mesophilic anaerobic treatment of sludge from saline fish farm effluents with biogas production

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: [email protected] (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,

mail to: [email protected]

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


3 253–260 Semi-continuous operation 4000 1.9 65


4a 267–282 Second start up with sludge from the reactor,

increase of sludge volume

4000–6100 2.42 26.2


5 338–359 Stop of feeding 5100–4600 0 16a 360–363 Some feeding 4700–4900 1.44 48.1


6c 384–402 Semi-continuous operation 4800 3.12 24.0


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.


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).


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).


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.


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


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)


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


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


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


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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