 514 ± 18 316 ± 17 61.5 ± 101 ± 13
resulting in 7.3% deviation (312 ± 23 L CH4 kg− 1 VS added). 0.7
The BMP results indicate that chicken manure under mesophilic CM3 750–1000 551 ± 14 350 ± 23 63.6 ± 126 ± 7
conditions can produce biogas with methane content of 61.5 ± 1.6%. 1.1
The obtained gas composition results are similar to those reported by CM4 750–1000 490 ± 15 309 ± 9 63.0 ± 97 ± 8
1.1
other researchers. Niu et al., 2013 [38] indicated 62% methane pro­
CM5 750–1000 535 ± 16 326 ± 8 61.0 ± 88 ± 9
duction during the early phase of experiment, while Nie et al., 2015 [13] 1.5
demonstrated the biogas quality of 64.4 ± 1.0% CH4 before inhibition CM6 500–750 524 ± 13 309 ± 11 59.0 ± 226 ± 11
and 58.9 ± 1.0% CH4 in the biogas during partly inhibited process due to 1.6
FAN concentration (0.58 g L-1) and high process OLR (6.0 g VSL− 1d− 1). CM7 500–750 497 ± 9 298 ± 12 60.0 ± 211 ± 12
1.1
Specific biogas production kinetic rate indicates that most of the Average 508 ± 18 312 ± 23 61.5 145 ± 13
biogas is produced during the first 10 days of anaerobic digestion and ± 1.6
the 95% of the obtained BMP potential is produced during the first 25
days of digestion incubation. The biogas production results are reported
in Fig. 2. The error bars represent standard deviation. The deviation of 3.3. Full scale anaerobic digestion process results
each chicken manure sample was lower than 10% during the first 15
days of experiment and the deviation decreased after 15 days of incu­ 3.3.1. Variation of biogas production and quality
bation. The reason for initial deviation within the chicken manure re­ The full scale anaerobic digestion process was analysed for 220 days.
actors might happen due to inhomogeneity of the biomass samples used. The experiment was divided into three stages: stable production (days
Another reason for the deviation might be the organic matter content of 0–22), unstable adaptation stage (days 22–67) and adapted new accli­
each chicken manure sample. However, the average deviation of mated conditions stage (days 67–217). Such division is based on biogas
methane production was 4% during 40 days of experiment, indicating production quantity during each experimental period. During the first
the representative and reliable biogas yield potential result. The biogas 22 days, 506 m3 of biogas per ton of loaded biomass was produced (m3
production started immediately with no lag phase in any of the tripli­ t− 1 VS in), while there was a significant drop in the biogas production as
cates, thanks to the inoculum obtained from the full scale anaerobic the adaptation period started reaching 451 m3 t − 1 VS in at the lowest
digestion plant treating pig slurry as the dominant biomass inlet stream. production point at experiment day 48. The biogas production recov­
ered since day 48 and kept increasing up to 495 at day 67 of the
experiment. The biogas production stabilized and produced 489 m3

Table 1
Chemical parameters of seven chicken manure samples collected in Lithuania.
Farm size, thousand chicken heads TS, % VS, % (TS) N, % (TS) P, % (TS) K, % (TS) Corg, % (TS) N–NH4, g/L pH

CM1 0.001–0.05 81.80 ± 1.75 45.90 ± 2.05 2.43 ± 0.04 1.52 ± 0.04 2.41 ± 0.11 27.00 ± 2.00 1.47 ± 0.23 8.30 ± 0.01
CM2 750–1000 31.60 ± 1.40 62.00 ± 1.76 4.37 ± 0.05 2.81 ± 0.02 2.81 ± 0.06 33.8 ± 1.70 8.05 ± 0.60 8.72 ± 0.03
CM3 750–1000 31.63 ± 0.92 72.10 ± 2.17 5.24 ± 0.02 1.53 ± 0.02 2.23 ± 0.03 38.02 ± 2.00 6.05 ± 0.45 7.28 ± 0.05
CM4 750–1000 32.75 ± 1.63 60.42 ± 2.62 3.26 ± 0.01 3.00 ± 0.05 2.20 ± 0.02 33.4 ± 1.40 5.76 ± 0.22 8.90 ± 0.02
CM5 750–1000 27.71 ± 1.13 59.50 ± 1.43 2.87 ± 0.14 2.32 ± 0.02 3.14 ± 0.01 32.76 ± 0.70 5.98 ± 0.45 9.20 ± 0.01
CM6 500–750 50.30 ± 0.75 85.88 ± 0.88 2.3 ± 0.07 1.97 ± 0.01 3.04 ± 0.03 50.21 ± 1.21 2.65 ± 0.11 8.01 ± 0.02
CM7 500–750 51.70 ± 1.50 82.09 ± 1.14 2.6 ± 0.12 1.99 ± 0.04 3.02 ± 0.01 45.61 ± 0.65 2.57 ± 0.11 7.90 ± 0.01
Average 43.93 66.84 3.30 2.16 2.69 37.26 4.65 8.33

5
L. Jurgutis et al. Biomass and Bioenergy 141 (2020) 105693

Table 4
Chicken manure anaerobic digestion brief literature review.
Method Proportion of Pretreatment Reactor Temperature Experiment Yield biomethane (Ym) or FAN or TAN Reference
substrates specifications duration, d yield biogas (Yb)

Co-digestion CM (laying No Lab scale, Mesophilic 240 d Ym 0.36 L g VS− 1 was TAN up to 6650 mg [6]
hens) and continuous, obtained when the TAN L− 1
spent poppy OLR: 2.78 to and FAN concentrations
straw 3.56 gVS were below 4000 and 300
4.3:1 w/w L− 1d− 1 mg L− 1 The results showed
that microbial consortia
were acclimated to high
ammonia concentrations
and a methane yield of
about 0.28 L g VS− 1 was
achieved up to 6100 mg
L− 1of TAN. When the TAN
concentration in the
digester increased above
6500 mg L− 1, the methane
yield sharply decreased
below 0.14 L g VS− 1
Co-digestion CM:WS WS-oxidative Lab scale n.d. 20 days Ym 0.297 L gVS− 1 TAN 1280 mg L− 1 [16]
cleavage with H2O2 OLR 1.5–4.5 Ym 0.170 L gVS− 1 FAN 49.9 mg L− 1
7.5% gVS L− 1d− 1
1
Co-digestion CM:CSI No pretreatment Lab scale n.d. 30 days Ym up to 0.356 L gVS− n.d. [17]
20:80, 30:70, Volume 2.5 L
40:60, 60:40 BMP assay
v/v
1
CM CM+ 1000W mircowave Lab scale 37 ◦ C 47 days OLR 1: Ym 0.123 L gVS− n.d. [22]
1
pretreatment activated pretreatment CSTR 0.4 L OLR 2: Ym 0.223 L gVS−
1
carbon +0.037–0.149 OLR 1: 3.5 gVS OLR 3: Ym 0.287 L gVS−
mmpowdered L− 1d− 1
activated carbon OLR 2: 4.7 gVS
pH of 5.0–7.0 L− 1d− 1
OLR 3: 5.8 gVS
L− 1d− 1
1 1
In situ CM Biogas pumping Lab scale, 37 ◦ C 194 d Ym 0.250 ± 0.014 L gVS− TAN 5800 mg L− [18]
ammonia rate of 15 s every 5 CSTR 12 L FAN
stripping min, and the biogas OLR 5.3 gVS 600 mg L− 1
flow rate was 2 L L− 1d− 1
min− 1.
1 1
Monodigestion CM No pretreatment Lab scale, 37 ◦ C 194 d Ym 0.187 ± 0.017 L gVS− TAN 6800 mg L− [18]
CSTR 12 L FAN
OLR 5.3 gVS 500 mg L− 1
L− 1d− 1
1
Monodigestion CM No pretreatment Lab scale, 35 ◦ C 30 d Ym 0.294 ± 0.002 L gVS− n.d. [23]
batch test,
Reactor
volume 0.12 L
1
Monodigestion CM No pretreament Lab scale, 37 ◦ C 93 d Ym 0.360 ± 0.010 L gVS− FAN 410 mg L− 1 [13]
CSTR 12 L TAN 2300 mg L− 1
OLR 1.8 gVS
L− 1d− 1 to 5.3
gVS
1 1
Monodigestion CM No pretreament Lab scale, 37 ◦ C 87 d Ym 0.340 ± 0.02 L gVS− FAN 1420 mg L− [13]
1
CSTR 12 L TAN 5000 mg L−
OLR 2.7 gVS
L− 1d− 1
1
Monodigestion CM No pretreament Lab scale, 37 ◦ C 193 d Ym 0.190 ± 0.02 L gVS− FAN 650 mg L− 1 [13]
CSTR 12 L TAN 6900 mg L− 1
OLR 5.3 gVS
L− 1d− 1
1 1
Monodigestion CM No pretreatment Lab scale, 37 ◦ C 100 d Ym 0.355 ± 0.026 L gVS− TAN 5634 mg L− [9]
CSTR 12 L
OLR 2.5 gTS
L− 1d− 1
Micro element CM+ 280 mg/L Fe2+ and Lab scale, 37 ◦ C 147 d Control digester: FAN 600 mg L− 1 [24]
supplements Fe2++Ni2+ 2 mg/L Ni2+ CSTR 12 L Ym 0.180 ± 0.009 L gVS− 1 TAN 6900 mg L− 1
supplements on OLR 4.8 gTS Fe–Ni digester:
chicken manure L− 1d− 1 Ym 0.241 ± 0.008 L gVS− 1
Micro element CM+ Ni+2, Lab scale 36 ◦ C 262 days Ym 0.27 ± 0.020 L g VS− 1 TAN 6560 ± 455 mg [10]
supplements Ni+2, Co+2, Mo+6, Volume 0.8 L L− 1
Co+2, Mo+6, Se+4,W+6 prepared OLR: 3.62 gVS
Se+4,W+6 in distilled water L− 1d− 1
Thermophilic CM No Lab scale Thermophilic 200 days Yb (0.74 m3 kg− 1VS) was TAN [19]
digestion Volume 12 L reactor 55 ◦ C harvested both in 60000 mg L− 1
1
pH 8.1 FAN 2118 mg L−
(continued on next page)

6
L. Jurgutis et al.
Table 4 (continued )
Method Proportion of Pretreatment Reactor Temperature
substrates specifications
Mesophilic
reactor 55 ◦ C
CM – chicken manure, WS – wheat straw, CSI – corn silage.
Fig. 2. Biogas production rate and kinetics.
biogas t− 1 VS during the rest of experimental period until day 217
(Fig. 3A).
Chicken manure was used as the sole source of organic matter during
the entire experimental period. Initially, the digester feeding organic
loading rate (OLR) was set to 2.24 kg/VS/m3/day and was kept stable
during the first 98 days of the experiment. After reaching stability and
due to biogas plant operator’s demand to produce more biogas per
reactor volume, it was decided to increase the OLR up to 3.14 kg VS/m3/
day after day 110 (Fig. 3B).
As shown in Fig. 3C, the gas composition varied during the different
stages of the experiment. Initially, methane content in produced biogas
was 60% until day 22, while during the second stage the methane
content in the biogas dropped to 51.1% (days 38–46) and slowly
recovered up to 59.2% at day 66. There was a second drop in the biogas
quality during days 112–137 reaching 53%. However, after day 66, the
methane content in the produced biogas was 58.5% and was considered
as stabilized biogas quality.
3.3.2. Process biological behaviour
During the experiment, the digester mass samples were analysed for
pH, VFA and N–NH4 on a weekly basis. On the 22nd day of the exper­
iment, inhibition was observed as the VFA level started to increase and
the biogas quantity as well as quality started to decrease. A sharp VFA
increase was observed during the unstable adaptation stage, reaching
the VFA peak of 10.82 g L-1 at day 43. Typically, one of the major reasons
of VFA increase caused by process imbalance is organic overloading as
the hydrolysis phase outperforms the methanogenic digestion phase
resulting in acetic and propionic acid accumulation in fermentation
media [20]. Another possible reason for symbiosis destruction might be
7
Biomass and Bioenergy 141 (2020) 105693
Experiment Yield biomethane (Ym) or FAN or TAN Reference
duration, d yield biogas (Yb)
thermophilic and Mesophilic reactor
mesophilic reactors has a higher
tolerance on TAN
than thermophilic
reactor. Mesophilic
reactor was
successfully
recovered
from seriously
inhibition of TAN 16
000 mg L− 1.
rapidly changed type of feedstock as the organic loading rate remains
the same but the deviation of feedstock degradation kinetics causes the
system overload. The reason of such imbalance might be complexed;
however, since the same chicken manure mix was fed at the fixed OLR,
the major cause of system imbalance should be considered accumulation
of ammonium nitrogen during VFA peak. The mechanism of VFA in­
crease can be provoked by stable total ammonium nitrogen (TAN) in­
crease in the digester, as TAN later is shifted to free ammonia nitrogen
(FAN) which is known to demonstrate inhibitory effects on the anaer­
obic digestion system [39,40]. FAN was 572 mgL− 1 and TAN 3.98 g L-1
at day 9 of the experiment, while FAN reached 686 mgL− 1 and TAN 5.01
g L-1 at day 58. However, this TAN level cannot be indicated as the
threshold level at which ammonium inhibition began, as this industrial
experiment was not designed to determine it.
Other authors have reported a wide range of ammonia inhibition
concentration ranging from 1.5 g L-1 to 7 g L-1 [41]. Such variation can
be explained by the ammonium-ammonia inhibition mechanism which
is highly dependent on the temperature and pH conditions of the
digester. In addition to that, the increased tolerance due to system
acclimatization is also the reason for different ammonium inhibition
research results provided in literature. Garcia et al., 2009 [42] reported
total inhibition of the methanogens at a FAN concentration of 250
mgL− 1 in an unacclimated anaerobic digestion system, while metha­
nogens can grow at a FAN concentration of 700 mgL− 1 once the system
is acclimatized. Acclimatization means adaptation of microorganism
populations to changed environment. The shift of methanogenic path­
ways with the increase of TAN and VFA levels are suggested as causes of
process imbalance and reduction in methane yields.
The physical factor effecting the FAN and TAN ratio is the
L. Jurgutis et al. Biomass and Bioenergy 141 (2020) 105693

Fig. 3. (A–G). Biogas production and quality.

8
L. Jurgutis et al.
temperature: reducing the temperature reduces the nitrogen transition
into the form of FAN. This is the reason why digester temperature was
gradually decreased from 40 ◦ C to 36 ◦ C at day 72 allowing the biogas
plant operators to control FAN concentrations in the digester (Figure F).
Reduced temperature allowed maintenance of the stable anaerobic
digestion performance with increased OLR.
3.3.3. Substrate utilization efficiency
The ratio of full scale methane yield to biomethane potential assessed
in the laboratory experiments was used as the performance efficiency
indicator for the analysis of industrial anaerobic digestion process and
evaluation of the adaptation phase performance. As can be seen in figure
G the significant drop in biomethane production efficiency started
approximately at day 25 reaching the lowest value of 71% at day 46 of
the experiment. The process operation temperature was gradually
reduced from 40 ◦ C to 35 ◦ C within 20 days’ period and the OLR was
kept stable of 2.24 kg VSL− 1d− 1. After day 46, the process recovery
started and substrate utilization efficiency increased gradually reaching
92% at day 66. The digester performance stabilized and as the OLR was
increased since day 100, another efficiency fluctuation was observed at
experimental day 124 reaching 82%. After day 150, substrate utilization
efficiency stabilized again producing 93% of the laboratory BMP results
with stable OLR of 3.14 kg VS L− 1d− 1.
4. Conclusions
This study applied biomethane potential (BMP) testing approach for
seven chicken manure samples sampled in Lithuania in 2018. The BMP
test showed that chicken manure is an attractive alternative source for
anaerobic digestion biogas plants due to the high biomethane potential
being able to produce 508 ± 36 mL biogas g− 1 VS. The results obtained
from the full scale anaerobic digestion plant from the 217 days’ opera­
tional period of chicken manure digestion as a mono substrate indicated
that there is time required for adaptation phase of the anaerobic
digestion process. This adaptation can be related to ammonium con­
centration in the fermentation media causing partial inhibition, which is
reflected in biogas volume as well as energy content reduction. How­
ever, the data analysis of anaerobic digestion performance indicates that
the system is able to adapt even if the same operational conditions, such
as organic loading rate and retention time are applied. Once adapted,
the performance of biogas plant fermenter was able to deliver 93% of
chicken manure biogas potential with a OLR of 3.14 kg VSL− 1d− 1 and
TAN concentration of 5.5 g L-1.
Finally, it would be useful to examine the shift of anaerobic popu­
lation during such adaptation and the response of process efficiency to
such microbial population changes. This controlled population shift
strategies could lead to improved digestion of high ammonium content
substrates under maximized biogas production quality and rates.
Funding
This paper presents the results of the research obtained through the
project “Quality diagnostics of biogas production by-product (digestate)
for innovative use as a biofertilizer” No. DOTSUT-217 (01.2.2-LMT-K-
718-01-0053) funded by the Research Council of Lithuania. The first
author acknowledges the funding of doctoral and research studies at
LAMMC.
Declaration of competing interest
We declared no potential conflicts of interest or personal relation­
ships that could have appeared to influence the work reported in this
paper.
9
Biomass and Bioenergy 141 (2020) 105693
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