Aquaculture 356–357 (2012) 328–341

Contents lists available at SciVerse ScienceDirect

Aquaculture
journal homepage: www.elsevier.com/locate/aqua-online

Incorporation of fish feed and growth of blue mussels (Mytilus edulis) in close
proximity to salmon (Salmo salar) aquaculture: Implications for integrated
multi-trophic aquaculture in Norwegian coastal waters
Aleksander Handå a, b,⁎, Hojune Min a, Xinxin Wang a, Ole Jacob Broch b, Kjell Inge Reitan b,
Helge Reinertsen a, Yngvar Olsen a
a
Norwegian University of Science and Technology (NTNU), Department of Biology, Centre of Fisheries and Aquaculture, N-7491 Trondheim, Norway
b
SINTEF Fisheries and Aquaculture, N-7465 Trondheim, Norway

a r t i c l e i n f o a b s t r a c t

Article history: The incorporation of fish feed wastes in digestive gland and mantle tissue and average growth in length and
Received 22 November 2011 standardized dry weight of soft tissue matter (DW′) of blue mussels (Mytilus edulis L.) were measured for one
Received in revised form 26 April 2012 year (June 2010–June 2011) at three experimental stations in close proximity to a salmon (Salmo salar) farm
Accepted 30 April 2012
at Tristein (63° 52′ N, 9° 37′ E) in Central Norway, with one on the west side (FW), one on the east side (FE)
Available online 11 May 2012
and one 100 m east of the farm (FE100), in addition to one reference station 4 km south of the farm.
Keywords:
A principal component analysis of fatty acid profiles clearly demonstrated the incorporation of fatty acids from
Mytilus edulis salmon fish feed in digestive gland and mantle tissue, identified by an increased content of 18:1 (n-9). The incor-
Salmon fish feed poration, and consequently the separation of mussels at stations close to the fish farm from mussels at the refer-
Fatty acids ence station, was more pronounced in February compared to August, while no clear differences were found in
Bivalve growth June.
Integrated multi-trophic aquaculture The growth in length correlated significantly to feed use at the fish farm (r = 0.89) and to the concentration of
suspended particulate matter (SPM) (r= 0.53) in the autumn–winter period (Oct–Feb) (pb 0.05). The mussels
at the reference station showed a significantly faster growth in length compared to the mussels at all stations
at the fish farm during the summer, while mussels at the FW station grew faster than the mussels at the reference
station during the spring (pb 0.05). The length growth was faster for mussels at the reference station than for
mussels at the FW and FE100 stations (pb 0.05), while no significant differences were found between mussels
at the reference and the FE stations for the entire year.
The DW′ was significantly positively correlated to the feed use at the fish farm stations (r= 0.53) (pb 0.05), and
the DW′ of mussels at stations at the fish farm was significantly higher compared to the DW′ of mussels at the
reference station in five months during autumn and winter (pb 0.05). The results suggest that the combined pro-
duction of mussels and salmon can be seen as a strategy to maintain a higher soft tissue content of mussels during
autumn and winter. Quantification of the mussel's assimilation capacities of farm-derived wastes at realistic scale
and under different environmental conditions is needed.
© 2012 Elsevier B.V. All rights reserved.

1. Introduction
The global salmonid production increased by around 60% from 1999
to 2009 (1.26 to 2.17 million tons), and further growth is expected (FAO,
2011). Atlantic salmon (Salmo salar) aquaculture accounts for the
majority of the salmonid production (1.44 million tons), with Norway,
Abbreviations: FW, Farm west (Station 1); FE, Farm east (Station 2); FE100, 100 m
east of farm (Station 3); AGRL, Average growth rate in length; SGRDW′, Specific growth
rate in soft tissue dry weight.
⁎ Corresponding author at: Norwegian University of Science and Technology (NTNU),
Department of Biology, Centre of Fisheries and Aquaculture, Brattørkaia 17B, N-7491
Trondheim, Norway. Tel.: +47 91577232; fax: +47 93270701.
E-mail address: aleksander.handa@sintef.no (A. Handå).
which doubled its production from 1999 to 2009 (0.43 to 0.86 mil-
lion tons), being the leading producer (FAO, 2011). The mean nutrient
release from Norwegian salmon aquaculture has been estimated at
61% of feed-N and 69% of feed-P. Out of this, 41% N and 19% P are re-
leased in a dissolved form, while 20% N and 50% P are released in partic-
ulate form (Olsen et al., 2008). The theoretical mean nutrient dispersal
from a Norwegian salmon farm producing 5000 t fish (FCR= 1.15, 6%
N and 0.9% P content in feed) is accordingly: 141 t dissolved inorganic
N, 10 t dissolved inorganic P, 69 t particulate organic N and 26 t particu-
late organic P.
There is an increasing concern regarding the potentially negative en-
vironmental impacts that nutrient wastes from marine aquaculture
may cause (Amberg and Hall, 2008; Braaten, 2007; FAO, 2009; Tett,
2008), and one of the major challenges for the sustainable development

0044-8486/$ – see front matter © 2012 Elsevier B.V. All rights reserved.
doi:10.1016/j.aquaculture.2012.04.048
 A. Handå et al. / Aquaculture 356–357 (2012) 328–341
of salmonid cage mariculture is to minimize discharge of wastes
that potentially can lead to degradation of the marine environment
(Cheshuk et al., 2003). For example, the sedimentation of particulate
matter may cause the organic enrichment of sediments (Carroll et al.,
2003; Jusup et al., 2007; Kutti et al., 2007; Stigebrandt et al., 2004),
which may have a negative effect on the benthic community if sedi-
mentation rates exceed the turnover rate of the community (Holmer
et al., 2005; Kalantzi and Karakassis, 2006), while dissolved nutrients
may cause eutrophication (Cloern, 2001; Folke et al., 1994; Nixon,
1995; Skogen et al., 2009).
For the purpose of minimizing the potentially negative effects of
waste discharges it has been suggested to cultivate extractive and filter
feeding species at lower trophic levels in close vicinity to the fish farms, a
strategy termed IMTA, or integrated multi-trophic aquaculture. IMTA is
used as a means of obtaining increased biomass production, thus adding
to the value of feed investments, and at the same time contributing to a
more sustainable aquaculture production (Chopin et al., 2001; Chopin et
al., 2008; Neori, 2008; Neori et al., 2004; Troell et al., 2003, 2009).
The dissolved inorganic nutrient wastes can be taken up by inor-
ganic extractive species such as seaweeds (Buschmann et al., 2001;
Chopin et al., 2001; Chopin et al., 2004), while released particulate or-
ganic nutrients can be consumed by filter feeding species such as
mussels. Several studies have suggested that bivalve filter feeders
can provide bioremediative services when co-cultivated with fish
aquaculture (Folke and Kautsky, 1989; Folke et al., 1994; Gao et al.,
2008; Mazzola and Sara, 2001; Peharda et al., 2007; Soto and Mena,
1999; Troell and Norberg, 1998; Whitmarsh et al., 2006), hence re-
ducing the environmental impact associated with a great release of
particulate organic matter from marine cage aquaculture (Cheshuk
et al., 2003 and references therein). However, little is known about
how particulate wastes from salmon farming may affect shellfish
growth (MacDonald et al., 2011).
While many studies have reported a better growth for mussels
grown adjacent to cage fish farms (Lander et al., 2004; Peharda et al.,
2007; Sara et al., 2009; Stirling and Okumus, 1995; Wallace, 1980),
others have failed to demonstrate such an effect (Cheshuk et al., 2003;
Navarrete-Mier et al., 2010; Taylor et al., 1992). These authors instead
suggest that the distance from the farms does not substantially influ-
ence food availability and growth of mussels. Previous research has
suggested several possible explanations for the lack of a distinct growth
response in mussels co-cultivated with fish cage aquaculture. The ex-
planations given are that: a) the particulate wastes of the fish farms
do not increase the seston concentrations significantly above ambient
levels, b) that the ambient seston concentrations remain consistently
above the pseudofeces threshold level, thereby limiting the potential
of mussels to increase their growth by feeding upon fish farm wastes
(Cheshuk et al., 2003), c) that the mussels' filtering response is to
slow to adapt to pulsed feeding regimes accompanied by d) non-
uniform effluents from salmon farms leaving mussels to only ingest
farm particulate wastes when natural seston concentrations are scarce,
and e) that spatial and temporal differences in hydrodynamic condi-
tions between sites, in addition to the experimental design, differ in
ways which make it difficult to obtain univocal conclusions for the
IMTA concept (Troell and Norberg, 1998; Troell et al., 2009, 2011). Con-
flicting results bring some uncertainty as to how efficiently blue mus-
sels can reduce the organic load from fish cage aquaculture; there is
hence a need to further investigate on the ability of mussels to incorpo-
rate and grow based on salmon fish feed and feces particles.
Blue mussels have been shown to clear salmon fish feed and feces
quite efficiently (Handå et al., submitted for publication; MacDonald
et al., 2011; Reid et al., 2010). Additionally, changes in fatty acid compo-
sition in the direction of the food source profile have demonstrated the
assimilation of salmon feed and feces in bivalve tissues (Gao et al., 2006;
Handå et al., submitted for publication; Redmond et al., 2010). Fish
feed has traditionally contained a high percentage of the fatty acids
20:1 (n-9) and 22:1 (n-11). There has been an increasing use of
329
terrestrial lipid sources with high proportions of, e.g. 18:1 (n-9) and
18:2 (n-6) in fish feed in recent years (Dalsgaard et al., 2003; Narváez
et al., 2008; Skog et al., 2003) which can be used as tracer fatty acids
for the incorporation of salmon feed. Significant changes in the propor-
tions of these fatty acids have been found to take place within 28 days in
the digestive gland (Handå et al., submitted for publication; Redmond
et al., 2010) and within 90 days in mantle tissue (Fukumori et al.,
2008; Post, 2002) of mussels. However, little is known about the
seasonal-dependent incorporation of salmon fish feed wastes and the
corresponding growth in bivalves under natural farming conditions.
The primary objectives of this study were to investigate the annual
and the seasonal-dependent incorporation of fish feed waste and
growth of blue mussels (Mytilus edulis) in close proximity to salmon
(S. salar) aquaculture in coastal waters of Central Norway.
2. Material and methods
2.1. Location and sampling program
Seston variables and mussel growth were measured monthly for
one year (June 2010–June 2011) at three experimental stations in
close proximity to a salmon farm at Tristein (63° 52′ N, 9° 37′ E) outside
the Trondheimsfjord, at the coast off Central Norway, with one station
on the west side (FW), one on the east side (FW), one 100 m east of
the farm (FE100), and a reference station 4 km south of the farm
(Fig. 1). The distance between the fish cages and the mussels was ap-
proximately 60 m for the FW and the FE station and 120 m for the
FE100 station. Hydrodynamic simulations were undertaken to deter-
mine the best location of the sampling stations (see Section 2.7). Fatty
acids were analyzed for salmon fish feed sampled from the feed barge
in December 2010 and June 2011, and from mussels' digestive glands
and mantle tissue in June and August 2011 and February and June 2011.
2.2. Salmon farm and area description
The fish farm consisted of eight Polar circle plastic cages (Fig. 1),
each with a circumference of 157 m, with 15 m deep net pens and a vol-
ume of 36.000 m 3. The total salmon production was 4.705 t, and the
corresponding use of feed was 5.216 t during the sampling period
(Fig. 2A). The cage on the west side, where station FW was located, con-
tained only mussels (no fish) during the experiment. The western side
of the farm was situated above the 50 m isobath, with the bottom slop-
ing steeply down to approximately 100 m on the eastern side. Although
the farm was situated approximately 4 km off shore of the main land,
it was sheltered from the ocean by the skerries of Tristeinen on the
western and northern sides. The area surrounding the Tristeinen skerries
is dominated by marine waters (salinity b34.5‰) from the Norwegian
coastal current, with temporary outflows of fresh surface water from
the Trondheimsfjord.
2.3. Environmental and seston variables
The temperature and salinity were measured at a depth of 2 m with
a CTD (SD 204, SAIV LTD, Norway), while integrated water samples for
the analysis of suspended particulate matter (SPM), particulate organic
carbon (POC), nitrogen (PON) and chlorophyll a (Chl a) were taken
from a depth of 0–8 m by mixing four consecutive samples (0–2, 2–4,
4–6 and 6–8 m) taken with a Ramberg water collector (L; 2 m, V; 5 L)
in a bucket prior to filtration. The samples were pre-filtered with a
200 μm net prior to a second filtration of 2 L with pre-combusted and
weighed Whatman GF/C filters. The SPM was measured in parallel
after drying the filters for 48 h at 70 °C, while 1/16 of two other filters
was punched out in parallel and stored at −81 °C for analysis of Chl a,
POC and PON. The Chl a was extracted with methanol and placed in a
refrigerator for 2 h prior to measurement of in vitro fluorescence with
a Turner Design Fluorometer according to Strickland and Parsons
330 A. Handå et al. / Aquaculture 356–357 (2012) 328–341

Fig. 1. Geographical location of the salmon farm and the experimental stations at the west (FW) and east (FE) side of the farm, 100 m east (FE100) and at the reference station (RS)
4 km south of the farm at Tristein in Central Norway.

(1968). POC and PON were analyzed by a Carlo Erba analyzer, model NA
1106 CHN.
2.4. Growth measurements
The shell length (L) (n = 25) was measured with a digital caliper
on individually marked mussels kept in rectangular net pots
(0.7 × 0.4 × 0.2 m) at a depth of 2 m. Changes in soft tissue dry weight
(DW) (n= 30) were represented using a condition index standardized
to a certain length L′ according to Bayne and Worrall (1980) and
Bonardelli and Himmelman (1995). The DW was measured with an
electronic weight (Mettler Toledo Precisa 180A) after drying the tissue
at 60 °C in a Termaks heat cabinet for 48 h, which was then calculated as
a standardized dry weight (DW′) by the following equation:

b b

DW′ ¼ DW L′ =L ð1Þ

A
500 Feed use 2400
Fish biomass
2000
Fish biomass (tons)

400
Feed use (tons)

1600
300
1200
200
800
100 400

0 0

B 14 36
Salinity
12 34
Temperature (°C)

Salinity (ppm)

10 32
30
8
Temperature 28
6 FE 26
4 FE
24
FE100
2 22
RS
0 20
Jun Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr May Jun Jul

Fig. 2. A) Fish biomass (right axis) and feed use (left axis) from June 2010 to June 2011, and B) temperature and salinity at 2 m depth at the west (FW) and east (FE) side of the farm,
100 m east (FE100) and at the reference station (RS) 4 km south of the farm from June 2010 to June 2011.
 A. Handå et al. / Aquaculture 356–357 (2012) 328–341
where DW is the weight in mg, L the length in mm and b the slope of
the log10 DW plotted as a function of log10 L. The DW′ corresponds to
the condition index, and was scaled so it equaled the DW when L equals
L′. L′ was set to 40 mm based on an average shell length of 40.4 ±
0.1 mm (n= 1200 measurements) during the sample period.
The specific growth rate (μ, day − 1) in DW′ (SGRDW′) was calculat-
ed by the equation:
μ ¼ ð ln DW′t − ln DW′0 Þ=t
where DW′0 and DW′t are the DW′ at the start and end of each period,
respectively, and t is the time in days. The percentage growth per day
(P) was calculated by the equation:
P ¼ 100  ð expðμ Þ−1Þ
The average rate of length increase (μm, day − 1) (AGRL) was calcu-
lated by the equation:
μm ¼ ðLt −L0 Þ=t
where L0 and Lt are L at the start and end of each period, respectively,
and t is the time in days. The initial shell length was 30.5–32.5 mm
(mean 31 ± 0.07 mm, n = 100).
The mussels originated from a suspended longline farm in the
Åfjord (63° 56′ N, 10° 11′ E) 30 km away.
2.5. Fatty acid analysis
The total lipids were extracted according to Bligh and Dyer (1959),
followed by an analysis of fatty acids after handling the samples
according to Metcalfe et al. (1966) (see Handå et al., submitted for
publication).
2.6. Data analysis
Data for the specific growth in DW′ (SGRDW′) and the average growth
in length (AGRL) were tested for normality using a Kolmogorov–Smirnov
test, and for the homogeneity of variance using a Levene's test. The equal-
ity of means for total fatty acid content (mg g− 1 dry weight) and the
relative content of identified fatty acids (% of total fatty acids) of digestive
gland and mantle tissue between June 2010 (Month 1), August (Month
3), February (Month 8) and June 2011 (Month 12), in addition to between
the different stations on each sampling day were tested using a
Kolmogorov–Smirnov test. The equality of means for SGRDW′ and AGRL
between sampling stations and sampling days, as well as between sum-
mer (June–September), autumn (October–November), winter (Decem-
ber–February) and spring (March–May), were tested using a one-way
ANOVA followed by post hoc comparisons by Tamhane's T2, not assum-
ing equal variances. The significance limit was set at 0.05 and the means
were given with the standard error. A Spearman's correlation analysis
was performed on seston data and mussel growth for the entire year
and for the five-month autumn–winter period from October to
February.
Statistical analyses were performed using SPSS (rel. 17.0, Chicago,
SPSS Inc.), while a principal component analysis (PCA) for fatty acid
composition was performed with an Unscrambler, version 9.8 2008
(Camo Software AS). Data was analyzed without weighing, leaving
the PCA for each tissue to be dominated by the fatty acids that dom-
inated the fatty acid composition. Missing measurement points in
the time plots were estimated by linear interpolation between the
two closest measurement points.
2.7. Hydrodynamical model
The coupled 3D hydrodynamic-biological model system SINMOD
was used for the hydrodynamic modeling. The hydrodynamic part of
331
the model is based on the primitive Navier–Stokes equations, which
are solved by a finite difference scheme. Detailed model descriptions
are given in Støle-Hansen and Slagstad (1991) and Slagstad and
McClimans (2005).
Boundary conditions are generated through a four step nesting pro-
cedure using consecutively finer grids from 20,000 m to 4000 m to
800 m to 160 m and finally to 32 m. A model of 32 m horizontal resolu-
tion was set up for the area surrounding the ACE facility (Fig. 1). A total
ð2Þ of 21 vertical layers were used in the 32 m model domain, with the sur-
face layer up to 3 m deep, and further depths of: 3–3.5, 3.5–4, 4–5, 5–6,
6–7, 7–8, 8–10, 10–12, 12–15, 15–20, 20–25, 30–35, 35–40, 40–50,
50–75, 75–100, 100–150, 150–200, 200–250 and 250–300 m. The
greatest depth in the model domain was 279.54 m. The coarser models
ð3Þ use up to 42 vertical layers.
Atmospheric forcing data were extracted from the eKlima data-
base (Norwegian Meteorological Institute). Data for the station at
Ørlandet (63° 42′ N, 9° 36′ E; elevation: 10 m) for 2010 and 2011
were used.
ð4Þ
3. Results
3.1. Environmental and seston variables
The water temperature ranged between 4 °C in February and
13.6 °C in August, with an average of 7.9 ± 0.5 °C for the entire year
(Fig. 2B). On average, the salinity decreased from 28.5‰ down to
21.7‰ in July, followed by a rapid increase before leveling off and
remaining stable >32‰ from October over the winter (Fig. 2B).
The hydrodynamic simulations indicated that the current speed of
the surface water at the FE100 and the reference stations generally
was between 0 and 0.2 m s− 1 (in June 2010, August 2010 and February
2011) (Fig. 3A), with the exception of FE100 in August, when the cur-
rent speeds were between 0.2 and 0.5 m s − 1 almost 20% of the time.
The direction of the surface current was generally from the farm to
the FE100 station (Fig. 3B).
The concentration of suspended particulate matter ranged between
5.2 and 11.2 mg L − 1, with an average of 8.4 ± 0.2 mg L − 1 for the entire
year (Fig. 4A) and demonstrated a similar pattern of variation as the use
of feed at the fish farm, with minimum concentrations in December–
January and occasional peaks in September and February. The concen-
tration was significantly positively correlated to the feed use at the
fish farm during the autumn–winter period (October–February)
(r= 0.53) (pb 0.05). Coincidently, high values of SPM and Chl a during
spring (March–May) resulted in a moderate correlation with Chl a for
the entire year (r = 0.34) (pb 0.05).
The POC concentrations ranged between 70 and 740 μg C L − 1,
with an average of 266 ± 23 μg C L − 1, and were negatively correlated
to feed use at the fish farm (r = − 0.36) for the entire year while, in
contrast, the POC concentrations were positively correlated to feed
use during the autumn–winter period (r = 0.40) (p b 0.05) (Fig. 4B).
The Chl a concentrations ranged between 0.06 and 18.6 μg L − 1,
but were generally low, with an average of 2.2 ± 0.5 μg L − 1 for the
entire year, values b0.6 μg L − 1 during the autumn–winter period
(Fig. 4C), and peak values in May. The Chl a values were positively
correlated to POC (r = 0.73) and PON (r = 0.82), and negatively corre-
lated to the feed use at the fish farm (r = −0.32) (p b 0.05). The SPM:
Chl a ratio (mg/μg) ranged between 0.5 and 107, with peak values
during winter when the Chl a concentrations were at a minimum
(Fig. 4D). The ratio was moderately correlated to feed use at the fish
farm over the year (r = 0.32) (p b 0.05).
3.2. Growth in length
The mussels showed a rapid average growth in length for the five-
month period from June to October before the growth leveled off
and remained low in winter, followed by a steady increase in the
332 A. Handå et al. / Aquaculture 356–357 (2012) 328–341

A 12
10

SPM (mg L-1)

8
6
4 FW
FE
2 FE100
RS
0

B 1000
FW

POC (µg L-1)

FE
800 FE100
RS
600

400

200

0 -1

C 20
FW
FE

Chl a (µg L-1)

15 FE100
RS

10

D 120 FW
100 FE
SPM:Chl a

FE100
80 RS
60
40
20
0
Fig. 3. A) Simulated surface water current situation at the ACE farm for February 15 to 21, Jun Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr May Jun Jul
2011. The area presented is 3.2 by 3.2 km. The arrows indicated the direction of the cur-
rent field, while their lengths indicate current speed; the thick blue line segment in the Fig. 4. A) Suspended particulate matter (SPM), B) particulate organic carbon (POC),
middle shows the scale of a speed of 0.2 m s− 1. The thick red curves indicate 50, 100 C) chlorophyll a (Chl a) and D) ratios of SPM over Chl a (mg:μg) in integrated samples
and 150 m isobaths. B) Probability of simulated surface current speeds at stations FE100 (0–8 m depth) at the west (FW) and east (FE) side of the farm, 100 m east (FE100) and
and RS in June 2010 (J), August 2010 (A) and February 2011 (F). The colors indicate rela- at the reference station (RS) 4 km south of the farm from June 2010 to June 2011.
tive frequency of simulation samples with current speeds in the intervals indicated below
the bars for the given months and locations.

the mussels at the FW and FE100 stations, while no significant differ-

spring (Fig. 5A). The average growth rate ranged between 0.1 and
125 μm day − 1 within single months and the growth was generally
high during summer (June–September) and low in autumn and win-
ter (October–February) (Fig. 5A). The growth was significantly higher
at the reference station compared to the stations at the fish farm in
June–July, whereas the opposite was evident in May–June when the
mussels at all stations at the fish farm grew faster than the mussels
at the reference station (p b 0.05). The mussels at the reference station
grew faster than the mussels at the FE100 station in the autumn–winter
period and in April–May, while mussels at the FW and FE stations inside
the farm grew faster than the mussels at the FE100 station in Novem-
ber–January and April–May (pb 0.05). A comparison of the different
seasons revealed that the mussels at the reference station showed a
faster growth in length compared to the mussels at all stations at the
fish farm during the summer, while mussels at the FW station grew
faster than the mussels at the reference station during the spring
(pb 0.05) (Fig. 5B). A comparison of the average growth rates for the en-
tire year revealed that mussels at the reference station grew faster than
ences were found between mussels at the reference and the FE stations.
At the fish farm, mussels at the FW station grew faster than the mussels
at the FE station during autumn and at the FE100 station during winter
and spring (pb 0.05).
The average growth in length for all stations was strongly correlated
to temperature (r= 0.73), moderately to POC (r = 0.53), PON (r= 0.6)
and Chl a (r= 0.43) and weakly to SPM (0.37) (pb 0.059), over the en-
tire year. While no correlation was found between the growth in length
and feed use over the entire year, there was a significant positive corre-
lation in the autumn–winter period (r= 0.89), when a correspondingly
high correlation to SPM was also found (r= 0.53) (pb 0.05).
3.3. Growth in soft tissue
The standardized dry weight of soft tissue matter (DW′) ranged
between 290 and 722 mg ind − 1 with an average of 517 ± 15 mg,
and it exhibited a rapid increase in the summer, reaching peak values
at the FW and the FE100 stations in September and at the FE and the
 A. Handå et al. / Aquaculture 356–357 (2012) 328–341 333

A 160
A 800
FW * *a FW
FE a FE
140 a FE100 * * FE100
a 1
** a RS 700 a
RS
a
* 1,2
120 A 2
2 *
AGRL (µm day-1)

b I
600 B *
100 B X

DW' (mg)
XY
II XY
II
80 b
b
b 500
Y
**
III x
b

60 y

400 z
*x * *
40 x x x
z

xy xy
A
20 A y
y
300
1
1,21,2
I 2
II II
BB III
0
Jun un-Jul ul-Aug ug-Sep ep-Oct ct-Nov ov-Jan an-Feb b-Mar ar-Apr r-May ay-Jun 200
J J A S O N J Fe M Ap M Jun-10 Jul Aug Sep Oct Nov Des Jan Feb Mar Apr May Jun-11

B 160 B 1.0 FW
FW FE
0.8 FE100
140 FE
FE100 0.6 RS

SGRDW'
RS 0.4
120 ** 0.2
AGRL (µm day-1)

a
0.0
100 -0.2
b
-0.4
80 b
-0.6
b
Summer Autumn Winter Spring
60
Fig. 6. A) Soft tissue dry weight of mussels (DW′) at the west (FW) and east (FE) side of
X
40 * Y
XY the farm, 100 m east (FE100) and at the reference station (RS) 4 km south of the farm
A 1 Y
AC 1,2 from June 2010 to June 2011, and B) SGRDW′ by season and the entire year (mean± se,
2
20 B
BC 2
n=30). Letters and numbers denote significant differences within months. * indicates a sig-
I I,II I,II
II
nificantly higher DW′ at stations at the salmon farm compared to the reference station
within months. ** indicates a significantly higher DW′ at the reference station compared
0
) ) ) ) . to stations at the salmon farm within months (p b 0.05).
(J-S (S-N N-M M-J (J-J)
mer umn ter ( ng ( year
Sum Aut Win Spri One

Fig. 5. A) Shell length (L) (right axis) and average growth in length (AGRL, μm day− 1) (left 3.4. Incorporation of fatty acids in mussel tissues
axis) at the west (FW) and east (FE) side of the farm, 100 m east (FE100) and at the
reference station (RS) 4 km south of the farm from June 2010 to June 2011, and B) average
3.4.1. PCA
growth in length (AGRL, μm day− 1) by season and the entire year (mean ± se, n = 25).
Letters and numbers denote significant differences within months. * indicates a sig-
The PCA of fatty acid (FA) profiles indicated a seasonal-dependent
nificantly higher AGRL at stations at the salmon farm compared to the reference station. incorporation of salmon fish feed in digestive gland and mantle tissue
** indicates a significantly higher AGRL at the reference station compared to stations at in mussels, identified by an increased content of percent 18:1 (n-9) of
the salmon farm within months (p b 0.05). total fatty acids. The PCA also revealed an increase in 20:1 (n-9) that
could be partly related to the incorporation of fish feed. Mussels at the
fish farm was weakly separated from mussels at the reference station
in August and strongly in February (Fig. 7A), while no systematic pat-
tern of variation or separation of stations at the fish farm from the
reference stations in October, followed by weight losses in November reference station was found in June (Fig. 7B). The score plot (Fig. 7A,
and December (Fig. 6A,B). Occasionally, increases were found in the upper panel) for the digestive gland tissue showed that 92% of the var-
period from January to May and a major decrease associated with iance in the data was explained by the two first principal components.
spawning was evident at the FW, FE and the FE100 stations in June. A similar pattern of variation as in the digestive gland tissue was
This decrease left the mussels at the reference station with a signifi- also found for the mantle tissue. The fatty acid profile changed in the
cantly higher DW′ compared to that at the fish farm (p b 0.05), as op- direction of the salmon feed profile from the start in June to August
posed to for the length growth, thus contributing to a significant and February (Fig. 7C), whereas no systematic pattern of variation or
correlation between the SGRDW′ and the growth in length (r = 0.46) separation of stations at the fish farm from the reference station was
(p b 0.05). found in June (Fig. 7D). The changes were more pronounced in the di-
The DW′ was significantly positively correlated to the use of feed at rection of the salmon feed signature in February compared to August,
the fish farm (r= 0.53) (pb 0.05), and the DW′ of mussels at one or although no clear separation was found between the reference station
more of the stations at the fish farm was higher compared to the DW′ and the stations at the fish farm. The score plot (Fig. 7C, upper panel)
of mussels at the reference station in August (at the FW station), showed that 83% of the variance in the data was explained by the two
September (at the FW, FE and F100 stations), October (at the FE sta- first principal components.
tion), December ( at the FW, FE and F100 stations) and February (at In the digestive gland samples, the loading plots (Fig. 7A, lower
the FE station) (pb 0.05). The average SGRDW′ was positive at all the sta- panel) confirmed the incorporation of 18:1 (n-9) and 20:1 (n-9) in
tions in summer and negative during autumn. The mussels at the fish August and February. 20:5 (n-3) (eicosapentaenoic acid, EPA) and
farm stations displayed a negative SGRDW′ in winter and spring while 16:1 (n-7) were the dominant fatty acids at the start, while 18:4 (n-3)
a positive SGRDW′ was found for mussels at the reference station. and 14:0 contributed more to the total FA profile in mussels in August.
334 A. Handå et al. / Aquaculture 356–357 (2012) 328–341

22:6 (n-3) (docosahexaenoic acid, DHA) contributed more to the total
FA profile in mussels at the reference station in February, thereby sepa-
rating the mussels in February from the mussels in August together
with 20:1 (n-9). 16:0 and 18:2 (n-6), which also contributed to chang-
ing the profile in mussels in August and February from the mussels at
the start.
The loading plots also confirmed the incorporation of 18:1 (n-9)
and 20:1 (n-9) in August and February in the mantle tissue (Fig. 7C,
lower panel), but the pattern was not as evident as for the digestive
gland samples (Fig. 7). The FA profile was dominated by EPA and 16:0
at the start, while 20:1 (n-9), 18:2 (n-6) and 18:4 (n-3) contributed
more to the total FA profile in mussels in August. As for the digestive
gland samples, DHA contributed more to the total FA profile in mussels
in February, separating mussels in February from mussels in August in
combination with 16:1 (n-7) and 18:1 (n-9).
3.4.2. Digestive gland
The general pattern of variation of the total FA content (mg/g), which
reflects the content of total lipids, demonstrated an increase from the
start in June until August, before a decrease was found in February and
at the end of the sampling period in June (Fig. 8A). The seasonal changes
were significant at the FE, FE100 and the reference stations (pb 0.05). No
differences were found for the total FA content in mussels at any of the
stations in August and February. The total FA content was also higher at
the FW compared to the FE and the FE100 stations (pb 0.05), while no
statistical differences were found between the total FA content of the di-
gestive gland tissue of mussels at the FW and the reference station at the
end of the sampling period.
The PCA particularly identified 18:1 (n-9), 20:1 (n-9), DHA, EPA and
18:4 (n-3) as the single fatty acids that were most responsible for the
difference between the digestive gland tissue of mussels at the start in
June and in August and February. The content of 18:1 (n-9) and 20:1
(n-9), as well as 18:2 (n-6), which was present in high amounts in
fish feed, exhibited a similar pattern of variation as the total FA (or
lipid) content of the digestive gland tissue over the year (Fig. 8A). The
content of 18:1 (n-9) in digestive gland tissue was significantly higher
in mussels at the FE station compared to the reference station in
February, and significantly higher in mussels at the FW station com-
pared to mussels at the FE, FE100 and the reference stations at the
end of the sampling period in June (pb 0.05). In contrast, the content
of 20:1 (n-9) was significantly higher in the digestive gland tissue of
mussels at the FE and the FE100 stations compared to mussels at the
FW and the reference stations in June (p= 0.05), while the content of
18:2 (n-6) was significantly higher in mussels at the FW station com-
pared to mussels at the reference station in February (pb 0.05) (Fig. 8A).
The content of 18:1 (n-9) of the total FA in the digestive gland tis-
sue increased from 1.7 ± 0.1% at the start to a maximum of 10 ± 0.3%
in mussels at the FE station, which reflected the high content of this
FA in the fish feed (39 ± 0.2%), while the contribution of 18:2 (n-6)
increased from 1.8 ± 0% to a maximum of 3.4 ± 0.1% at the FW station

Fig. 7. A, C) Principal component analysis of fatty acid profiles in digestive gland and mantle tissue of mussels at the west (FW) and east (FE) side of the farm, 100 m east (FE100)
and at the reference station (RS) 4 km south of the farm in June 2010, August and February, and B, D) June 2011. The upper panels show the score plot, while the lower panels show
loading plots for the corresponding fatty acids' contribution to the score plot. Numbers at the x (PC-1)- and y-axis (PC-2) are the percentages of variance in fatty acid profiles
explained by principal components 1 and 2.
 A. Handå et al. / Aquaculture 356–357 (2012) 328–341
Fig. 7 (continued).
in February. 20:1 (n-9) increased from 1.3 ± 0.0% to an average of
4.5 ± 2.2% for all stations in February, exceeding that of the fish feed
(3.1 ± 0%).
3.4.3. Mantle
A similar pattern of variation of 18:1 (n-9), 20:1 (n-9) and 18:2 (n-6)
as was found for the digestive gland tissue was also found for the mantle
tissue, though with some greater variation (Fig. 8B). The total FA content
of mussels at the FW station remained stable over the year, while an in-
crease was found for mussels at the FE and FE100 stations, which
resulted in a significantly higher FA content compared to that of mussels
at the FW and the reference stations at the end of the sampling period
(pb 0.05).
4. Discussion
4.1. Food availability
The concentrations of suspended particulate matter at all stations
ranged consistently above the threshold level of 4 mg L − 1 for pseudo-
feces production in mussels of 1 g of soft tissue dry matter (Widdows
et al., 1979), suggesting that the SPM concentrations did not restrict
mussel growth at any time of the year. Furthermore, the significant
correlation between SPM and the feed use at the fish farm during the
autumn–winter (October–February) period suggested that the mussels'
food availability could be associated with the release of fish feed wastes
during this period. The organic content of the SPM, particularly the car-
bon, is a feed variable that largely determines the amount of surplus
energy available for growth (Bayne et al., 1987; Hawkins et al., 1997;
335
Navarro et al., 2003), and because mussels have shown the same
absorption efficiency for particulate organic C, N and P, respectively,
their growth will depend on the nutritional composition of the
absorbed organic matter and how this meets the mussels' nutritional
requirements (Hawkins et al., 1997).
As was found for SPM, the POC concentrations correlated well to
the use of feed in winter. According to an estimated minimum feed
requirement of 240 μg C ind − 1 h − 1 at 7°C and 570 μg C ind − 1 h − 1
at 14°C for the weight maintenance of mussels with 500 mg DW of
soft tissue matter from this population (Handå et al., in press), the
POC concentrations were found to support weight maintenance
and/or growth over the entire year. Even the minimum POC concen-
trations in January (95 ± 11 μg C L − 1) would leave the mussels with
a feed intake of 247 μg C ind − 1 h − 1, given a clearance rate of 2.6 L
ind − 1 h − 1, which has been found for mussels of this size (40 mm)
from this population (Handå et al., submitted for publication). Indeed,
the temperature in January was 5°C, suggesting a 30% lower
temperature-dependent feed requirement of only 168 μg C ind− 1 h− 1,
allowing the mussels to increase their soft tissue weight during winter.
In contrast, the Chl a concentrations remained below 0.6 μg L − 1
from October to February, suggesting that the food availability in
terms of Chl a might not have met the mussels' energy requirements
as a zero net energy balance is found to be sustained in M. edulis by
Chl a values between 0.67 and 1.02 μg L − 1 (Hawkins et al., 1999). Filter-
ing activity has previously been observed to cease below a Chl a con-
centration of 0.3–0.6 μg L− 1 (Dolmer, 2000; Norén et al., 1999; Riisgård
and Larsen, 2001), whereas in a recent study by Strohmeier et al.
(2009), it was demonstrated that M. edulis is capable of clearing particles
out of suspension at Chl a concentrations down to 0.01 μg Chl a L− 1,
336 A. Handå et al. / Aquaculture 356–357 (2012) 328–341

A Digestive gland
400 40
Total FA 18:1 (n-9)
38

Total fatty acids (mg g DW-1)

FW FW

Fatty acids (% of total FA)

FE 36 FE
300 FE100 FE100
RS
A*
14 RS
A*
A 12
1*
200 1 10 A
1* A* A* 1,2 1,2*
a
* 8 2*
1* 1* a
b*
6
100 b* a*
b* 4 b* b*
2 *

0 0
Jun-10 Aug Feb Jun-11 Fish feed Jun-10 Aug Feb Jun-11 Fish feed
8 13
20:1 (n-9) 18:2 (n-6)
FW FW
Fatty acids (% of total FA)

Fatty acids (% of total FA)

FE 12 FE
6 FE100 FE100
RS 4 RS
1 1 1* 1
1*
a*a 1,2* a
4 3 1,2
A A* a
A* b* A 2
A b
A* 2 a*
* a
2
* 1

0 0
Jun-10 Aug Feb Jun-11 Fish feed Jun-10 Aug Feb Jun-11 Fish feed

B Mantle
400 40
Total FA 18:1 (n-9)
Total fatty acids (mg g DW-1)

FW 38 FW
Fatty acids (% of total FA)

FE 36 FE
300 FE100 FE100
RS 14 RS
12
200 10
a
8 1
1* a* a
1* 1
b* 6 1 1
100 A 1 1 a
* A 4 a
A* c c AA A
2
0 0
Jun-10 Aug Feb Jun-11 Fish feed Jun-10 Aug Feb Jun-11 Fish feed
8 13
20:1 (n-9) 18:2 (n-6)
FW FW
Fatty acids (% of total FA)

Fatty acids (% of total FA)

FE 12 FE
6 FE100 1 FE100
RS 4 RS
A
1
11 aa 3
4 A A a
a a
1 a a
2 1 1 a
AA A
2 1

0 0
Jun-10 Aug Feb Jun-11 Fish feed Jun-10 Aug Feb Jun-11 Fish feed

Fig. 8. A) Fatty acid content (mg g− 1 dry weight tissue) and contribution of selected fatty acids (% of total FA) to the total fatty acid composition of mantle and digestive gland of mussels at
the west (FW) and east (FE) side of the farm, 100 m east (FE100) and at the reference station (RS) 4 km south of the farm in June 2010 and August, February and June 2011 (mean ± se,
n = 3–5). Letters and numbers denote significant differences within months. * indicates seasonal variation between months (pb 0.05).
 A. Handå et al. / Aquaculture 356–357 (2012) 328–341
suggesting that mussels can maintain their filtering activity at low phy-
toplankton concentrations in winter, thereby also maintaining bio-
remediative services on fish farm wastes.
4.2. Incorporation of fatty acids in mussel tissues
The PCA suggested a seasonal-dependent incorporation of salmon
fish feed in digestive gland and mantle tissues. This was evident from
the increased relative content of 18:1 (n-9) in August and February.
The response was significantly higher in the digestive gland tissue
of mussels at the stations located at the fish farm compared to that
at the reference station in February and June. Surprisingly, the con-
tent of 20:1 (n-9) was only higher in mussels at the fish farm than
at the reference station in June, whereas a similar contribution to
the total FA profile in mussels at the fish farm and the reference sta-
tion was found in August (also for 18:1n-9) and February. This sug-
gests that fish feed fines were filtered out and incorporated more
efficiently in August and February, when phytoplankton concentra-
tions were low, compared to after the spring bloom of phytoplankton
in June which provided mussels with their primary food source.
Phytoplankton is a natural part of seston that is selected for by
M. edulis prior to ingestion (Kiørboe and Møhlenberg, 1981), and
mussels exhibit clearance and selected incorporation among various
phytoplankton species and other organic and inorganic particles
(Bougrier et al., 1997; Defossez and Hawkins, 1997; Kiørboe et al.,
1980; Newell et al., 1989; Prins et al., 1991, 1994; Rouillon and
Navarro, 2003). The criteria for selection are not fully known, although
chemical composition, shape and size have all been suggested to play a
role (Jørgensen, 1996; Ward and Targett, 1989).
The selection of phytoplankton over other organic matter in this
study can be identified from the incorporation of certain fatty acids
that are found in high amounts in e.g. diatoms and/or dinoflagelates.
The high content of EPA and 16:1 (n-7) in digestive gland tissue and
16:0 and EPA in mantle tissue at start in June and the high content of
18:4 (n-3) in August, reflected the typical phytoplankton composition
of the spring and an autumn bloom in the Trondheimsfjord area
(Sakshaug and Myklestad, 1973). Based on the measured Chl a concen-
trations in the present study, blooms occurred in March and August,
while the spring bloom was prolonged and reached its peak values in
May in connection with the spring flood of river discharges that were
evident from the significant decrease in salinity.
The spring bloom is based on stored nutrients in deep water, as a re-
sult of vertical mixing and low nutrient consumption over the winter,
and is dominated by diatoms, while the autumn bloom is related to
freshwater discharge and vertical mixing and tends to be dominated
by dinoflagellates and other small flagellates (Sakshaug and Myklestad,
1973; Sakshaug and Olsen, 1986). EPA, 16:1 (n-7) and 16:0 are typical
fatty acids in diatoms (Kates and Volcani, 1966; Reitan et al., 1994),
whereas the contents of 18:4 (n-3), 16:0, C18:5 (n-3), EPA and DHA is
high in dinoflagellates (Harrington et al., 1970). Accordingly, the high
content of 16:1 (n-7) in digestive gland tissue, 16:0 in mantle tissue
and EPA in digestive gland and mantle tissue at the start suggested
that diatoms accounted for the larger part of the diet in spring, while
the increased content of 18:4 (n-3) in digestive gland tissue in August
suggested a shift towards a dianoflagellate-dominated diet during sum-
mer. The significantly higher content of 18:1 (n-9) in the digestive gland
tissue of mussels at the FE and of 18:2 (n-6) at the FW station compared
to the reference station in February suggested an incorporation of fish
feed in mussels at the fish farm in winter, whereas the general increase
of 18:2 (n-6) as well as 18:4 (n-3) in August could be related to mussels
feeding on flagellates, which has a high content of these FA (Hamm et al.,
2001; Reitan et al., 1994) and which has been found in high densities in
the Trondheimsfjord (Haug et al., 1973).
The high content of DHA in the digestive gland tissue of mussels at
the reference station station in February suggested that DHA did not
originate from the fish feed. The high content of 18:1 (n-9) and 20:1
337
(n-9) in August could also originate from phytoplankton and even zoo-
plankton, in which these FA can be present in high amounts (Sargent et
al., 1981 and references therein). However, although mussels have been
found to filter out various sizes of nauplii and copepodite stages of zoo-
plankton (Davenport et al., 2000; Lehane and Davenport, 2002; Lehane
and Davenport, 2004, 2006; Molloy et al., 2011), it should be questioned
and further investigated if early stages of copepods could be a tempo-
rary food source of mussels.
The results of our study were consistent with previous findings that
phytoplankton is the main component of the mussels' diet (e.g.
Fernández-Reiriz et al., 1996; Garen et al., 2004; Smaal and Stralen,
1990; Strohmeier et al., 2005, 2008; Wildish and Miyares, 1990) and
that other organic particles may also constitute an important part of
the diet, particularly when phytoplankton concentrations are low
(Arifin and Bendell-Young, 1997; Bayne et al., 1993; Grant and Bacher,
1998; Handå et al., 2011). In a low seston environment, e.g. in winter,
mussels can alternate between two different strategies to take maxi-
mum advantage of the available organic matter (Arifin and Bendell-
Young, 1997; Bayne et al., 1993). When the SPM is high, the mussels se-
lect for particles with a high organic content (e.g. phytoplankton > fish
feed > feces), resulting in an increased organic content in the consumed
feed relative to that of SPM. Inorganic particles are likely rejected
(Iglesias et al., 1996). When the particle concentration is low, however,
there is no such strong selection of food items even if the food has a poor
organic content, which leaves mussels feeding on both organic and in-
organic materials. Although feces from fish has been suggested to be
less suitable for supporting mussel growth compared to fish feed
(Handå et al., submitted for publication), mussels are likely to have a
low selection coefficient in winter, leaving both fish feed and feces to
be filtered out with a high efficiency.
4.3. Growth in length and soft tissue
The maximum growth in length was found when the water temper-
ature peaked in August–September and was accompanied by strong
vertical mixing and a corresponding autumn bloom of phytoplankton,
after which the growth decreased in autumn and remained low in
winter. A mean peak in average length growth of 120–125 μm day− 1
at the reference station in June–July and at the reference station and
the stations at the west side of the farm (FE and FE100) in August–
September is considered high, while the average growth rates in spring
(25 μm day− 1) and summer (79 μm day − 1) were comparable to the
previously reported growth rate for farmed mussels of a similar length
(~38–65 μm day− 1) during this period of the year in the landlocked
Koet Bay, located close to the study area (Handå et al., 2011).
The growth in length was strongly correlated to temperature and
weakly to SPM over the entire year, whereas a significant correlation
was found to the feed use at the fish farm in the autumn–winter period
(October–February), hence supporting the results from the PCA of the
fatty acid composition showing that fish feed contributed most to the
mussels' diet during autumn and winter, when phytoplankton concen-
trations were low, in agreement with Troell and Norberg (1998).
The growth in length was significantly higher for mussels growing
on the west side (FW) of the farm in spring compared to the other
stations close to the farm (FE and FE100) and at the reference station,
while mussels at the reference station grew faster than mussels at the
fish farm during the summer. A comparison of growth in length over
the entire year revealed that mussels at the FE station exhibited equal
growth rates compared to the mussels at the reference station, while
mussels at the reference station grew faster than the mussels at the
FW and the FE100 stations, which was mainly due to the significantly
faster growth at the reference station in June–July.
Mussels at the reference station grew significantly faster than the
mussels 100 m away from the salmon farm (FE100), though not signif-
icantly faster than the mussels at the east side of the farm (FE) over the
year. Moreover, mussels at the west side (FW) grew faster than mussels
338 A. Handå et al. / Aquaculture 356–357 (2012) 328–341
at the FE100 station in autumn, winter and spring. The results suggests
that the placement of mussels should be firmly located in IMTA systems
and that the distance between the fish and mussels should probably be
less than the 120 m, as was the distance to the FE100 station, to enable
mussels to perform bioremediative services on salmon farm wastes
under environmental conditions such as the ones studied.
In agreement with the growth in length, the specific growth rate of
DW′ peaked in August–September followed by a period with decreas-
ing DW′ in autumn and winter, although with quite a bit of variation.
The DW′ was significantly correlated to feed use at the fish farm and
the general pattern of variation found showed a higher DW′ for mussels
at the fish farm in autumn and winter, while the DW′ of mussels at the
fish farm and the reference station was more equal in spring and
highest at the reference station in June, most likely because of a more
distinct spawning in mussels at the fish farm and thus a more negative
SGRDW′ compared to mussels at the reference station in spring. Further-
more, the significantly higher DW′ at the FE at the beginning of the win-
ter period resulted in a negative SGRDW′ for mussels at this station in
winter, although the DW′ of mussels at the FE station was significantly
higher than that of the mussels at the reference station both in Decem-
ber and February. This suggested that the monthly measured DW′ was
more representative for growth in weight than the average of the four
seasons (SGRDW′) due to large fluctuations within each period, while
the four seasons represented the growth in length in a good way. The
DW′ of mussels at the fish farm was particularly higher compared to
that of mussels at the reference station at the FW station in August,
the FW, FE and FE100 stations in September and December and at the
FE station in October and February, thereby suggesting that the mussels
at these stations at the fish farm used less of their energy storage in the
autumn and winter months compared to mussels at the reference
station.
4.4. Implications for integrated multi-trophic aquaculture in Norwegian
coastal waters
The results of our study suggested a higher soft tissue content of
mussels cultivated in integration with salmon farming than in monocul-
tures during autumn and winter when ambient food availability in
terms of Chl a are low. This is in agreement with Stirling and Okumus
(1995) who examined blue mussels in two lochs in western Scotland
and found that growth in both soft tissue and shell length of mussels
kept in close proximity to salmon farms were slightly, but significantly
higher compared to control mussels located further away from the
farms, and that the mussels at the farms used less of their energy stor-
ages during winter. A faster growth in length of mussels in close prox-
imity to fish farming has also been reported by Wallace (1980),
Peharda et al. (2007), Lander et al. (2004) and Sara et al. (2009).
Wallace found that mussels at a salmon farm in northern Norway
grew faster and did not show marked growth-stoppage rings during
winter compared to mussels cultivated without any influence from
salmon farming, while Sarà et al. examined Mytilus galloprovincialis
grown up- and downstream a sea bass (Dicentrarchus labrax) and sea
bream (Sparus aurata) farm in the Mediterranean and found a faster
growth in shell length and an increase in total biomass of the mussels
situated downstream of the farm compared to mussels at upstream lo-
cations associated with significantly higher organic matter and Chl a
concentrations downstream the farm. In contrast, Taylor et al. (1992)
studied the influence of salmon farms on growth of M. edulis in British
Columbia and found that the distance from the salmon farm did not
have any significant influence on the mussel's food availability. Except
for that the incorporation of 18:1 (n-9), which was found in high
amounts in fish feed, suggested that salmon fish feed constituted a larg-
er part of the mussel's diet in winter than during spring and summer, no
increased concentrations of suspended particulate matter or Chl a at the
fish farm compared to the reference station was neither found in our
study. In another study of co-cultivation of salmon and mussels (M.
edulis) in Australia, Cheshuk et al. (2003) found only some minor and
not significant differences in growth of mussels situated in 70 and
100 m distance from salmon cages compared to mussels cultivated 500
and 1200 m away. Navarrete-Mier et al. (2010) studied co-cultivation
of oyster (Ostrea edulis) and mussels (M. galloprovincialis) cultivated in
close proximity to a sea bass (D. labrax) and sea bream (S. aurata) farm
in the Mediterranean and found no differences in growth in length or
soft tissue of mussels cultivated at a distance of 0 to 1800 m away from
the farm. They did neither find any increase in food availability nor incor-
poration of components of fish feed in mussel tissue when using stable
isotope ratios as tracers. Some possible explanations for this lack of
measureable interactions of the co-cultivation have been addressed by
Troell et al. (2011). Notwithstanding, despite the many case studies of
the combined cultivation of fish and bivalves, there seem to be more dif-
ferences than generalities making up the state of the art for using bi-
valves in open ocean IMTA.
Varying results and the lacking quantification of the assimilative
capacities of farm-derived wastes by filter feeders under ambient culti-
vation conditions may explain why, although IMTA has been practiced
for centuries in Asian countries to increase the carrying capacity of in-
tensively cultured sea areas, there is still a wait-and-see attitude to
this concept of ecological engineering for the purpose of reducing the
environmental impact of intensive fish farming in open water in the
western world (Chopin et al., 2008). The reluctance is reflected by the
absence of continuous research and technological development aiming
at designing sophisticated systems for integration of species at lower
trophic levels with today's intensively fed monocultures of fish. Based
on the existing literature it seems that up-scaling of pilot experiments
is a prerequisite for the quantification of the potential for bioremediative
services of co-cultivation under various environmental conditions. Blue
mussels have been shown to filter small particles of salmon fish feed
(MacDonald et al., 2011; Reid et al., 2010) and feces (Reid et al., 2010),
while changes in fatty acid composition have been used to demonstrate
an incorporation of fish feed components in bivalves (Gao et al., 2006;
Redmond et al., 2010). Redmond et al. (2010) showed, by using stable
isotopes and fatty acids as tracers, that blue mussels can incorporate
components of salmon fish feed, and several studies have identified
the incorporation of fish farm-derived waste products in bivalves, there-
by suggesting that bivalves can perform bioremediating services when
integrated with fish farming (e.g. Gao et al., 2006; Mazzola and Sara,
2001; Peharda et al., 2007; Soto and Mena, 1999). Accordingly, the capa-
bility of bivalves to incorporate components of fish feed has been well
documented, while, on the other hand, little is known about the incor-
poration of components of fish feces. The waste particulate food source
for mussels to feed on in IMTA with salmon has been seen as the partic-
ulate part of both feed and feces. In this study we only focused on the in-
corporation of components of the fish feed and not of feces. Considering
that feed wastes probably account for less than 5% of the feed use in
modern cage aquaculture of salmon (Mente et al., 2006), and that
most of the particles probably sinks rapidly to the seafloor, the possibil-
ity of growing mussels on this part of the wastes seems challenging.
However, the results from the present work indicated a seasonal incor-
poration of particulate wastes of salmon fish feed in M. edulis kept in
close proximity to the fish suggesting that a part of the feed waste is
available for mussels to feed on. The largest salmon farms are currently
producing 12,000 t of fish per year, with a corresponding feed use of
13,800 t (feed conversion ratio = 1.15). Given a theoretical 5% feed loss
constitutes 690 t of particles or 345 t particulate organic carbon from a
single farm from which a part can be utilized by mussels. Moreover, a
5% feed loss from the Norwegian salmon production of 0.84 million tons
in 2009 (FAO, 2011) comprises 49,500 t of particles, which have the
possibility to be utilized by filter- and deposit feeders in IMTA. Further-
more, on a single-farm scale, the bioremediative capacities of mussels
must be considered according to their capability of filtering out fish
feed and feces. On a regional scale, mussels can still contribute to bal-
ancing the nutrient concentrations in, e.g. a fjord system, by filtering
 A. Handå et al. / Aquaculture 356–357 (2012) 328–341
out phytoplankton that has accumulated anthropogenic N from fish
farming. Sheltered sites, e.g. fjords with a low current velocity, uniform
currents and a long water retention time, have the potential for increased
phytoplankton growth within the IMTA system. However, a low current
speed is a disadvantage regarding feed wastes in that it will sink rapidly
below the fish cages, thus constituting a negligible contribution to mussel
growth at such sites. On the other hand, the feed particles at exposed
sites will form a larger part of the food availability for mussels, whereas
the currents will dilute and transport waste nutrients away so quickly
that phytoplankton growth will take place outside the IMTA system. In
any case one has to also take the seasonality of the mussels nutrient re-
moval and biodeposit rates into account (see Newell, 2004 and refer-
ences therein). Deposit rates of e.g. nitrogen have been estimated at
equal amounts to that of the harvested biomass from mussel farms
(Lindahl et al., 2005). The careful monitoring of Chl a levels, in combina-
tion with modeling of the local current conditions and the corresponding
nutrient dispersal patterns downstream from salmon farms, can be a
useful tool to localize possibly high productive areas with increased phy-
toplankton growth at a distance from the fish farm. Mussel production in
such areas has the potential to contribute in equal terms to traditional
IMTA in terms of ecosystem services, taking into consideration the indi-
rect removal of anthropogenic nutrients from fish farming.
5. Conclusions
The incorporation of 18:1 (n-9), which was found in high amounts
in fish feed, suggested that salmon fish feed constituted a larger part
of the mussel's diet in winter than during spring and summer. The
growth in length and soft tissue matter of the mussels was closely relat-
ed to season while the localization of mussels at the fish farm versus at
the reference station was of minor importance to the result. Meanwhile,
five months during autumn and winter with a higher soft tissue weight
for mussels at the fish farm supported a seasonally-dependent utiliza-
tion of salmon farm wastes for maintenance and growth of soft tissue
matter. The incorporation of components of salmon fish feed and
feces and the growth of mussels under different environmental condi-
tions should be further assessed to elaborate the possibility for integrat-
ed salmon-mussel production along the Norwegian coast.
6. Concluding remarks
The results from the present study are based on an experimental
design involving only a limited amount of mussels not allowing for a
general consideration of the potential contribution of a combined pro-
duction of mussels and salmon to mitigate a potential environmental ef-
fect of particulate nutrient wastes from salmon farming. Accordingly,
the upscaling of cultures at lower trophic levels in IMTA with salmon
is essential to further assess the potential for mitigating the environ-
mental effects of farm-derived nutrient wastes, in addition to obtaining
increased growth of species at lower trophic levels in IMTA in e.g. cool
temperate North Atlantic waters. For example, the upscaling can take
place at existing salmon farms: anchoring frames for fish cages are typ-
ically 100 × 100 m, and provide a 1 ha submerged frame that can easily
be modified to provide anchoring at desired depths from which a float-
ing structure, e.g. a collar for fish nets, can be used to produce mussels or
seaweed in IMTA with salmon.
Acknowledgments
The work was a part of the Research Council of Norway project no.
173527 (INTEGRATE). We are grateful to Tom Ek and Guttorm Lange
at AquaCulture Engineering (ACE) for kindly providing research facil-
ities and data on monthly fish biomass and feed usage, and to Kjersti
Rennan at the Norwegian University of Science and Technology
(NTNU) for her fatty acid analysis. The hydrodynamic model for the
339
Tristein area was set up in the Research Council of Norway project no.
199391/I10 (MACROBIOMASS).
References
Amberg, S.M., Hall, T.E., 2008. Communicating risks and benefits of aquaculture: a con-
tent analysis of US newsprint representations of farmed salmon. Journal of the
World Aquaculture Society 39, 143–157.
Arifin, Z., Bendell-Young, L.I., 1997. Feeding response and carbon assimilation by the
blue mussel Mytilus trossulus exposed to environmentally relevant seston matrices.
Marine Ecology Progress Series 160, 241–253.
Bayne, B.L., Worrall, C.M., 1980. Growth and production of mussels Mytilus edulis from
two populations. Marine Ecology Progress Series 3, 317–328.
Bayne, B.L., Hawkins, A.J., Navarro, E., 1987. Feeding and digestion by the mussel
Mytilus edulis L. (Bivalvia: Mollusca) in mixtures of silt and algal cells at low con-
centrations. Journal of Experimental Marine Biology and Ecology 111, 1–22.
Bayne, B.L., Iglesias, J.I.P., Hawkins, A.J.S., Navarro, E., Heral, M., Deslouspaoli, J.M., 1993.
Feeding-behavior of the mussel, Mytilus edulis — responses to variations in quanti-
ty and organic content of the seston. Journal of the Marine Biological Association of
the United Kingdom 73, 813–829.
Bligh, E.G., Dyer, W.J., 1959. A rapid method of total lipid extraction and purification.
Canadian Journal of Biochemistry and Physiology 37, 911–917.
Bonardelli, J.C., Himmelman, J.H., 1995. Examination of assumptions critical to body com-
ponent indices: application to the giant scallop Placopecten magellanicus. Canadian
Journal of Fisheries and Aquatic Sciences 52, 2457–2469.
Bougrier, S., Hawkins, A.J.S., Heral, M., 1997. Preingestive selection of different micro-
algal mixtures in Crassostrea gigas and Mytilus edulis, analysed by flow cytometry.
Aquaculture 150, 123–134.
Braaten, B.R., 2007. Cage aquaculture and environmental impacts. In: Bergheim, A. (Ed.),
Aquacultural Engineering and Environment: Research Signpost, pp. 49–91.
Buschmann, A.H., Correa, J.A., Westermeier, R., Hernandez-Gonzalez, M.D.C., Norambuena,
R., 2001. Red algal farming in Chile: a review. Aquaculture 194, 203–220.
Carroll, M.L., Cochrane, S., Fieler, R., Velvin, R., White, P., 2003. Organic enrichment of
sediments from salmon farming in Norway: environmental factors, management
practices, and monitoring techniques. Aquaculture 226, 165–180.
Cheshuk, B.W., Purser, G.J., Quintana, R., 2003. Integrated open-water mussel (Mytilus
planulatus) and Atlantic salmon (Salmo salar) culture in Tasmania, Australia. Aquaculture
218, 357–378.
Chopin, T., Buschmann, A.H., Halling, C., Troell, M., Kautsky, N., Neori, A., Kraemer, G.P.,
Zertuche-Gonzalez, J.A., Yarish, C., Neefus, C., 2001. Integrating seaweeds into ma-
rine aquaculture systems: a key toward sustainability. Journal of Phycology 37,
975–986.
Chopin, T., Robinson, S., Sawhney, M., Bastarache, S., Belyea, E., Shea, R., Armstrong, W.,
Stewart, I., Fitzgerald, P., 2004. The AquaNet integrated multi-trophic aquaculture pro-
ject: rationale of the project and development as kelp cultivation as the inorganic ex-
tractive component of the system. Bulletin of the Aquaculture Association of Canada
104, 11–18.
Chopin, T., Robinson, S.M.C., Troell, M., Neori, A., Bushmann, A.H., Fang, J., 2008. Multitrophic
integration for sustainable marine aquaculture. In: Jørgensen, S.E., Fath, B.D. (Eds.), The
Encyclopedia of Ecology, Ecological Engineering. Elsevier, Oxford, pp. 2463–2475.
Cloern, J.E., 2001. Our evolving conceptual model of the coastal eutrophication problem.
Marine Ecology Progress Series 210, 223–253.
Dalsgaard, J., St John, M., Kattner, G., Muller-Navarra, D., Hagen, W., 2003. Fatty acid
trophic markers in the pelagic marine environment. Advances in Marine Biology,
vol. 46. Academic Press Ltd, London, pp. 225–340.
Davenport, J., Smith, R., Packer, M., 2000. Mussels Mytilus edulis: significant consumers
and destroyers of mesozooplankton. Marine Ecology Progress Series 198, 131–137.
Defossez, J.M., Hawkins, A.J.S., 1997. Selective feeding in shellfish: size-dependent rejection
of large particles within pseudofaeces from Mytilus edulis, Ruditapes philippinarum and
Tapes decussatus. Marine Biology 129, 139–147.
Dolmer, P., 2000. Feeding activity of mussels Mytilus edulis related to near-bed currents
and phytoplankton biomass. Journal of Sea Research 44, 221–231.
FAO, 2009. Fisheries and Aquaculture Department. The State of the World Fisheries and
Aquaculture 2008.
FAO, 2011. Fisheries and Aquaculture Department. FishStatJ, version 1.0.1.
Fernández-Reiriz, M.J., Labarta, U., Babarro, J.M.F., 1996. Comparative allometries in
growth and chemical composition of mussel (Mytilus galloprovincialis Lmk) cultured
in two zones in the ria Sada ( Galicia, NW Spain). Journal of Shellfish Research 15,
349–354.
Folke, C., Kautsky, N., 1989. The role of ecosystems for a sustainable development of
aquaculture. Ambio 18, 234–243.
Folke, C., Kautsky, N., Troell, M., 1994. The costs of eutrophication from salmon farming
— implications for policy. Journal of Environmental Management 40, 173–182.
Fukumori, K., Oi, M., Doi, H., Takahashi, D., Okuda, N., Miller, T.W., Kuwae, M., Miyasaka,
H., Genkai-Kato, M., Koizumi, Y., Omori, K., Takeoka, H., 2008. Bivalve tissue as a
carbon and nitrogen isotope baseline indicator in coastal ecosystems. Estuarine,
Coastal and Shelf Science 79, 45–50.
Gao, Q.F., Shin, P.K.S., Lin, G.H., Chen, S.P., Cheung, S.G., 2006. Stable isotope and fatty
acid evidence for uptake of organic waste by green-lipped mussels Perna viridis
in a polyculture fish farm system. Marine Ecology Progress Series 317, 273–283.
Gao, Q.F., Xu, W.Z., Liu, X.S., Cheung, S.G., Shin, P.K.S., 2008. Seasonal changes in C, N
and P budigestive glandets of green-lipped mussels Perna viridis and removal of
nutrients from fish farming in Hong Kong. Marine Ecology Progress Series 353,
137–146.
340 A. Handå et al. / Aquaculture 356–357 (2012) 328–341
Garen, P., Robert, S., Bougrier, S., 2004. Comparison of growth of mussel, Mytilus edulis,
on longline, pole and bottom culture sites in the Pertuis Breton, France. Aquacul-
ture 232, 511–524.
Grant, J., Bacher, C., 1998. Comparative models of mussel bioenergetics and their vali-
dation at field culture sites. Journal of Experimental Marine Biology and Ecology
219, 21–44.
Hamm, C., Reigstad, M., Riser, C.W., Muhlebach, A., Wassmann, P., 2001. On the trophic
fate of Phaeocystis pouchetii. VII. Sterols and fatty acids reveal sedimentation of P-
pouchetii-derived organic matter via krill fecal strings. Marine Ecology Progress
Series 209, 55–69.
Handå, A., Nordtug, T., Olsen, A.J., Halstensen, S., Reitan, K.I., Olsen, Y., Reinertsen, H. in press.
Temperature-dependent feed requirements in farmed blue mussel (Mytilus edulis L.)
estimated from soft tissue growth and oxygen consumption and ammonia-N excretion.
Aquaculture Research, http://dx.doi.org/10.1111/j.1365-2109.2011.03069.x.
Handå, A., Alver, M., Edvardsen, C.V., Halstensen, S., Olsen, A.J., Øie, G., Reitan, K.I.,
Olsen, Y., Reinertsen, H., 2011. Growth of farmed blue mussels (Mytilus edulis L.)
in a Norwegian coastal area; comparison of food proxies by DEB modeling. Journal
of Sea Research 66, 297–307.
Handå, A., Ranheim, A., Altin, D., Olsen, A.J., Reitan, K.I., Olsen, Y., Reinertsen, H., sub-
mitted for publication. Incorporation of food components in tissues of mussels
(Mytilus edulis) fed salmon fish feed and faeces: implications for integrated
multi-trophic aquaculture in cool-temperate North Atlantic waters.
Harrington, G.W., Beach, D.H., Dunham, J.E., Holz, G.G., 1970. Polyunsaturated fatty
acids of marine dinoflagellates. The Journal of Protozoology 17, 213–219.
Haug, A., Myklestad, S., Sakshaug, E., 1973. Studies on the phytoplankton ecology of the
Trondheimsfjord. I. The chemical composition of phytoplankton populations. Journal
of Experimental Marine Biology and Ecology 11, 15–26.
Hawkins, A.J., Smith, R.F.M., Bougrier, S., Bayne, B.L., Héral, M., 1997. Manipulation of
dietary conditions for maximal growth in mussels, Mytilus edulis, from the
Marennes-Oléron Bay, France. Aquatic Living Resources 10, 13–22.
Hawkins, A.J.S., James, M.R., Hickman, R.W., Hatton, S., Weatherhead, M., 1999. Modelling
of suspension-feeding and growth in the green-lipped mussel Perna canaliculus
exposed to natural and experimental variations of seston availability in the
Marlborough Sounds, New Zealand. Marine Ecology Progress Series 191, 217–232.
Holmer, M., Wildfish, D., Hargrave, B., 2005. Organic enrichment from marine finfish
Aquaculture and effects on sediment biogeochemical processes. Environmental Ef-
fects of Marine Finfish Aquaculture 5, 181–206.
Iglesias, J.I.P., Urrutia, M.B., Navarro, E., Alvarez-Jorna, P., Larretxea, X., Bougrier, S., Heral,
M., 1996. Variability of feeding processes in the cockle Cerastoderma edule (L.) in re-
sponse to changes in seston concentration and composition. Journal of Experimental
Marine Biology and Ecology 197, 121–143.
Jørgensen, C.B., 1996. Bivalve filter feeding revisited. Marine Ecology Progress Series
142, 287–302.
Jusup, M., Gecek, S., Legovic, T., 2007. Impact of aquacultures on the marine ecosystem:
modelling benthic carbon loading over variable depth. Ecological Modelling 200,
459–466.
Kalantzi, I., Karakassis, I., 2006. Benthic impacts of fish farming: meta-analysis of com-
munity and geochemical data. Marine Pollution Bulletin 52, 484–493.
Kates, M., Volcani, B.E., 1966. Lipid components of diatoms. Biochimica et Biophysica
Acta 116, 264–278.
Kiørboe, T., Møhlenberg, F., 1981. Particle selection in suspension-feeding bivalves. Ma-
rine Ecology Progress Series 5, 291–296.
Kiørboe, T., Møhlenberg, F., Nøhr, O., 1980. Feeding, particle selection and carbon ab-
sorption in Mytilus edulis in different mixtures of algae and resuspended bottom
material. Ophelia 19, 193–205.
Kutti, T., Ervik, A., Hansen, P.K., 2007. Effects of organic effluents from a salmon farm on a
fjord system. I. Vertical export and dispersal processes. Aquaculture 262, 367–381.
Lander, T., Barrington, K., Robinson, S., MacDonald, B., Martin, J., 2004. Dynamics of the
blue mussel as an extractive organism in an integrated multi-trophic aquaculture
system. Bulletin of the Aquaculture Association of Canada 104, 19–28.
Lehane, C., Davenport, J., 2002. Ingestion of mesozooplankton by three species of bi-
valve; Mytilus edulis, Cerastoderma edule and Aequipecten opercularis. Journal of
the Marine Biological Association of the United Kingdom 82, 615–619.
Lehane, C., Davenport, J., 2004. Ingestion of bivalve larvae by Mytilus edulis: experimen-
tal and field demonstrations of larviphagy in farmed blue mussels. Marine Biology
145, 101–107.
Lehane, C., Davenport, J., 2006. A 15-month study of zooplankton ingestion by farmed
mussels (Mytilus edulis) in Bantry Bay, Southwest Ireland. Estuarine, Coastal and
Shelf Science 67, 645–652.
Lindahl, O., Hart, R., Hernroth, B., Kollberg, S., Loo, L.O., Olrog, L., Rehnstam-Holm, A.S.,
Svensson, J., Svensson, S., Syversen, U., 2005. Improving marine water quality by
mussel farming: a profitable solution for Swedish society. Ambio 34, 131–138.
MacDonald, B.A., Robinson, S.M.C., Barrington, K.A., 2011. Feeding activity of mussels
(Mytilus edulis) held in the field at an integrated multi-trophic aquaculture
(IMTA) site (Salmo salar) and exposed to fish food in the laboratory. Aquaculture
314, 244–251.
Mazzola, A., Sara, G., 2001. The effect of fish farming organic waste on food availability
for bivalve molluscs (Gaeta Gulf, Central Tyrrhenian, MED): stable carbon isotopic
analysis. Aquaculture 192, 361–379.
Mente, E., Pierce, G.J., Santos, M.B., Neofitou, C., 2006. Effect of feed and feeding in the
culture of salmonids on the marine aquatic environment: a synthesis for European
aquaculture. Aquaculture International 14, 499–522.
Metcalfe, L.D., Schmitz, A.A., Pelka, J.R., 1966. Rapid preparation of fatty acid esters from
lipids for gas chromatographic analysis. Analytical Chemistry 38, 514–515.
Molloy, S.D., Pietrak, M.R., Bouchard, D.A., Bricknell, I., 2011. Ingestion of Lepeophtheirus
salmonis by the blue mussel Mytilus edulis. Aquaculture 311, 61–64.
Narváez, M., Freites, L., Guevara, M., Mendoza, J., Guderley, H., Lodeiros, C.J., Salazar, G.,
2008. Food availability and reproduction affects lipid and fatty acid composition of
the brown mussel, Perna perna, raised in suspension culture. Comparative Bio-
chemistry and Physiology. Part B, Biochemistry & Molecular Biology 149, 293–302.
Navarrete-Mier, F., Sanz-Lázaro, C., Marín, A., 2010. Does bivalve mollusc polyculture
reduce marine fin fish farming environmental impact? Aquaculture 306, 101–107.
Navarro, J.M., Labarta, U., Fernandez-Reiriz, M.J., Velasco, A., 2003. Feeding behavior
and differential absorption of biochemical components by the infaunal bivalve
Mulinia edulis and the epibenthic Mytilus chilensis in response to changes in food
regimes. Journal of Experimental Marine Biology and Ecology 287, 13–35.
Neori, A., 2008. Essential role of seaweed cultivation in integrated multi-trophic aqua-
culture farms for global expansion of mariculture: an analysis. Journal of Applied
Phycology 20, 567–570.
Neori, A., Chopin, T., Troell, M., Buschmann, A.H., Kraemer, G.P., Halling, C., Shpigel, M.,
Yarish, C., 2004. Integrated aquaculture: rationale, evolution and state of the art em-
phasizing seaweed biofiltration in modern mariculture. Aquaculture 231, 361–391.
Newell, R.I.E., 2004. Ecosystem influences of natural and cultivated populations of
suspension-feeding bivalve molluscs: a review. Journal of Shellfish Research 23, 51–61.
Newell, C.R., Shumway, S.E., Cucci, T., Selvin, R., 1989. The effects of natural seston par-
ticle size and type on feeding rates, feeding selectivity and food resource availabil-
ity for the mussel Mytilus edulis Linnaeus, 1758 at bottom culture sites in Maine.
Journal of Shellfish Research 8, 187–196.
Nixon, S.W., 1995. Coastal marine eutrophication—a definition, social causes, and fu-
ture concerns. Ophelia 41, 199–219.
Norén, F., Haamer, J., Lindahl, O., 1999. Changes in the plankton community passing a
Mytilus edulis mussel bed. Marine Ecology Progress Series 191, 187–194.
Norwegian Meteorological Institute, http://www.eklima.no.
Olsen, L.M., Holmer, M., Olsen, Y., 2008. Perspectives of nutrient emission from fish aqua-
culture in coastal waters: literature review with evaluated state of knowledigestive
glande. The Fishery and Aquaculture Industry Research Fund (FHF). Final report. 87 pp.
Peharda, M., Zupan, I., Bavcevic, L., Frankic, A., Klanjscek, T., 2007. Growth and condition
index of mussel Mytilus galloprovincialis in experimental integrated aquaculture.
Aquaculture Research 38, 1714–1720.
Post, D.M., 2002. Using stable isotopes to estimate trophic position: models, methods,
and assumptions. Ecology 83, 703–718.
Prins, T.C., Smaal, A.C., Pouwer, A.J., 1991. Selective ingestion of phytoplankton by the
bivalves Mytilus edulis L. and Cerastoderma edule L. Hydrobiological Bulletin 25,
93–100.
Prins, T.C., Dankers, N., Smaal, A.C., 1994. Seasonal variation in the filtration rates of a
semi-natural mussel bed in relation to seston composition 1. Journal of Experimental
Marine Biology and Ecology 176, 69–86.
Redmond, K.J., Magnesen, T., Hansen, P.K., Strand, O., Meier, S., 2010. Stable isotopes
and fatty acids as tracers of the assimilation of salmon fish feed in blue mussels
(Mytilus edulis). Aquaculture 298, 202–210.
Reid, G.K., Liutkus, M., Bennett, A., Robinson, S.M.C., MacDonald, B., Page, F., 2010. Absorp-
tion efficiency of blue mussels (Mytilus edulis and M. trossulus) feeding on Atlantic
salmon (Salmo salar) feed and fecal particulates: implications for integrated multi-
trophic aquaculture. Aquaculture 299, 165–169.
Reitan, K.I., Rainuzzo, J.R., Olsen, Y., 1994. Effect of nutrient limitation on fatty-acid and
lipid-content of marine microalgae. Journal of Phycology 30, 972–979.
Riisgård, H.U., Larsen, P.S., 2001. Minireview: ciliary filter feeding and bio-fluid mechanics —
present understanding and unsolved problems. Limnology and Oceanography 46,
882–891.
Rouillon, G., Navarro, E., 2003. Differential utilization of species of phytoplankton by
the mussel Mytilus edulis. Acta Oecologica 24, S299–S305.
Sakshaug, E., Myklestad, S., 1973. Studies on the phytoplankton ecology of the
Trondheimsfjord. III. Dynamics of Phytolplankton blooms in relation to environ-
mental factors, bioassay experiments and parameters for the physiological state
of populations. Journal of Experimental Marine Biology and Ecology 11, 157–188.
Sakshaug, E., Olsen, Y., 1986. Nutrient status of phytoplankton blooms in Norwegian
waters and algal strategies for nutrient competition. Canadian Journal of Fisheries
and Aquatic Sciences 43, 389–396.
Sara, G., Zenone, A., Tomasello, A., 2009. Growth of Mytilus galloprovincialis (mollusca,
bivalvia) close to fish farms: a case of integrated multi-trophic aquaculture within
the Tyrrhenian Sea. Hydrobiologia 636, 129–136.
Sargent, J.R., Gatten, R.R., Henderson, R.J., 1981. Marine wax esters. Pure and Applied
Chemistry 53, 867–871.
Skog, T.E., Hylland, K., Torstensen, B.E., Berntssen, M.H.G., 2003. Salmon farming affects
the fatty acid composition and taste of wild saithe Pollachius virens L. Aquaculture
Research 34, 999–1007.
Skogen, M.D., Eknes, M., Asplin, L.C., Sandvik, A.D., 2009. Modelling the environmental
effects of fish farming in a Norwegian fjord. Aquaculture 298, 70–75.
Slagstad, D., McClimans, T.A., 2005. Modeling the ecosystem dynamics of the Barents
sea including the marginal ice zone: I. Physical and chemical oceanography. Journal
of Marine Systems 58, 1–18.
Smaal, A.C., Stralen, M.R., 1990. Average annual growth and condition of mussels as a
function of food source. Hydrobiologia V195, 179–188.
Soto, D., Mena, G., 1999. Filter feeding by the freshwater mussel, Diplodon chilensis, as a
biocontrol of salmon farming eutrophication. Aquaculture 171, 65–81.
Stigebrandt, A., Aure, J., Ervik, A., Hansen, P.K., 2004. Regulating the local environmental
impact of intensive marine fish farming. III. A model for estimation of the holding ca-
pacity in the Modelling–Ongrowing fish farm–Monitoring system. Aquaculture 234,
239–261.
Stirling, H.P., Okumus, B., 1995. Growth and production of mussels (Mytilus edulis L.)
suspended at salmon cages and shellfish farms in two Scottish sea lochs. Aquaculture
134, 193–210.
 A. Handå et al. / Aquaculture 356–357 (2012) 328–341
Støle-Hansen, K., Slagstad, D., 1991. Simulations of currents, ice melting and vertical
mixing in the Barents Sea using a 3D baroclinic model. Polar Research 10, 33–44.
Strickland, J.H.D., Parsons, T.R., 1968. A Practical Handbook of Seawater Analysis. Bulletin,
167. Fisheries Research Board of Canada, Ottawa. 293 pp.
Strohmeier, T., Aure, J., Duinker, A., Castberg, T., Svardal, A., Strand, Ø., 2005. Flow re-
duction, seston depletion, meat content and distribution of diarrhetic shellfish
toxins in a long-line blue mussel (Mytilus edulis) farm. Journal of Shellfish Research
24, 15–23.
Strohmeier, T., Duinker, A., Strand, Ø., Aure, J., 2008. Temporal and spatial variation in food
availability and meat ratio in a longline mussel farm (Mytilus edulis). Aquaculture 276,
83–90.
Strohmeier, T., Strand, Ø., Cranford, P., 2009. Clearance rates of the great scallop (Pecten
maximus) and blue mussel (Mytilus edulis) at low natural seston concentrations.
Marine Biology 156, 1781–1795.
Taylor, B.E., Jamieson, G., Carefoot, T.H., 1992. Mussel culture in British-columbia — the
influence of salmon farms on growth of Mytilus edulis. Aquaculture 108, 51–66.
Tett, P., 2008. Fish Farm Wastes in the Ecosystem. Springer, pp. 1–46.
Troell, M., Norberg, J., 1998. Modelling output and retention of suspended solids in an
integrated salmon–mussel culture. Ecological Modelling 110, 65–77.
Troell, M., Halling, C., Neori, A., Chopin, T., Buschmann, A.H., Kautsky, N., Yarish, C.,
2003. Integrated mariculture: asking the right questions. Aquaculture 226, 69–90.
341
Troell, M., Joyce, A., Chopin, T., Neori, A., Buschmann, A.H., Fang, J.G., 2009. Ecological
engineering in aquaculture — potential for integrated multi-trophic aquaculture
(IMTA) in marine offshore systems. Aquaculture 297, 1–9.
Troell, M., Chopin, T., Reid, G., Robinson, S., Sará, G., 2011. Letter to the Editor. Aquaculture
313, 171–172.
Wallace, J.C., 1980. Growth rates of different populations of the edible mussel, Mytilus
edulis, in north Norway. Aquaculture 19, 303–311.
Ward, J.E., Targett, N.M., 1989. Influence of marine microalgal metabolites on the feed-
ing behavior of the blue mussel Mytilus edulis. Marine Biology 101, 313–321.
Whitmarsh, D.J., Cook, E.J., Black, K.D., 2006. Searching for sustainability in aquaculture: an
investigation into the economic prospects for an integrated salmon-mussel production
system. Marine Policy 30, 293–298.
Widdows, J., Fieth, P., Worrall, C.M., 1979. Relationships between seston, available food
and feeding activity in the common mussel Mytilus edulis. Marine Biology 50,
195–207.
Wildish, D.J., Miyares, M.P., 1990. Filtration rate of blue mussels as a function of flow
velocity: preliminary experiments. Journal of Experimental Marine Biology and
Ecology 142, 213–219.