PII: S0043-1354(98)00410-2
Wat. Res. Vol. 33, No. 8, pp. 1805±1810, 1999
# 1999 Elsevier Science Ltd. All rights reserved
Printed in Great Britain
0043-1354/99/$ - see front matter
IMPROVING THERMOPHILIC ANAEROBIC DIGESTION
OF SWINE MANURE
M
KAARE HVID HANSEN, IRINI ANGELIDAKI and BIRGITTE KIáR AHRING**
Department of Environmental Science and Engineering, Technical University of Denmark,
Building 115, DK-2800 Lyngby, Denmark
(First received January 1998; accepted in revised form September 1998)
AbstractÐThermophilic (558C) anaerobic degradation of swine manure was found possible even at an
ammonia content of 6 g-N/l, with a low methane yield of only 67 ml CH4/g-VS and a high concentration of volatile fatty acids (11.5 g acetate/l). Several methods were tested in order to increase the
methane yield. Addition of 1.5% (w/w) activated carbon, 10% (w/w) glauconite or 1.5% (w/w) activated carbon and 10% (w/w) glauconite resulted in an increase of the methane yield to 126 ml CH4/g
VS, 90 ml CH4/g VS and 195 ml CH4/g-VS respectively. Batch experiments showed that at an ammonia
concentration of 4.6 g-N/l even small amounts of sulphide (23 mg S2ÿ/l) inhibited biogas production.
However, addition of activated carbon (2.5% (w/w)) or FeCl2 (4.4 mM) could counteract the inhibition
which was mainly explained by a reduction of the sulphide content by adsorption to the activated carbon or precipitation as ferrous sulphide. The methane yield could be increased to 102 ml CH4/g-VS by
switching o€ the stirrer half an hour before and after substrate addition, which was attributed to
increased biomass retention due to improved sedimentation. Increasing the hydraulic retention time
(HRT) from 15 to 30 days resulted in an increase of the methane yield to 182 ml CH4/g-VS. Addition
of granules from a thermophilic up¯ow anaerobic sludge blanket reactor treating volatile fatty acids
gave only a temporary increase in the methane yield. # 1999 Elsevier Science Ltd. All rights reserved
INTRODUCTION
The use of anaerobic processes for treatment of organic wastes has increased in recent years. Many
centralized large scale biogas plants (CBP) serving a
number of farmers have emerged over the last 10
years in Denmark. These plants treat mainly manure (80%) together with other organic wastes
(Ahring et al., 1992; Tafdrup, 1994). A large part of
the manure is swine manure. Anaerobic degradation
of swine manure, especially at thermophilic temperatures, has proven to be dicult (Braun et al.,
1981; Chen and Day, 1986; Hansen et al., 1997).
Thermophilic digestion is a preferred choice for the
CBP for many reasons such as improved sanitary
e€ects and the wish to minimize the risk of spreading pathogens (Lund et al., 1995). The diculty in
digesting swine manure is attributed to its high content of ammonia (NH+
4 +NH3) (Angelidaki and
Ahring, 1993b; Hansen et al., 1997). Ammonia is
considered to be the main cause of inhibition when
animal waste is digested to methane (Farina et al.,
1988; van Velsen, 1979; Zeeman et al., 1985). It has
previously been shown that the biogas process can
be adapted to an ammonia concentration of about
4 g-N/l without any reduction of the methane yield
(Angelidaki and Ahring, 1993b; Hashimoto, 1986;
*Author to whom all correspondence should be addressed.
[Tel: +4545251566, Fax: +4545932850, E-mail:
bka@imt.dtu.dk].
van Velsen, 1979). Swine manure will, in addition
to ammonia, contain a high sulphate concentration
derived from a protein-rich diet. Sulphate is used as
electron acceptor of the sulphate reducing bacteria
(Hao et al., 1996, Petersen and Ahring, 1992). Since
sulphate reduction is more favourable energetically
than methane production, the sulphate reducing
bacteria will compete with the methanogens for
substrates such as acetate and H2/CO2 (Hao et al.,
1996). At the same time sulphate will be metabolised to sulphide (S2ÿ+HSÿ+H2S). Sulphide inhibits the biogas process at concentrations around
50 mg S2ÿ/l (Karhadkar et al., 1987; Parkin et al.,
1983; Rudolfs and Amberg, 1952). Severe inhibition
of the biogas process is observed when the concentration exceeds 150 to 200 mg S2ÿ/l (Karhadkar et
al., 1987).
Many papers have dealt with the inhibition of the
biogas process (Angelidaki and Ahring, 1993b;
Hansen et al., 1997). However, these studies present
no solution to the problems. A few studies have
shown that various types of inhibition can be counteracted by immobilising the bacteria with either
di€erent types of clay, activated carbon (AC) or by
addition of calcium (Angelidaki et al., 1990; Nakhla
et al., 1990; Sanchez et al., 1994; Angelidaki and
Ahring, 1995). In the present study we show that
the concentration of sulphide has to be taken into
account when studying ammonia inhibition of manure. We further examine the e€ect of di€erent
1805
1806
Kaare Hvid Hansen et al.
methods (addition of AC, glauconite, bentonite
bound oil (BBO) and sedimentation of the biomass
and particles within the reactor) for improvement
of the biogas yield of swine manure when digested
in thermophilic continously stirred tank reactors
(CSTR).
MATERIALS AND METHODS
Manure used in the experiments was from the same
batch taken at a Danish biogas plant. It was thoroughly
mixed and poured into 5 and 10 l bottles and kept frozen
until used.
Batch experiments
Two batch experiments were performed in 58 ml serum
vials containing 14 ml inoculum and 6 ml swine manure.
The serum vials were closed with butyl rubber stoppers
and sealed with aluminium crimps. The vials were incubated at 558C. The vials were shaken vigorously once a
day and methane production was measured. Each experiment was done in duplicate. pH and ammonia concentration were measured at the end of the experiment. The
ammonia concentration in the supernatant was measured
by centrifuging the sample at 7000 g for 10 min.
E€ect of activated carbon (AC). (Experiment 1): The
purpose of this experiment was to investigate the e€ect of
AC on the degradation of swine manure. The inoculum
was taken from a lab scale reactor (Rsed,gra see CSTR experiments) at day 20 and stored in a 558C incubator for 3
days before use. Swine manure was used as substrate. AC
(Activated Charcoal, 14/60 mesh, Sigma) was added in 4
di€erent concentrations (0.5% (w/w), 1.0% (w/w), 2.5%
(w/w) and 5.0% (w/w)).
E€ect of sulphide. (Experiment 2): The purpose of this
experiment was to investigate the e€ect of sulphide on the
degradation of swine manure. Therefore, an inocula with
a low sulphide concentration had to be used. Furthermore
AC or FeCl2 were tested for their ability to counteract sulphide inhibition. The inoculum was taken from a Danish
biogas plant degrading a mixture of swine manure
(approx. 40%), cattle manure (approx. 40%) and industrial waste (approx. 20%). The composition of industrial
waste was similar to swine manure composition. The plant
had a hydraulic retention time (HRT) of 18±20 days and
was operated at 528C. The inocula had an ammonia concentration of 3.8 g-N/l. The volatile fatty acids (VFA) concentration was 3000 mg-acetate/l and the sulphide
concentration was less than 2 mg-S2ÿ/l. Fresh swine manure, supplemented with AC, FeCl2 and/or Na2S, was used
as substrate (Table 1).
CSTR experiments
Eight 4.5 l lab-scale CSTR reactors with a working
volume of 3 l were used (Hansen et al., 1997). All reactors
were operated at 558C with 15 days HRT except one
which was kept at 378C. The substrate was pumped to the
reactor every fourth hour. If not otherwise stated the reactors were started up with 2.8 l inoculum from a Danish
biogas plant (see Batch Experiment 2) and 200 ml swine
manure.
Nine di€erent reactor experiments divided in two groups
were performed, including two controls. The controls for
both groups were two reactors fed with swine manure at
either 558C (Rcont, 55) or at 378C (Rcont, 37).
The reactors were run until they reached steady state
for at least 10 days. Steady state was assumed when the
methane yield, pH, content of VFAs and ammonia were
constant. Methane yield was measured daily, while pH,
VFAs and ammonia concentration were measured at least
twice a week.
Methods for improvement of reactor performance
Group 1. One method was an increase of the HRT from
15 to 30 days (RHRT,30). In the second method the biomass content was increased by sedimentation of both the
particles and the biomass in the reactor. Sedimentation
was obtained by switching o€ the stirrer for half an hour
before and after substrate was introduced to the reactor
(RSed). A third method (RSed,Gra) was to add extra biomass (200 ml granules from a thermophilic up¯ow anaerobic sludge blanket reactor treating VFAs was added
during start-up). This reactor was also operated with sedimentation as described for reactor RSed.
Group 2. Di€erent inorganic compounds were added to
the substrate in this group of CSTR experiments. In RAC
1.5% (w/w) activated carbon was added to fresh swine
manure. After the reactor reached steady state it was operated for about 20 days. Then additional 10% (w/w) glauconite was supplemented to the substrate of the same
reactor (RAC,Glau). 10% (w/w) glauconite was added to the
substrate of one reactor (RGlau), and another reactor
(RBBO) was fed with substrate containing 5% (w/w) BBO.
Analytical methods
The methane production in batch experiments and composition of the biogas from CSTR reactors was determined by gas chromatography, as previously described
(Angelidaki et al., 1990). The content of VFA, presented
here are a summation of acetate, propionate, butyrate, isobutyrate, valerate and isovalerate, was measured with a
Shimadzu GC-8A gas chromatograph and all converted to
acetate (Angelidaki et al., 1990).
The total nitrogen content was measured by the
Kjeldahl method, and the dissolved ammonia content were
measured by the Kjeldahl method without the destruction
step (Greenberg et al., 1992). Total solids and organic
solids were measured by standard methods (Greenberg et
al., 1992). Total sulfur was measured by the ICP method
by Steins Laboratories (Denmark) (Greenberg et al.,
1992).
The sulphide content (H2S, HSÿ and S2ÿ) in the reactor
¯uid was determined by the methylene blue method after
pretreating the sample with zinc sulphate (Greenberg et
al., 1992).
RESULTS
The swine manure used had a pH of 7.62 2 0.02,
a content of volatile solids (VS) of 45 2 1 g/l and a
total concentration of volatile fatty acids of
11.0 2 0.5 g as acetate/l (183 mM). The Kjeldahl-N
was determined to 6.6 g-N/l and the ammonia concentration was 5.3 2 0.1 g-N/l. The ammonia conTable 1. Total concentration of H2S, activated carbon and Fe2+
in the vials in Batch Experiment 2
Designation
10 S
23 S
36 S
36 S + AC
36 S + Fe
36 S + AC + Fe
Sulphide
concentration
(mg S/l)
AC
concentration
(% (w/w))
Fe2+
concentration
(mmol)
10
23
36
36
36
36
0
0
0
2.5
0
2.5
0
0
0
0
4.4
4.4
Anaerobic digestion of swine manure
centration in the supernatant was 4.7 2 0.1 g-N/l.
The
dissolved
sulphide
concentration
was
27.5 2 0.5 mg-S/l and the total sulphur content was
60 2 1 mg-S/l. The maximum practical methane potential (B0), which could be obtained with this material, was 3002 20 ml CH4/g-VS (Hansen et al.,
1997).
Batch experiments
Addition of AC at concentrations equal to 2.5%
(w/w) or higher reduced inhibition (Fig. 1).
Furthermore, these AC concentrations resulted in a
methane production equal to the B0 in about 50
days. If only 0.5% (w/w) or 1.0% (w/w) AC was
added the methane yield was doubled in comparison to the vials without addition of AC (Fig. 1),
however, the yield was only 10% of B0 after 68
days. The pH was 8.0 and the ammonia concentration was 5.7 g-N/l in all vials at the end of the
experiment. The ammonia concentration in the
supernatant was determined to 5.4 g-N/l. The lack
of any signi®cant di€erence in pH and ammonia in
the vials at the end of the experiment showed that
activated carbon was not adsorbing the ammonia.
All the vials in Batch Experiment 2 (e€ect of sulphide experiment) had an ammonia concentration
of 4.6 g-N/l and a pH of 7.7 at the end of the experiment. Addition of sulphide to a total of 23 g
S2ÿ/l or higher resulted in inhibition (Fig. 2). The
methane production decreased from 165 ml/g-VS in
vials with 10 g-S2ÿ/l to 100 and 62 ml/g-VS in vials
with 23 and 36 g-S2ÿ/l, respectively. The sulphide
inhibition could be counteracted by adding either
activated carbon or Fe2+ (Fig. 2). Addition of both
carbon and Fe2+ did not signi®cantly increase the
biogas production further compared to addition of
the compounds alone (Fig. 2).
1807
CSTR experiments
The development of VFA and biogas production
of RSed and RSed,Gra are shown in Fig. 3a and 3b.
The reactors were in steady state with regard to
biogas production, VFA, methane percent, TS, VS,
pH and ammonia concentration after 55 days of
operation. Accumulation of particulate matter
resulted in a higher TS and VS content in RSed and
RSed,Gra (85 g/l and 58 g/l) compared to the TS and
VS measured in the thermophilic control reactor
(64 g/l and 46 g/l). The steady state methane yield
in these two reactors RSed and RSed,Gra was 102 ml
CH4/g-VS and 80 ml CH4/g-VS, respectively, which
corresponded to an increase of up to 52% compared to the parallel thermophilic control (Table 2).
RSed,Gra which was further inoculated with granules
had a gas production between 2500 and 3000 ml/
day for the ®rst 25 days (Fig. 3b). No granules
were observed in the e‚uent, and an examination
of the reactor content after day 68 showed that the
granules disintegrated within the reactor. However,
after 10 and 25 days in RSed and RSed,Gra, respectively the gas production dropped to less than
2000 ml/day (Fig. 3a and 3b). Increasing the HRT
to 30 days (RHRT,30) also increased the methane
yield to 182 ml CH4/g-VS, which was comparable
to that of the mesophilic control (Rcont, 37) (Table 2).
Addition of 1.5% (w/w) AC or 10% (w/w) glauconite to a reactor resulted in an increase of the
steady state methane yield by 88% or 34%, respectively, compared to that of the thermophilic control
(Table 2). RAC was in steady state after 40 days
(Fig. 3c), while RGlau was in steady state after 65
days (not shown). The soluble sulphide concentration in the RAC was less than 2 mg S2ÿ/l compared to 36 mg S2ÿ/l in RGlau and the thermophilic
Fig. 1. Methane development plotted against time for vials containing swine manure as a substrate and
di€erent concentrations of activated carbon (AC).
1808
Kaare Hvid Hansen et al.
Fig. 2. Methane development plotted against time for vials containing swine manure as substrate and
di€erent concentrations of H2S (S), activated carbon (AC) and Fe2+ (see Table 2).
control. The soluble ammonia concentration was
4.4 g-N/l and 5.2 g-N/l in RGlau and RAC respectively. Supplementing RAC with glauconite after 72
days of operation (RAC,Glau) caused an almost
instant increase in the methane production and the
steady state methane yield also increased compared
to RAC (191% compared to the thermophilic control) (Table 2 and Fig. 3c). The VFA level
decreased in RAC,Glau compared to RAC from
10.5 g-acetate/l to 6 g-acetate/l after an initial
Fig. 3. The daily biogas production and the total VFA concentration as a function of time in three
di€erent CSTR reactors. Q = Total VFA concentration and W = Biogas production (a) RSed, (b)
RSed,Gra and (c) RAC and RAC,Glau, change from only addition of AC (RAC) to addition of AC and
glauconite (RAC,Glau) is marked with vertical line.
Anaerobic digestion of swine manure
1809
Table 2. Measured and calculated parameters for the CSTR reactors in steady state
Designation
R378C
R558C
RSed
RSed,Gra
RHRT,30
RAC
Rglau
RAC,Glau
RBBO
CH4 yield (ml CH4/g-VS)
CH4% (%)1
Ammonia (g-N/l)
pH
NH3 (g-N/l)2
Total VFA (g-AC/l)3
188
67
102
80
182
126
90
195
24
71
51
63
53
63
65
63
66
41
5.9
6.0
5.7
5.7
5.8
5.8
5.8
5.8
6.0
8.06
7.97
7.95
7.95
8.06
8.03
7.97
8.04
7.46
0.75
1.6
1.5
1.5
1.8
1.5
1.1
1.3
0.60
4.8
11.5
10.7
10.2
8.5
10.3
9.1
6.4
15.4
1
Percent of methane in the gas phase; 2 Free ammonia; 3 Total concentration of volatile fatty acids. Standard deviations: CH4
yield = 10 ml CH4/g-VS, CH4% = 1%, Ammonia = 0.1 g-N/l, pH = 0.03, NH3=0.4 and Total VFA = 0.2 g-AC/l
increase (Fig. 3). In this case an even higher
methane yield than in the mesophilic control was
observed (Table 2). The ammonia content in solution was only 4.5 g-N/l in RAC,Glau while it was
5.2 g-N/l in RAC. An addition of 5% (w/w) of BBO
decreased the steady state methane yield, and lowered the pH (Table 2).
Although most of the di€erent methods applied
resulted in increase of the methane yield, the biogas
process was still severely inhibited as indicated by
the high content of VFA (Table 2). The process
was, however, stable with constant levels of
methane production, VFA and pH. Total failure
with pH breakdown and cease of methane production was never observed even when the VFA
concentration was 11.5 g-acetate/l.
DISCUSSION
Thermophilic anaerobic degradation of swine
manure containing high concentration of ammonia
was seen to be stable but with a low methane yield.
The problem with anaerobic digestion of swine
manure has previously only been attributed to the
presence of high ammonia concentrations (Farina et
al., 1988; Hansen et al., 1997; van Velsen, 1979).
However, this study shows that inhibition by sulphide is also of importance. A sulphide concentration of 23 mg-S/l or more led to approximately
40% decrease of the methane production when
digesting material with a high ammonia concentration. A combined e€ect of the two inhibitors,
ammonia and sulphide, could explain why we
found that much lower concentrations of sulphide
can be inhibitory compared to previous studies
(Karhadkar et al., 1987; Parkin et al., 1983;
Rudolfs and Amberg, 1952).
We found several ways of increasing the methane
yield of inhibited reactors (increasing the HRT,
sedimenting the biomass/particles within the CSTR
reactor or adding activated carbon, glauconite or
methanogenic granules) when digesting swine manure containing ammonia and sulphide in inhibiting
concentrations. However, we have been unable to
con®rm previous results showing that an addition
of bentonite bound oil, BBO, could counteract
some of the inhibition by ammonia as found for
thermophilic digestion of cow manure (Angelidaki
and Ahring, 1993a). The reason could be a less
stable process which will result in accumulation of
the VFA released by BBO. Addition of AC to the
in¯uent resulted in a signi®cant increase in the
methane yield. AC will remove most of the sulphide
found in solution, as indicated by the lowering of
the soluble sulphide concentration from 36 mg-S/l
to less than 2 mg-S/l. It has previously been
reported that AC removes metal ions like Cu2+ and
Zn2+ from a solution (Budinova et al., 1994).
Furthermore, addition of AC decreased the acclimation time of the anaerobic processes degrading
waste waters containing phenols and long-chain
fatty acids (Kindzierski et al., 1992). Another possible explanation for the positive e€ect exhibited by
AC could be that AC particles o€er an immobilization matrix for bacteria (Kindzierski et al., 1992).
It has previously been reported that inert materials
could reduce inhibition of the biogas process and
make the process more stable (Angelidaki et al.,
1990; Hanaki et al., 1994; Nakhla et al., 1990).
Addition of glauconite increased the steady state
methane yield from 67 ml CH4/g-VS to 90 ml CH4/
g-VS. At the same time the soluble ammonia concentration decreased from 5.2 g-N/l to 4.5 g-N/l due
to ion exchange corresponding to a free ammonia
concentration of 1.1 g-N/l compared to 1.6 g-N/l
for RGlau and Rcont, 55, respectively (Table 2). A
decrease in the free ammonia concentration was
expected to give rise to an increase in the methane
yield (Hansen et al., 1997). Addition of both glauconite and AC (RAC,Glau) resulted in an increase in
the steady state methane yield (195 ml CH4/g-VS)
which is a higher yield than seen for addition of
AC and glauconite alone. This shows that the inhibition of ammonia and sulphide are in¯uencing
each other.
By sedimentation of the particles/biomass an
increased biomass concentration can be obtained.
This resulted in an increased biogas yield. Adding
methanogenic granules resulted in a biogas yield
near the B0 for the ®rst 20 days of operation com-
1810
Kaare Hvid Hansen et al.
pared to RSed where the biogas production
decreased below 2000 ml/day after 8 days (Fig. 3a
and 3b). Immobilized biomass is more resistant to
inhibition than suspended biomass (De Baere et al.,
1984) and the results from this study are in agreement with this. However, it seems that the granules
disintegrate in CSTR reactors, and it would therefore be necessary to continuously apply granular
sludge to maintain the high methane yield. After
the two reactors (RSed, RSed,Gra) reached steady
state there was a signi®cant di€erence in their
methane yield (Fig. 3). This could be because the
methanogenic population in RSed,Gra originated
from granules and therefore was not adapted to
growth in suspended culture. Increasing the HRT
increased the biogas yield as would be expected. An
HRT of 15 days was probably too short to maintain a high density of active bacterial groups in the
system. This is in agreement with the increased
methane yield that we achieved by increasing the
biomass concentration in the reactor (RSed,
RSed,Gra).
To summarize we have tested ®ve di€erent
methods to increase the methane yield during thermophilic digestion of swine manure. The method
where particles within the reactor are allowed to
settle is perhaps the most promising, since it is easy
and cheap to achieve in both new and existing biogas plants. An addition of glauconite or other materials able to ion exchange ammonia will also
increase the methane yield. Furthermore, addition
of granules or activated carbon, or increasing the
HRT, were found to have an positive e€ect on the
methane yield.
AcknowledgementsÐA special thanks to Hector Garcia for
excellent technical assistance. The Danish Energy
Program, project number j. nr 1383/95-002, supported this
project.
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