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Como la piscicultura onshore en el agua de mar raras veces es usada, el tratamiento anaerobio de estos efluentes no ha sido investigado antes. El objetivo del estudio presente es por lo tanto para averiguar como el proceso trabaja con el lodo de piscicultura de salina, y lo que pueden esperar la producción de energía. El proceso puede ser problemático porque el lodo contiene varias sustancias en concentraciones inhibitorias
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Bioresource Technology 93 (2004) 155–167
Mesophilic anaerobic treatment of sludge from saline fishfarm effluents with biogas production
Ruth Gebauer *
Department of Aquaculture and Natural Sciences, Finnmark University College, Follums vei 31, N-9509 Alta, Norway
Received 27 June 2003; received in revised form 2 September 2003; accepted 28 October 2003
Abstract
The mesophilic anaerobic treatment of sludge from saline fish farm effluents (total solids (TS): 8.2–10.2 wt%, chemical oxygen
demand (COD): 60–74 g/l, sodium (Na): 10–10.5 g/l) was carried out in continuously stirred tank reactors (CSTRs) at 35 �C. COD
stabilization between 36% and 55% and methane yields between 0.114 and 0.184 l/g COD added were achieved. However, the
process was strongly inhibited, presumably by sodium, and unstable, with propionic acid being the main compound of the volatile
fatty acids (VFA). When diluting the sludge 1:1 with tap water (Na: 5.3 g/l), the inhibition could be overcome and a stable process
with low VFA concentrations was achieved. The results of the study are used to make recommendations for the configuration of
full-scale treatment plants for the collected sludge from one salmon farming licence and to estimate the energy production from
these plants.
� 2003 Elsevier Ltd. All rights reserved.
Keywords: Anaerobic treatment; Fish farming sludge; Salinity; Energy production; Biogas; Sludge treatment plant
1. Introduction
Due to significant problems with diseases in Nor-
wegian salmon farming, in the late 1980s some onshore
facilities for salmon grow-out in seawater were built, to
enable better control of rearing conditions. At these
onshore plants it is easier to control the discharge of
organic matter and nutrients (corresponding to that of
10,000 people per salmon licence) to the sea by purifyingthe effluents at the end of the outlet pipe, for example by
using micro sieves. But the purification produces sludge,
consisting of faeces and excess feed, that must be dis-
posed of. If possible it should be reused as a fertilizer
which according to the regulations of the Norwegian
Ministry of Agriculture requires sufficient stabilization
of the organic matter to avoid bothersome odours, and
hygienization to avoid spreading fish pathogens (Nor-wegian Ministry of Agriculture, 1998).
Stabilization and hygienization of sludge may be
achieved through several methods, among them an-
aerobic treatment, which, because of its energy pro-
* Tel.: +47-7765-6377, +47-7845-0475.
E-mail address: ruth@hifm.no (R. Gebauer).
0960-8524/$ - see front matter � 2003 Elsevier Ltd. All rights reserved.
doi:10.1016/j.biortech.2003.10.024
duction, may be preferable to others. The energy may,among other purposes, be used for pasteurisation of the
sludge, in case hygienization cannot be achieved through
the anaerobic treatment alone.
Because onshore fish farming in seawater is rarely
used, anaerobic treatment of these effluents has not been
investigated before. The purpose of the present study is
therefore to find out how the process works with saline
fish farming sludge, and what energy production may beexpected. The process may be problematic because the
sludge contains several substances at inhibitory con-
centrations: sodium (10.2 g Na/l) and sulphate (1.2 g
SO4-S/l) from the seawater, which in the anaerobic
process will be reduced to sulphide, and ammonia from
the degradation of the protein in the faeces and the ex-
cess feed (29% VS, 2.4–3.0 g Tot-N/l). Additionally,
about 70% of the organic matter exists as particles andthe sludge arises at low temperatures (1–10 �C). The
latter may require operating the process with a high
solid content, in order to minimize the energy demand
for heating of the sludge to process temperature.
When treating sludge collected from effluents from
fresh-water trout farming, Kugelman and Van Gorder
(1991) found strong inhibition, attributed to ammonia,
when treating a concentrated sludge (4–6 wt% of TS,
Nomenclature
Ca calcium ion, Ca2þ (mg/l)
CH4 methane
Cl chloride ion, Cl� (mg/l)
CO2 carbon dioxide
COD chemical oxygen demand (g/l)CSTR continuously stirred tank reactor
HRT hydraulic retention time (days)
H2S hydrogen sulphide (mg/l)
H2S-S hydrogen sulphide sulphur
K potassium ion, Kþ (mg/l)
Kj-N Kjeldahl nitrogen (mg/l)
MWh mega watt-hour
Mg magnesium ion, Mg2þ (mg/l)Na sodium ion, Naþ (g/l or mg/l)
NH3-N unionized ammonia nitrogen (mg/l)
NH4-N ammonium nitrogen (g/l or mg/l)
NO3-N nitrate nitrogen (mg/l)
NOK Norwegian crowns
OLR organic loading rate (g COD/g VSS day�1)
SO4 sulphate ion, SO2�4 (mg/l)
SO4-S sulphate sulphur (mg/l)
SS suspended solids (g/l)
STP standard temperature and pressure, 0 �C,1 atm
Tot-H2S total suphide, S2�+HS�+H2S (mg/l)
Tot-H2S-S total sulphide sulphur (mg/l)
Tot-N total nitrogen (g/l)
Tot-NH4-N total ammonium nitrogen
Tot-P total phosphor (mg/l)
Tot-S total sulphur (mg/l)
TS total solids (% of weight)
UASB upflow anaerobic sludge blanket digesterVFA volatile fatty acids
vol.% % of volume
VS volatile (organic) solids (% of weight)
VSS volatile (organic) suspended solids (g/l)
wt% % of weight
156 R. Gebauer / Bioresource Technology 93 (2004) 155–167
2.5–3.5 g Tot-N/l) in CSTRs. While Lanari and Franci
(1998) were able to successfully treat a diluted sludge
(1.3–2.4 wt% of TS, 0.16–0.24 g Tot-N/l) at only 25 �C,in an anaerobic filter filled with polyurethane foam, in
accordance with the reported threshold concentrations
for initial inhibition by ammonia of 1500–1900 mg Tot-
NH4-N/l (McCarty, 1964; Melbinger and Donellon,
1971; Koster and Lettinga, 1988).Initial inhibition of anaerobic treatment of complex
waste by sodium has been reported from 3–4 g Na/l, and
total inhibition has been reported from 10–11 g Na/l
(Georgacakis and Sievers, 1979: dairy waste; Toldra
et al., 1984: tomato waste). Serious disturbance by sul-
phide has been reported from 100 to 200 mg H2S/l
(Lawrence and McCarty, 1966; Rinzema and Lettinga,
1988). However, Soto et al. (1991), Mendez et al. (1995),Omil et al. (1996), and Punal and Lema (1999) reported
successful treatment of saline seafood processing efflu-
ents with concentrations of sodium (5–12 g/l), sulphate
(0.6–2.7 g SO4-S/l) and protein (1–4 g Tot-N/l) similar to
those in the fish farm sludge of the present investigation.
However, more than 80% of the organic matter in their
wastes was soluble, and the concentration of organic
matter was only 25–50% of that in the fish farm sludgeof the present investigation.
In the present study anaerobic treatment of sludge
(8.2–10.2 wt% of TS) collected from saline fish farm
effluents was investigated at mesophilic temperature (35
�C) and in the easiest process configuration, the CSTR.
The results were used as the basis for recommendations
for process configurations for full-scale treatment plants
and for estimating the potential energy production from
these plants.
2. Methods
2.1. Inoculum
The inoculum was taken from an experimental
anaerobic digester that was originally inoculated with a
mixture of digested municipal sewage sludge and cow
manure at the Agricultural University of Norway at �As,
Southern Norway. Examination of the biomass by anti-
agent tests (Ahring and Nørgaard, 1994) showed theoccurrence of Methanosarcina barkeri and Methano-
coccus varnietii, but the absence of Methanogenium sp.
UCLA. Thus the methanogenic biomass was predomi-
nated by species that are normally found in low-salinity
digesters with suspended cultures.
2.2. Fish farming sludge (substrate)
The sludge (substrate) was collected with an air-flu-
shed ribbon strainer in a pilot plant at the onshore fish
farm for Atlantic salmon grown out at Hemnskjel in
Middle Norway (Ulgenes et al., 1994), with the farm
operated at a feed coefficient of 1.06. The composition isprovided in Table 1.
The sludge (substrate) was collected during two
periods totalling 10–12 h in April 1992, at a surrounding
Table 1
Composition of sludge from sieving of saline fish farm effluents with an
air-flushed ribbon strainer
Component Content
TS (wt%) 8.2–10.2a
VS (% of TS) 49.8–54.1a
Protein (% of VS) 29b
Fat (% of VS) 15b
Carbohydrates (% of VS) 56b
COD (g/l) 60.3–74.1a
Kj-N (mg/l) 2440–3040a
NH4-N (mg/l) 430–530a
NO3-N (mg/l) 2.2–2.7b
Tot-P (mg/l) 1350–1683b
Tot-S (mg/l) 990–1230b
SO4-S (mg/l) 920–1150b
Na (mg/l) 10 200c
K (mg/l) 476c
Ca (mg/l)d 4640 (1670)c
Mg (mg/l) 1759c
Cl (mg/l) 23 600c
a 10 Samples.b 4 Samples.c 2 Samples.d Concentration of dissolved Ca in parentheses.
R. Gebauer / Bioresource Technology 93 (2004) 155–167 157
temperature of 10–12 �C, and prior to the experiments
stored frozen at )28 �C for up to two and a half years.
2.3. Experimental set up
The experiments were carried out in two 15-l digesters
of metal that were placed in a common water bath. The
Fig. 1. Experimental set up for the experiments with sludge from sa
experimental set up for one of the digesters is shown in
detail in Fig. 1. The digesters were operated semi-con-
tinuously at 35 �C with 4–6 l of sludge volume and
stirred continuously at 200 rpm. The digesters were
sampled and fed manually, through, respectively, a
double siphon and a tube through the digester lid. The
biogas was collected in 15-l aluminium bags. For ana-
lysis of the gas composition, gas samples were takenwith a gas-tight syringe through a gas sampling point
placed on the tube leading to the gas-sampling bag. The
gas production was measured manually by emptying of
the gasbags by suction of acid sodium sulphate solution
(DIN 38 414-S8, 1985) from a tight demijohn of 25 l,
and following weighing of the collected liquid. The
weighed amount was corrected for the pressure differ-
ence caused by the height difference between the fluidlevels in the demijohn and the collection can.
2.4. Experimental design
At first, one of the digesters was started up in order
to get the process into operation with (undiluted) fish
farming sludge at a HRT of about 30 days (cf. Section
2.5.1), because this HRT traditionally has been recom-
mended for the starting of anaerobic CSTRs. However,due to malfunction of the equipment, the real HRT was
somewhat lower (cf. Table 2). Because the inoculum was
taken from a low salinity environment, the salinity in the
digester was increased gradually over a period of 266
days in order to enable probable adaptation of the
biomass. This was achieved by successive feeding with
different types of fish farming sludge with increasing
line fish farm effluents, drawing for one of the two digesters.
Table 2
Operating conditions during the mesophilic treatment of undiluted sludge from saline fish farm effluents (Salinity: 35‰; Na: 10.2 g/l; TS: 8.2–10.2
wt%; VS: 4.8–5.5 wt%; COD: 60.3–74.1 g/l)
Period Days Operating condition SLV
(ml)
OLRa
(g COD/l day)
HRTa
(days)
1a 1–57 First start up increase of sludge volume 3750–6100 1.0 until day 40,
1.55 from day 41
50.9
1b 58–95 Semi-continuous operation, withdrawal of sludge
for serum bottle experiments on day 78 and
following increase of sludge volume
3650–6000 1.38 61.5
1c 96–124 Semi-continuous operation, withdrawal of sludge
for serum bottle experiments on day 118 and
following increase of sludge volume
5150–6000 1.56 41.2
125–191 Stop of operation
2a 192–207 Increase of sludge volume 3500–4200 2.12 32.7
2b 208–232 Semi-continuous operation 4200–4000 2.55 27.5
233–252 Stop of operation
3 253–260 Semi-continuous operation 4000 1.9 65
261–266 Stop of operation
4a 267–282 Second start up with sludge from the reactor,
increase of sludge volume
4000–6100 2.42 26.2
4b 283–337 Semi-continuous operation 5840–5240 2.52 27.9
5 338–359 Stop of feeding 5100–4600 0 16a 360–363 Some feeding 4700–4900 1.44 48.1
6b 364–383 Semi-continuous operation 4900–4800 2.85 24.3
6c 384–402 Semi-continuous operation 4800 3.12 24.0
402–404 Stop of operation
7a 405–423 Third start up with sludge from the reactor,
increase of sludge volume
4900–6000 1.15 54.4
7b 424–440 Semi-continuous operation 6000 1.24 60
aAverage for the period.
158 R. Gebauer / Bioresource Technology 93 (2004) 155–167
salinity (cf. Section 2.5.1). Because the process still was
unstable with high VFA concentrations after 400 days of
operation (cf. Section 3.1), the digester was operated at
60 days HRT for 40 more days. However, the increase in
HRT did not lead to a reduction to the VFA concen-trations in the digester (cf. Section 3). Therefore, a sec-
ond digester was started with diluted sludge (1:1 with
tap water) with 30 days HRT (cf. Section 2.5.2) in order
to establish a well functioning process with low con-
centrations of VFA. Because time was short this process
could not be further optimised.
2.5. Running of experiments
During start up, the digesters were feed irregularly
(cf. Sections 2.5.1 and 2.5.2) and only sampled occa-
sionally. During periods when the sludge volume had to
be increased, at start up or after removal of sludge for
serum bottle experiments (results shown in Gebauer,
1998), the digesters were feed regularly, daily or every
second day, but not sampled, until the working volumewas reached. During semi-continuous operation, the
digesters were first sampled and then fed once a day,
every day at the same time. However, feeding was
postponed when the pH had decreased substantially.
The pH value in the digester was measured daily, before
feeding. The gas production was measured two to three
times per week, and the gas composition was analysed
twice per week. The TS, VS and COD of the raw sludgewere analysed in every new batch of sludge. The TS, VS,
COD, VFA and ammonia in the digested sludge were
analysed twice per week. The alkalinity and the Na, K,
Ca, Mg and Cl were analysed occasionally.
2.5.1. Digester with undiluted sludge
This digester was operated for a total of 440 days. The
operating conditions during the whole period are pre-sented in Fig. 2 and summarized in Table 2. The process
was started up with 0.8 l of inoculum, 2 l of a freshwater
fish farming sludge (TS: 3.6 wt%; VS: 2.9 wt%), 0.95 l of
tap water and 4 g of sodium bicarbonate (Na2CO3) as a
buffer. During the following days, the pH value was
maintained at around 7.0 by the almost daily addition of
a few grams of sodium bicarbonate. Thus in total about
60 g of Na2CO3 were added during the start up period.When the methane content in the biogas was significant,
having exceeded 15 vol%, the digester was fed sporadi-
cally to avoid acidification due to overloading. First, on
Fig. 2. Operating conditions, performance and pH-value and VFA-concentrations in the digester, during the mesophilic treatment of undiluted
sludge from saline fish farm effluents (salinity: 35‰; Na: 10.2 g/l; TS: 8.2–10.2 wt%; VS: 4.8–5.5 wt%; COD: 60.3–74.1 g/l).
R. Gebauer / Bioresource Technology 93 (2004) 155–167 159
day 27 and 30 respectively, 500 ml of a diluted saline fish
farming sludge with low salinity (7‰ after dilution,
Gebauer and Hanssen, 1992) was added. Then, on day
41, 43 and 44 respectively, 50 ml of the same saline fish
farming sludge (salinity of 14‰) was added undiluted.
From day 45, the sludge of the present investigation
(salinity of 35‰, cf. Table 1) was used as substrate. First,
the digester was fed every second day with 200 ml of this
sludge, until the working volume of 6 l was reached on
day 57 (cf. Fig. 2). Further on the digester was operated
as summarized in Table 2, according to the procedures
that were described in the previous section.
Fig. 3. Operating conditions, performance and pH-value and VFA-
concentrations in the digester, during the mesophilic treatment of di-
luted sludge from saline fish farm effluents (salinity: 17.5‰; Na: 5.3 g/l;
TS: 4.5 wt%; VS: 2.3 wt%; COD: 33.7 g/l).
160 R. Gebauer / Bioresource Technology 93 (2004) 155–167
The sodium concentration in the digester was in-
creased gradually from 1400 mg/l at start up to 5500,
6200, and 7700 mg/l on day 30, 40 and 57 respectively.
9100 mg/l were reached at the end of Period 1 (day 124),
and the sodium concentration of the raw sludge (cf.
Table 1) at the end of Period 3 (day 266).
Roughly three different operating regimes may be
distinguished: uneven OLR around 1.5 g COD/l day�1
and HRT around 40 days (Period 1 in Table 2 and Fig.
2), OLRs around 2.5–3.1 g COD/l day�1 and HRT
around 24–28 days (Periods 2–6 in Table 2 and Fig. 2),
and OLR around 1.2 g COD/l day�1 and HRT around
60 days (Period 7 Table 2 and Fig. 2). The operation had
to be stopped four times for practical reasons (day 125–
191, day 233–252, day 261–266, day 402–404). During
these periods the digester content was kept at roomtemperature without stirring. Twice, (day 267 and day
405) the digester was emptied and cleaned and started
up again with the former digester content.
2.5.2. Digester with diluted sludge
This digester was operated for a total of 74 days
under the conditions presented in Fig. 3. It was startedwith 2 l of digested undiluted sludge as inoculum and 2 l
of tap water. At start up the pH value in the digester was
almost 8 and was adjusted several times to pH levels of
7.2–7.5 through addition of hydrochloric acid during the
first 7 days of operation. Feeding started on day 7, when
there was measured about 10 vol.% of methane in the
biogas. The digester content was adjusted to 3900 ml,
and 300 ml of the digester content was replaced withdiluted fish farming sludge once a day. When the pH
value decreased substantially, feeding was stopped for
some days. Therefore, the loading was somewhat uneven
until day 28, when daily feeding was started at an OLR
of 1.1 g COD/l day�1 and 30 days HRT.
2.6. Analytical methods
The Kj-N was analysed according to standard
methods (APHA, 1989). The fat content was analysed
according to Folchs method (Folch et al., 1957).
The TS, VS, COD, Tot-NH4-N, NO3-N, Tot-P, Tot-
S, SO4-S and Cl were determined according to Nor-
wegian standards (status of 1994). Before analyses ofthe COD, the samples were diluted to less than 700 mg
COD/l and less than 200 mg Cl/l and homogenized. The
concentrations of the cations: Naþ, Kþ, Ca2þ and Mg2þ
were analysed by inductive couplet plasma analyses
(ICP). The composition of the biogas with respect to
CH4, CO2 and H2S was analysed on a gas chromato-
graph equipped with a packed column and a thermic
conductivity dectector (TCD) and with helium as carriergas. The concentrations of VFA were analysed by a gas
chromatograph equipped with a megabore capillary
column and a flame ionization detector (FID), with
nitrogen as carrier gas. The alkalinity was determined
from unfiltered samples, according to the method by
Hill (1990) for sludge with a high concentration of VFA.
All analyses were carried out with two replicates, and
the COD analyses were carried out with two samples
each from two replicates (four analyses) usually withdifferences of less than 5% between the replicates. The
presented values are the average values of the replicates.
R. Gebauer / Bioresource Technology 93 (2004) 155–167 161
More information about the analytical methods is pro-
vided in Gebauer (1998).
2.7. Calculations
The protein content was calculated from the content
of Kj-N and NH4-N according to the formula: g pro-
tein¼ 6.25 � (g Kj-N-g NH4-N). The carbohydrate con-
tent was calculated as the difference between the VS and
the protein and fat content. The concentration of H2S
in the sludge was calculated from the percentage of H2S
in the biogas by means of Henrys law: [H2S]sludge ¼a Æ [H2S]gas, with the absorption coefficient, a, set to24.661 mg H2Sliquid/vol% H2Sgas (calculated from Law-
rence and McCarty, 1966). The concentration of Tot-
H2S in the sludge was calculated from equilibrium at
the pH value in the sample: [Tot-H2S]sludge ¼ [H2S]sludge Æ(1+10ðpH�pK1Þ), with a pK1 value of 6.83 at 35 �C(Lawrence and McCarty, 1966). The concentrations of
NH3-N was calculated from the NH4-N concentration
Table 3
Operating conditions and performance, during characteristic operating perio
10.2 g/l) and diluted sludge (salinity: 17.5‰; Na: 5.3 g/l) from saline fish far
Undiluted sludge
Operating period 6c 2b 4
Parameter
HRT (days) 24.0 27.5
OLR (g COD/l day�1) 3.12 2.55
Length of period (days) 19 25
Feed
CODin (g/l) 74.9 70.1
TSin (wt%) 9.36 9.43
VSin (wt%) 4.90 4.92
% VS of TSin 52.3 52.2
Sludge in digester
CODout (g/l) 39.5 29.7
TSout (wt%) 6.51 5.79
VSout (wt%) 2.40 1.97a
% VS of TSout 36.9 34.0
Stabilization
% COD removed 43.3 55.2
% VS removed 48.2 48.2
Gas composition
vol.% methane 50.9 51.7
vol.% H2S 2.3–3.5 2.5–2.8
Meth. Product. (STP)
1 methane/g COD added 0.136 0.161
1 methane/g VS added 0.201 0.221
1 methane/g COD removed 0.314 0.291
1 methane/l sludge added 10.1 11.3
Vol. Meth. Prod. Rate (STP)
1 methane/l day�1 0.414 0.409
Spec. Meth. Prod. Rate (STP)
1 methane/g VS in dig. day�1 0.017 0.020
aValue caused by low VS concentration at the start of the operating peribUncertain value, see Section 4 in the text.
and the pH value in the sample according to: [NH3-
N]¼ 1/(1+10ðpKa�pHÞ) Æ [NH4-N], with pKa values of 9.03
(Whitfield, 1974) and 8.95 (Perrin, 1982) respectively for
undiluted and diluted sludge at 35 �C.The COD methanised was calculated as the ratio of
the methane production per g COD added and the
stochiometric methane production of 0.350 l/g COD at
STP. The COD converted to VFA (CODVFA) was cal-culated from the concentrations and COD values of the
different VFA. The COD anaerobically degradable was
calculated as the sum of the COD removed COD and
the CODVFA.
3. Results
The operating conditions, the performance and the
control parameters pH and concentration of VFA dur-
ing the operating periods are presented in Figs. 2 and 3
for the digesters with undiluted and diluted sludge,
ds of the mesophilic treatment of undiluted sludge (salinity: 35‰; Na:
m effluents, ordered with respect to increasing HRT
Diluted sludge
b 1c 7b 2b
27.9 41.2 60 30
2.51 1.56 1.24 1.10
55 29 17 34
70.0 64.2 74.2 33.7
9.19 9.4 10.18 4.51
4.81 4.76 5.51 2.30
52.3 50.6 54.1 51.0
40.6 29.2 37.5 13.6
6.67 5.09 6.21 2.88
2.51 1.75 2.18 0.93
37.6 34.4 35.1 32.3
36.7 53.6 53.7 60
47.4 59.0 61.9 58
48.9 50.0 54.1 57.6
2.8–3.6 2.4–3.3 2.2–2.5 1–1.6
0.114 0.165 0.184 0.154b
0.160 0.215 0.241 0.220b
0.309 0.306 0.343 0.257b
8.0 10.6 13.7 5.2 (diluted)b
0.286 0.256 0.228 0.174b
0.011 0.014 0.010 0.019b
od. VS accumulated in the digester during the operating period.
Table 5
Degradation of COD during characteristic operating periods of the mesophilic treatment of undiluted sludge (salinity: 35‰; Na: 10.2 g/l) and diluted
sludge (salinity: 17.5‰; Na: 5.3 g/l) from saline fish farm effluents, ordered with respect to increasing HRT
Undiluted sludge Diluted sludge
Operating period 6c 2b 4b 1c 7b 2b
HRT (days) 24.0 27.5 27.9 41.2 60 30
% COD methanised 38.9 46.0 32.6 47.1 52.6 44.0a
% COD removed 43.3 55.2 36.7 53.6 53.7 60.0
% CODVFA 13.8 6.4 15.3 ND 12.8 2.1
% COD anaerob. degradable 57.1 61.6 52.0 >53.6 66.5 62.1
aUncertain value, see Sections 3.2 and 4.1 in the text.
Table 4
Conditions in the digester during characteristic operating periods of the mesophilic treatment of undiluted sludge (salinity: 35‰; Na: 10.5 g/l) and
diluted sludge (salinity: 17.5‰; Na: 5.3 g/l) from saline fish farm effluents, ordered with respect to increasing HRT (nd¼ not determined)
Undiluted sludge Diluted sludge
Operating period 6c 2b 4b 1c 7b 2b
Condition
pH-value 6.95–7.0 7.05–7.1 6.85–7.0 6.76–6.95 7.05 6.7–7.0
Alkalinity (mg CaCO3/l) 6200 nd nd nd 6500 >3000
VFA: acetic acid (mg/l) 1660–2000 791–1102 980–1480 nd 1170–1590 282–466
stable stable stable stable stable
Propionic acid (mg/l) 3670–4380 1680–2660 3460–5430 3840–4650 40–159
stable increasing increasing stable stable
IONS from the salts
Naþ (mg/l) nd 9310 10 520 nd nd 5320
Kþ (mg/l) 445 494 240
Ca2þ (mg/l) 741 1050 500
Mg2þ (mg/l) 1300 1610 770
Cl� (mg/l) 18 800 19 720 9500
Sulphide
H2S (mg/l) 62–86 62–69 69–89 59–81 54–62 25–40
Tot-sulphide (HS�+H2S)(mg/l) 137–200 169–202 160–202 124–155 144–164 62–93
Ammonia
NH3-N (mg/l) 11 nd 11 nd 15–19 <20
Tot-NH4-N (mg/l) 1289 1443 1507–1694 <1000
162 R. Gebauer / Bioresource Technology 93 (2004) 155–167
respectively. More values for the operating conditions
and the performance during characteristic operating
periods of both processes are presented in Table 3.
Values for the conditions in the digesters during the
same periods are presented in Table 4, and values for the
degradation of COD during the same periods are pre-
sented in Table 5.
3.1. Digester with undiluted sludge
The digester with undiluted sludge was operated for a
total of 440 days under the conditions described in Table
2 in Section 2.5.1 and in Fig. 2.
During Period 1 (cf. Table 2 and Fig. 2) the digester
was operated with an uneven OLR of around 1.5 gCOD/l day�1, HRTs around 40 days and increasing
sodium concentration (cf. Section 2.5.1 of the Methods).
Gas and methane production started around the 15th
day of operation. After 70–80 days of operation the
percentage of methane in the biogas had reached the
stable level of 50 vol.%. During the first 95 days of
operation the gas production was unstable, as a result of
the unstable loading. When the loading was stabilized
the gas production also stabilized at around 0.34 l/g
COD added (at STP) corresponding to 0.46 l/l day�1 (cf.Fig. 2 and Table 3). From day 65 the stabilization of
COD stabilized slightly above 50% and the pH was
stable around pH 7. The volatile fatty acids were not
measured during the first 124 days of operation.
During the Periods 2–4 the digester was operated
with an OLR between 2.1 and 2.5 g COD/l day�1 and
HRT around 28 days, after 67 days of rest (cf. Table 2
and Fig. 2). This time the stabilization of COD de-creased steadily from 60% on day 208 to 30% on day 334
(cf. Fig. 2 and Table 3). However, the gas production
was stable both throughout Period 2b (day 208–232)
R. Gebauer / Bioresource Technology 93 (2004) 155–167 163
and throughout Period 4b (day 283–337), at the values
given in Table 3, before it suddenly stopped on day 337
(cf. Fig. 2). The pH-value was rather stable, first slightly
above pH 7 during Period 2, and then slightly below pH
7 during Period 4. But the concentrations of VFA in-
creased strongly, from zero at day 192 to about 2000
and 5000 mg/l for acetic and propionic acid, respec-
tively, on day 337, when the gas production stopped.It was assumed that the cessation of the gas produc-
tion was caused by inhibition due to high concentrations
of volatile fatty acids as a result of overloading. There-
fore, the feeding was stopped, and no feeding took place
during the following 22 days (Period 5). Gas production
began again the day after feeding was stopped and
continued during the whole period, decreasing from 0.33
to 0.19 l/l day�1, while the percentage of methane in thebiogas increased to 60 vol.%. The concentration of all
VFA other than propionic acid decreased right after stop
of feeding, to below 400 mg/l after 3 days without feed-
ing. However, the concentration of propionic acid in-
creased for 10 more days after feeding was stopped, to
6000 mg/l, before decreasing slightly to 5000 mg/l at the
end of Period 5. When the pH value had increased to 7.1,
feeding was started again, on day 360 (Period 6) at asomewhat higher OLR, 3.1 g COD/l day�1, and a shorter
HRT, 24 days, than before. The change in the operating
conditions was caused by changing to a batch of sludge
with a higher VS concentration, and by a reduction in the
sludge volume in the digester due to evaporation in the
previous period. During Period 6 stable operation was
achieved 15 days after the restart of feeding, under the
conditions presented in Fig. 2 and Table 3, but theconcentrations of VFA were high.
Finally, during Period 7 (day 405–440) the digester
was operated with lower OLRs around 1.2 g COD/l
day�1 and higher HRTs of 55–60 days (cf. Table 2 and
Fig. 2), in order to achieve a reduction of the VFA
concentrations. The average stabilization of COD, the
gas production, the percentage of methane in the biogas
and the pH-value all increased, to the values presentedin Table 3. The concentration of propionic acid in-
creased slightly, to 4500 mg/l. Due to the new start up
the level of acetic acid first decreased and then increased
to about 2000 mg/l and was still increasing at the end of
the experimental period. The concentrations of the
longer VFA decreased to below 500 mg/l.
3.2. Digester with diluted sludge
This digester was operated for a total of 74 days under
the conditions described in Section 2.5.2 and Fig. 3.
The digester was mainly operated at 30 days HRT
and the corresponding OLR of 1.1 g COD/l day�1.Feeding was started on day 7, but until day 28 the
loading was somewhat uneven (cf. Section 2.5.2). Gas
production started immediately after feeding was star-
ted, at 0.18 l/l day�1, corresponding to 0.16 l/g COD
added, and increased steadily to 0.30 l/l day�1 and 0.32
l/g COD added. However, the great difference between
the percentage of COD removed and the percentage of
COD methanised (cf. Table 5) indicates that the gas
production was measured 25–30% too low due to mea-
surement errors that not could be localized. Thus the
values provided for the gas and methane productionfrom the diluted sludge must be considered as uncertain.
The stabilization of COD varied first around 60% and
from day 39 stabilized at 60% (cf. Fig. 3), and the per-
centage of methane in the biogas stabilized at 58 vol.%
after 34 days of operation. The pH-value stabilized
slightly below pH 7. The concentration of propionic acid
was above 1000 mg/l during the first 25 days of opera-
tion, due to the propionic acid content of the inoculum(digested undiluted sludge). But, on day 30 it had de-
creased to about 100 mg/l, while the concentration of
acetic acid had increased to about 450 mg/l. Both con-
centrations stabilized at these levels throughout the
remainder of the operating period.
4. Discussion
4.1. Performance
The digesters were operated as low-loaded sewage
digesters, with HRTs in the upper range, and performedcorrespondingly with respect to stabilization of organic
matter, methane yield, volumetric methane production
rate and specific methane production rate (Metcalf &
Eddy, 1991; ATV, 1996). However, the digested undi-
luted sludge was not stabilized according to VFA-
criteria (demanded: VFA<1000 mg/l; Loll and M€oller,1984). The percentage of methane in the biogas was
lower than the usual 60% in biogas from sewage diges-tion, which indicates inhibition of lipid degradation. The
methane yield and, as far as provided, the removal of
organic matter were in accordance with the values from
the trout farming sludge measured by Kugelman and
Van Gorder (1991) for fresh water fish farming sludge,
provided that the values for the yields are corrected for
the different COD/VS ratios of the two types of sludge.
As expected, both the methane yield and the removaland degradation of organic matter (cf. Tables 5 and 3)
increased with increasing HRT, apart from the period
with the strong increase of the VFA, Period 4b in Fig. 2.
Anaerobic degradability (cf. Table 5) was, at compar-
able HRTs, similar during the digestion of undiluted
sludge and diluted sludge. This indicates that it pri-
marily depended on the composition of the sludge, and
that the inhibition presumably not affected the hydro-lytic and fermentative bacteria had.
The dilution of the sludge increased the COD re-
moval by at least 5%, corresponding to the lower VFA
164 R. Gebauer / Bioresource Technology 93 (2004) 155–167
concentrations in the digested sludge (cf. the periods 2b
in Tables 3 and 5). However, the methane yield did not
increase correspondingly, to values around 0.20 l/g COD
added. This raises doubts about whether the measured
value of 0.154 l/g COD added is correct (cf. comments in
Section 3.2 of the Results). From the presented values,
the methane yield and removal and degradation of or-
ganic matter for high rate CSTRs with 10–20 days ofHRT may be (linearly) extrapolated to about 0.10–0.12
l/g COD added, 35–40% and 53–56% respectively. Well-
functioning processes may achieve methane yields of
about 0.20 l/g COD added and COD removal and
degradation of 60–70%. The consequences of the results
for the configuration of full-scale plants are further
discussed in Section 4.7.
4.2. Process stability
The treatment process with undiluted sludge was too
unstable––due to strong inhibition––to be scaled up.
The inhibition and instability were indicated by high
concentrations of VFA (4.2–7.2 g/l as acetic acid), with
high propionate/acetate ratios of 2.4–3.7, that were farbeyond the value of 1.4 that Hill et al. (1987) proposed
as the threshold value for a stable digestion process. The
concentrations of isobutyric and isovaleric acid were
also far beyond the threshold value of 6 mg/l that Hill
and Holmberg (1988) proposed as an indicator for
process stability. However, because of the high alka-
linity in the digester sludge (cf. Table 4), the high con-
centrations of VFA did not cause process disturbance,due to acidification of the digester content. It is more
likely that the propionic acid directly inhibited the
hydrogenotrophic methanogens (Hobson and Shaw,
1976) and, probably, other bacterial groups active in the
digestion process.
The inhibition was overcome by dilution of the sludge
1:1 with tap water, and a stable process (propionate/
acetate ratio 0.1–0.3) with satisfactory VFA concentra-tions (<600 mg/l) could be achieved after 30 days of
operation (cf. Fig. 3 and Table 4). However, dilution will
increase both the digester size and thus the capital costs of
the treatment plant, and the energy demand for heating
the sludge to process temperature (cf. Section 4.7).
4.3. Reasons for inhibition
Previously, Soto et al. (1991) suggested that either
ammonia (up to 4 g NH4-N/l) or sulphide (beyond 40–
133 mg H2S/l) was the reason for the inhibition occur-
ring during the anaerobic treatment of saline (Na: 9.9
and 8.4 g/l respectively) seafood-processing wastewaters.
The inhibitory effect of the sodium was assumed to havebeen overcome through adaptation of the biomass and
by the antagonistic effects of other cations (Omil et al.,
1995). However, in the present study, the ammonia
concentration in the digester with undiluted sludge
(cf. Table 4) was only slightly above the reported
threshold levels of 1500–1900 mg/l for initial inhibition
of unadaptated suspended cultures (McCarty, 1964;
Melbinger and Donellon, 1971). In addition, the H2S
concentration was lower than the inhibitory 133 mg
H2S/l measured in the experiments by Soto et al. (1991)
(cf. Table 4), because of a higher COD:SO4-ratio in thefish farming sludge than in the seafood processing
wastewater, so that more sulphide was removed with the
biogas. Thus, in the present study, only the sodium, and
perhaps other salt-ions, could have been the main rea-
son for the strong inhibition. This assumption is sup-
ported first by the high concentration of propionic acid
in the digester, because the propionic acid-using bacteria
are more sensitive to sodium than the acetoclasticmethanogens (Liu and Boone, 1991; Feijoo et al., 1995),
and then by the fact that dilution to the moderately
inhibitory sodium concentration of 5.3 g/l (McCarty,
1964) enabled a stable digestion process.
4.4. Adaptation of the biomass
The process with undiluted sludge was strongly
inhibited even after more than 400 days of operation.
This indicates that only insignificant adaptation of the
biomass to the high sodium concentration can have
occurred, even if the sodium concentration was in-
creased gradually during start up (cf. Section 2.5.1). This
was in contrast to the results obtained by Soto et al.
(1991) and Omil et al. (1995, 1996), who both reportedsignificant adaptation, and indicates that the biomass
used in the present study did not contain species that
could tolerate high sodium concentrations. Thus, Shipin
et al. (1994) and Aspe et al. (1997) found little adapta-
tion in methanogenic cultures from low salinity environ-
ments, but considerable adaptation in cultures from
saline environments. This indicates that adaptation to
high sodium concentrations is more likely to happen asa result of selection of tolerant species than by adapta-
tion of every single microorganism. These tolerant spe-
cies were probably absent from the biomass used in
the present investigation, as the inoculum was taken
from low salinity environments (cf. Section 2.1 of the
Methods), the bacteria in the faeces in the sludge (sub-
strate) had mainly been exposed to the low salinity
environments (10–12‰) in the intestine, and the sea-water for the fish farm was pumped from 70 m depth
and had low bacteria concentrations. Additionally, the
storing at )28 �C may have been unfortunate for the
survival of salt tolerant methanogens.
4.5. Antagonistic effects
Because of the strong inhibition of the process, it is
unlikely that the other ions in the fish farming sludge
R. Gebauer / Bioresource Technology 93 (2004) 155–167 165
acted antagonistically on the sodium inhibition. This
result also goes against the observations of Soto et al.
(1991) and Omil et al. (1995, 1996), who reported sub-
stantial antagonistic effects during the treatment of
seafood processing wastewaters with the ion composi-
tion of: 12 g Na/l, 0.17 g K/l, 0.51 g Ca/l, 0.38 g Mg/l,
19.2 g Cl/l and 0.26 g SO4/l (Feijoo et al., 1995). How-
ever, this ion composition deviated significantly fromthat of the fish farming sludge used in the present
study (cf. Tables 1 and 4). In particular, the concentra-
tion of magnesium––which, according to Kugelman and
McCarty (1965), acts synergistically on sodium inhibi-
tion two-ion systems––was three times higher in the fish
farming sludge. This could explain the lack of antago-
nistic effects in the present investigation.
4.6. Development of active methanogenic biomass
The specific methane production rate of the biomass
was low throughout the whole operating period (cf.
Table 3). In contrast, Soto et al. (1991) and Omil et al.
(1996) could, during 100–357 days of treatment of saline
seafood processing wastewaters, increase the methane
production rates of the biomass by three to four times to
0.18 and 0.16 g COD/gVSS day�1 (corresponding to
0.063 and 0.056 l methane/gVSS day�1) from the samelow methane production rates as measured in the pres-
ent study (Omil et al., 1995). The different results may be
explained by the high particle content found in the
digesters with fish farming sludge. The particles prob-
ably reduced the contact between substrate and biomass
and thus prohibited biomass growth and development
of more active sludge. This indicates that low particle
content in the digester sludge may be a condition for thedevelopment of active methanogenic biomass.
4.7. Consequences for full-scale treatment plants
The main goals of the treatment process are stabil-
ization and hygienization of the sludge. Additionally,
the process may be interesting as a method for energy
production.
It was only possible to achieve stabilization, accord-
ing to VFA-criteria, in the process with diluted sludge;and the methane yield of this process––about 6.2 l/l
sludge estimated with the comment in Section 4.1––
would be sufficient to warm the sludge to process tem-
perature (required: 4.5 l/l sludge at incoming sludge
temperature of 1 �C). However, to reduce the reactor
size and the reactor costs treatment of diluted sludge
should be further investigated in a process configuration
with increased biomass retention as an anaerobic con-tact process, an AF or an UASB.
But, unless unexpensive external heat is available for
heating of the sludge to process temperature (see below),
treatment of undiluted sludge will give a greater net
energy production due to reduced energy demand for
heating. Therefore, it should be further investigated
whether stabilization of undiluted sludge may be
achieved through the use of an inoculum from a saline
environment, through a better adaptation regime during
start up, and/or by increasing biomass retention through
an anaerobic contact process. However, because of the
high particle content of the fish farming sludge it may bemost appropriate, to divide the treatment process in two
steps, as earlier proposed by Kugelman and Van Gorder
(1991): a first step in a CSTR for solubilisation and
acidification of the particulate organic matter, possibly
after it has been removed from the main stream, and a
second step in an AF or UASB for methanogenesis of
the dissolved organic substrate in the overflow from the
first step. In such a two-step process, both steps may beoptimised separately, both increasing the stabilization
and methane production and reducing the treatment
time and thus the reactor volumes and the costs for the
treatment plant.
It has to be further investigated whether sufficient
hygienization may be achieved by mesophilic anaerobic
treatment. So far, only thermophilic (55 �C) anaerobictreatment has been approved for hygienization. Thus, ifhygienization by pasteurisation were to be required,
only the methane production from digestion of undi-
luted sludge (10 l/l sludge, cf. Table 3) would be suffi-
cient to warm the sludge to 60 �C for pasteurisation
(requiring 8l methane/l sludge).
Today most Norwegian salmon farms operate at least
two to four salmon licences, but often one per single
location. Therefore a farm size of one salmon farm-ing licence, i.e. presently the licence to use 700 tons of
salmon dry feed per year (Norwegian Directorate of
Fisheries, 1996), is used to evaluate the consequences
of the results of the present investigation for full-scale
plants. As 15–20% of this feed will be recovered as
sludge dry matter, a salmon licence will discharge about
100 tons of VS/year. With a performance as in the
digesters of this investigation, the gross energy produc-tion from the collected sludge from one salmon farming
licence will be 180–250 MWh per year, while warming
of the sludge to process temperature will reduce the
energy production to 80 or 165 MWh/year. The net
energy production corresponds to the energy demand of
two to five Norwegian family households per year and
may be a significant contribution to the energy supply of
the small settlements often situated in the neighbour-hood of fish farms. Given an energy price of 0.4–0.5
NOK/kWh, the value of the net energy production
would be 32 000–82 500 NOK/year. However, with the
process configuration examined in this study, the
investment costs for the digestion plant (digester size
170–350 m3) would be around 1.5–2 million NOK
(Knap, 2002). Comparison of these numbers suggests
that the economic sustainability of the process requires
166 R. Gebauer / Bioresource Technology 93 (2004) 155–167
lower investment costs for the treatment plant, and thus
optimalisation of the process towards smaller digester
sizes, as suggested above. Additionally, economic sus-
tainability may be achieved if inexpensive external heat
is available to warm the sludge to process temperature,
as in cases where the fish farm is situated close to a
cooling or freezing facility.
5. Conclusions
• Anaerobic treatment of saline fish farming sludge
could reduce the COD content by between 36% and
60% and yielded a methane production of 0.114–
0.184 l methane/g COD added.• The gross and net energy production of the biogas
from one salmon farming licence would be 180–250
MWh/year and 80–165 MWh/year, respectively.
• The treatment process with undiluted sludge was
unstable due to strong inhibition and did not result
in stabilized sludge.
• The inhibition was most probably caused by sodium
and there were no signs of adaptation of the biomassor antagonistic effects of other ions.
• The high particle concentration in the digester most
probably prohibited the development of active meth-
anogenic biomass.
• The treatment process with diluted sludge (1:1 with
tap water) was stable, the sludge was stabilized and
the inhibition was overcome.
• For full-scale treatment of undiluted sludge a two-step process with inoculum from a saline environ-
ment should be investigated.
• For full-scale treatment of diluted sludge processes
with increased biomass retention should be investi-
gated.
• Treatment of both undiluted and diluted sludge may
be economically sustainable if inexpensive external
heat is available for warming of the sludge to processtemperature, for example from the condenser of a
cooling plant.
Acknowledgements
I would like to thank The Research Council of
Norway, The Technical University of Trondheim and
Finnmark University College in Alta for the financial
support of this investigation, and the Technical Uni-
versity of Norway for my working place. I would like to
thank Jon Fredrik Hanssen at The Agricultural Uni-
versity of Norway at �As for kindly providing the inoc-
ulum and Birgitte Ahring and Claus Nørgaard at TheTechnical University of Denmark for conducting the
bacterial analyses of the inoculum. I would like to thank
my former colleague at Finnmark University College
Rolf Erik Olsen for the fat analyses. I would also like to
thank Gunnar Hartvigsen at The University of Tromsø
for a good course in ‘‘Introduction to research’’ and my
fellow students Therese With-Berge, Marianne Stens-
rød, Jørgen Møllmann and Sveinn-Are Hanssen for
their valuable comments on the paper. Finally, I would
like to thank Ian Harkness for proofreading of the paper
and language corrections.
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