Incorporation of fish feed and growth of blue mussels...

Aquaculture 356–357 (2012) 328–341

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Incorporation of fish feed and growth of blue mussels (Mytilus edulis) in closeproximity to salmon (Salmo salar) aquaculture: Implications for integratedmulti-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, Norwayb SINTEF Fisheries and Aquaculture, N-7465 Trondheim, Norway

Abbreviations: FW, Farm west (Station 1); FE, Farmeast of farm (Station 3); AGRL, Average growth rate in lerate in soft tissue dry weight.⁎ Corresponding author at: Norwegian University of Sc

Department of Biology, Centre of Fisheries and AquacuTrondheim, Norway. Tel.: +47 91577232; fax: +47 9327

E-mail address: [email protected] (A. Han

0044-8486/$ – see front matter © 2012 Elsevier B.V. Alldoi:10.1016/j.aquaculture.2012.04.048

a b s t r a c t
a r t i c l e i n f o
Article history:Received 22 November 2011Received in revised form 26 April 2012Accepted 30 April 2012Available online 11 May 2012

Keywords:Mytilus edulisSalmon fish feedFatty acidsBivalve growthIntegrated multi-trophic aquaculture

The incorporation of fish feed wastes in digestive gland and mantle tissue and average growth in length andstandardized dry weight of soft tissue matter (DW′) of blue mussels (Mytilus edulis L.) were measured for oneyear (June 2010–June 2011) at three experimental stations in close proximity to a salmon (Salmo salar) farmat Tristein (63° 52′ N, 9° 37′ E) in Central Norway, with one on the west side (FW), one on the east side (FE)and one 100 m east of the farm (FE100), in addition to one reference station 4 km south of the farm.A principal component analysis of fatty acid profiles clearly demonstrated the incorporation of fatty acids fromsalmon fish feed in digestive gland andmantle tissue, identified by an increased content of 18:1 (n-9). The incor-poration, and consequently the separation of mussels at stations close to the fish farm frommussels at the refer-ence station, was more pronounced in February compared to August, while no clear differences were found inJune.The growth in length correlated significantly to feed use at the fish farm (r=0.89) and to the concentration ofsuspended particulate matter (SPM) (r=0.53) in the autumn–winter period (Oct–Feb) (pb0.05). The musselsat the reference station showed a significantly faster growth in length compared to the mussels at all stationsat thefish farmduring the summer,whilemussels at the FWstation grew faster than themussels at the referencestation during the spring (pb0.05). The length growth was faster for mussels at the reference station than formussels at the FW and FE100 stations (pb0.05), while no significant differences were found between musselsat 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) (pb0.05), andthe DW′ of mussels at stations at the fish farm was significantly higher compared to the DW′ of mussels at thereference station infivemonths during autumn andwinter (pb0.05). The results suggest that the combined pro-duction ofmussels and salmon can be seen as a strategy tomaintain a higher soft tissue content ofmussels duringautumn andwinter. Quantification of themussel's assimilation capacities of farm-derivedwastes at realistic scaleand under different environmental conditions is needed.

© 2012 Elsevier B.V. All rights reserved.

1. Introduction

The global salmonid production increased by around 60% from 1999to 2009 (1.26 to 2.17 million tons), and further growth is expected (FAO,2011). Atlantic salmon (Salmo salar) aquaculture accounts for themajority of the salmonid production (1.44 million tons), with Norway,

east (Station 2); FE100, 100 mngth; SGRDW′, Specific growth

ience and Technology (NTNU),lture, Brattørkaia 17B, N-74910701.då).

rights reserved.

which doubled its production from 1999 to 2009 (0.43 to 0.86 mil-lion tons), being the leading producer (FAO, 2011). The mean nutrientrelease from Norwegian salmon aquaculture has been estimated at61% 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 dispersalfrom 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 inorganicN, 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 aquaculturemay cause (Amberg and Hall, 2008; Braaten, 2007; FAO, 2009; Tett,2008), and one of themajor challenges for the sustainable development

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329A. Handå et al. / Aquaculture 356–357 (2012) 328–341

of salmonid cage mariculture is to minimize discharge of wastesthat potentially can lead to degradation of the marine environment(Cheshuk et al., 2003). For example, the sedimentation of particulatematter 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 (Holmeret al., 2005; Kalantzi and Karakassis, 2006), while dissolved nutrientsmay cause eutrophication (Cloern, 2001; Folke et al., 1994; Nixon,1995; Skogen et al., 2009).

For the purpose of minimizing the potentially negative effects ofwaste discharges it has been suggested to cultivate extractive and filterfeeding species at lower trophic levels in close vicinity to thefish farms, astrategy termed IMTA, or integrated multi-trophic aquaculture. IMTA isused as ameans of obtaining increased biomass production, thus addingto the value of feed investments, and at the same time contributing to amore sustainable aquaculture production (Chopin et al., 2001; Chopin etal., 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 asmussels. Several studies have suggested that bivalve filter feederscan provide bioremediative services when co-cultivated with fishaquaculture (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 ofparticulate organic matter from marine cage aquaculture (Cheshuket al., 2003 and references therein). However, little is known abouthow particulate wastes from salmon farming may affect shellfishgrowth (MacDonald et al., 2011).

While many studies have reported a better growth for musselsgrown 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 insteadsuggest that the distance from the farms does not substantially influ-ence food availability and growth of mussels. Previous research hassuggested several possible explanations for the lack of a distinct growthresponse in mussels co-cultivated with fish cage aquaculture. The ex-planations given are that: a) the particulate wastes of the fish farmsdo not increase the seston concentrations significantly above ambientlevels, b) that the ambient seston concentrations remain consistentlyabove the pseudofeces threshold level, thereby limiting the potentialof mussels to increase their growth by feeding upon fish farm wastes(Cheshuk et al., 2003), c) that the mussels' filtering response is toslow to adapt to pulsed feeding regimes accompanied by d) non-uniform effluents from salmon farms leaving mussels to only ingestfarm 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 inways which make it difficult to obtain univocal conclusions for theIMTA 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 ishence 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 fecesquite efficiently (Handå et al., submitted for publication; MacDonaldet al., 2011; Reid et al., 2010). Additionally, changes in fatty acid compo-sition in the direction of the food source profile have demonstrated theassimilation of salmon feed and feces in bivalve tissues (Gao et al., 2006;Handå et al., submitted for publication; Redmond et al., 2010). Fishfeed has traditionally contained a high percentage of the fatty acids20:1 (n-9) and 22:1 (n-11). There has been an increasing use of

terrestrial lipid sources with high proportions of, e.g. 18:1 (n-9) and18:2 (n-6) in fish feed in recent years (Dalsgaard et al., 2003; Narváezet al., 2008; Skog et al., 2003) which can be used as tracer fatty acidsfor the incorporation of salmon feed. Significant changes in the propor-tions of these fatty acids have been found to take placewithin 28 days inthe digestive gland (Handå et al., submitted for publication; Redmondet al., 2010) and within 90 days in mantle tissue (Fukumori et al.,2008; Post, 2002) of mussels. However, little is known about theseasonal-dependent incorporation of salmon fish feed wastes and thecorresponding growth in bivalves under natural farming conditions.

The primary objectives of this study were to investigate the annualand the seasonal-dependent incorporation of fish feed waste andgrowth 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 forone year (June 2010–June 2011) at three experimental stations inclose proximity to a salmon farm at Tristein (63° 52′N, 9° 37′ E) outsidethe Trondheimsfjord, at the coast off Central Norway, with one stationon the west side (FW), one on the east side (FW), one 100 m east ofthe 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 theFE100 station. Hydrodynamic simulations were undertaken to deter-mine the best location of the sampling stations (see Section 2.7). Fattyacids were analyzed for salmon fish feed sampled from the feed bargein December 2010 and June 2011, and from mussels' digestive glandsandmantle 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),eachwith a circumference of 157 m,with 15 mdeep net pens and a vol-ume of 36.000 m3. The total salmon production was 4.705 t, and thecorresponding use of feed was 5.216 t during the sampling period(Fig. 2A). The cage on thewest side, where station FWwas located, con-tained only mussels (no fish) during the experiment. The western sideof the farmwas situated above the 50 m isobath, with the bottom slop-ing steeply down to approximately 100 m on the eastern side. Althoughthe farm was situated approximately 4 km off shore of the main land,it was sheltered from the ocean by the skerries of Tristeinen on thewestern andnorthern sides. The area surrounding the Tristeinen skerriesis dominated by marine waters (salinity b34.5‰) from the Norwegiancoastal current, with temporary outflows of fresh surface water fromthe Trondheimsfjord.

2.3. Environmental and seston variables

The temperature and salinity were measured at a depth of 2 mwitha CTD (SD 204, SAIV LTD, Norway), while integrated water samples forthe analysis of suspended particulate matter (SPM), particulate organiccarbon (POC), nitrogen (PON) and chlorophyll a (Chl a) were takenfrom 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 a200 μm net prior to a second filtration of 2 L with pre-combusted andweighed Whatman GF/C filters. The SPM was measured in parallelafter drying the filters for 48 h at 70 °C, while 1/16 of two other filterswas 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 arefrigerator for 2 h prior to measurement of in vitro fluorescence witha Turner Design Fluorometer according to Strickland and Parsons

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.

330 A. Handå et al. / Aquaculture 356–357 (2012) 328–341

(1968). POC and PONwere analyzed by a Carlo Erba analyzer, model NA1106 CHN.

2.4. Growth measurements

The shell length (L) (n=25) was measured with a digital caliperon 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

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Fig. 2. A) Fish biomass (right axis) and feed use (left axis) from June 2010 to June 2011, and B100 m east (FE100) and at the reference station (RS) 4 km south of the farm from June 201

(DW) (n=30) were represented using a condition index standardizedto a certain length L′ according to Bayne and Worrall (1980) andBonardelli and Himmelman (1995). The DW was measured with anelectronic weight (Mettler Toledo Precisa 180A) after drying the tissueat 60 °C in a Termaks heat cabinet for 48 h,whichwas then calculated asa standardized dry weight (DW′) by the following equation:

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where DW is the weight in mg, L the length in mm and b the slope ofthe log10 DW plotted as a function of log10 L. The DW′ corresponds tothe condition index, andwas scaled so it equaled the DWwhen L equalsL′. 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 ln DW′t− ln DW′0ð Þ=t ð2Þ

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� exp μð Þ−1ð Þ ð3Þ

The average rate of length increase (μm, day−1) (AGRL) was calcu-lated by the equation:

μm ¼ Lt−L0ð Þ=t ð4Þ

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 theÅfjord (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 samplesaccording to Metcalfe et al. (1966) (see Handå et al., submitted forpublication).

2.6. Data analysis

Data for the specific growth in DW′ (SGRDW′) and the average growthin length (AGRL) were tested for normality using a Kolmogorov–Smirnovtest, 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 therelative content of identified fatty acids (% of total fatty acids) of digestivegland and mantle tissue between June 2010 (Month 1), August (Month3), February (Month8) and June 2011 (Month12), in addition to betweenthe different stations on each sampling day were tested using aKolmogorov–Smirnov test. The equality of means for SGRDW′ and AGRLbetween 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-wayANOVA followed by post hoc comparisons by Tamhane's T2, not assum-ing equal variances. The significance limit was set at 0.05 and themeanswere given with the standard error. A Spearman's correlation analysiswas performed on seston data and mussel growth for the entire yearand for the five-month autumn–winter period from October toFebruary.

Statistical analyses were performed using SPSS (rel. 17.0, Chicago,SPSS Inc.), while a principal component analysis (PCA) for fatty acidcomposition was performed with an Unscrambler, version 9.8 2008(Camo Software AS). Data was analyzed without weighing, leavingthe PCA for each tissue to be dominated by the fatty acids that dom-inated the fatty acid composition. Missing measurement points inthe time plots were estimated by linear interpolation between thetwo closest measurement points.

2.7. Hydrodynamical model

The coupled 3D hydrodynamic-biological model system SINMODwas used for the hydrodynamic modeling. The hydrodynamic part of

the model is based on the primitive Navier–Stokes equations, whichare solved by a finite difference scheme. Detailed model descriptionsare given in Støle-Hansen and Slagstad (1991) and Slagstad andMcClimans (2005).

Boundary conditions are generated through a four step nesting pro-cedure using consecutively finer grids from 20,000 m to 4000 m to800 m to 160 m and finally to 32 m. Amodel of 32 m horizontal resolu-tion was set up for the area surrounding the ACE facility (Fig. 1). A totalof 21 vertical layers were used in the 32 mmodel 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. Thegreatest depth in the model domain was 279.54 m. The coarser modelsuse up to 42 vertical layers.

Atmospheric forcing data were extracted from the eKlima data-base (Norwegian Meteorological Institute). Data for the station atØrlandet (63° 42′ N, 9° 36′ E; elevation: 10 m) for 2010 and 2011were used.

3. Results

3.1. Environmental and seston variables

The water temperature ranged between 4 °C in February and13.6 °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 to21.7‰ in July, followed by a rapid increase before leveling off andremaining stable >32‰ from October over the winter (Fig. 2B).

The hydrodynamic simulations indicated that the current speed ofthe surface water at the FE100 and the reference stations generallywas between 0 and 0.2 m s−1 (in June 2010, August 2010 and February2011) (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 tothe FE100 station (Fig. 3B).

The concentration of suspended particulate matter ranged between5.2 and 11.2 mg L−1, with an average of 8.4±0.2 mg L−1 for the entireyear (Fig. 4A) and demonstrated a similar pattern of variation as the useof 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 thefish farm during the autumn–winter period (October–February)(r=0.53) (pb0.05). Coincidently, high values of SPM and Chl a duringspring (March–May) resulted in a moderate correlation with Chl a forthe entire year (r=0.34) (pb0.05).

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 correlatedto feed use at the fish farm (r=−0.36) for the entire year while, incontrast, the POC concentrations were positively correlated to feeduse during the autumn–winter period (r=0.40) (pb0.05) (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 theentire year, values b0.6 μg L−1 during the autumn–winter period(Fig. 4C), and peak values in May. The Chl a values were positivelycorrelated 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) (pb0.05). The SPM:Chl a ratio (mg/μg) ranged between 0.5 and 107, with peak valuesduring winter when the Chl a concentrations were at a minimum(Fig. 4D). The ratio was moderately correlated to feed use at the fishfarm over the year (r=0.32) (pb0.05).

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 offand remained low in winter, followed by a steady increase in the

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Fig. 4. A) Suspended particulate matter (SPM), B) particulate organic carbon (POC),C) chlorophyll a (Chl a) and D) ratios of SPM over Chl a (mg:μg) in integrated samples(0–8 m depth) at the west (FW) and east (FE) side of the farm, 100 m east (FE100) andat the reference station (RS) 4 km south of the farm from June 2010 to June 2011.

Fig. 3. A) Simulated surface water current situation at the ACE farm for February 15 to 21,2011. 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 themiddle shows the scale of a speed of 0.2 m s−1. The thick red curves indicate 50, 100and 150 m isobaths. B) Probability of simulated surface current speeds at stations FE100and RS in June 2010 (J), August 2010 (A) and February 2011 (F). The colors indicate rela-tive frequency of simulation samples with current speeds in the intervals indicated belowthe bars for the given months and locations.


spring (Fig. 5A). The average growth rate ranged between 0.1 and125 μm day−1 within single months and the growth was generallyhigh during summer (June–September) and low in autumn and win-ter (October–February) (Fig. 5A). The growth was significantly higherat the reference station compared to the stations at the fish farm inJune–July, whereas the opposite was evident in May–June when themussels at all stations at the fish farm grew faster than the musselsat the reference station (pb0.05). The mussels at the reference stationgrew faster than themussels at the FE100 station in the autumn–winterperiod and in April–May,whilemussels at the FWand FE stations insidethe farm grew faster than the mussels at the FE100 station in Novem-ber–January and April–May (pb0.05). A comparison of the differentseasons revealed that the mussels at the reference station showed afaster growth in length compared to the mussels at all stations at thefish farm during the summer, while mussels at the FW station grewfaster than the mussels at the reference station during the spring(pb0.05) (Fig. 5B). A comparison of the average growth rates for the en-tire year revealed that mussels at the reference station grew faster than

the mussels at the FW and FE100 stations, while no significant differ-ences were found betweenmussels at the reference and the FE stations.At the fish farm,mussels at the FW station grew faster than themusselsat the FE station during autumn and at the FE100 station during winterand spring (pb0.05).

The average growth in length for all stationswas strongly correlatedto 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) (pb0.059), over the en-tire year. While no correlationwas found between the growth in lengthand feed use over the entire year, there was a significant positive corre-lation in the autumn–winter period (r=0.89), when a correspondinglyhigh correlation to SPM was also found (r=0.53) (pb0.05).

3.3. Growth in soft tissue

The standardized dry weight of soft tissue matter (DW′) rangedbetween 290 and 722 mg ind−1 with an average of 517±15 mg,and it exhibited a rapid increase in the summer, reaching peak valuesat the FW and the FE100 stations in September and at the FE and the

image of Fig.�4

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Fig. 6. A) Soft tissue dry weight of mussels (DW′) at the west (FW) and east (FE) side ofthe farm, 100 m east (FE100) and at the reference station (RS) 4 km south of the farmfrom June 2010 to June 2011, and B) SGRDW′ by season and the entire year (mean±se,n=30). Letters andnumbers denote significant differenceswithinmonths. * indicates a sig-nificantly higher DW′ at stations at the salmon farm compared to the reference stationwithin months. ** indicates a significantly higher DW′ at the reference station comparedto stations at the salmon farm within months (pb0.05).

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Fig. 5. A) Shell length (L) (right axis) and average growth in length (AGRL, μm day−1) (leftaxis) at the west (FW) and east (FE) side of the farm, 100 m east (FE100) and at thereference station (RS) 4 km south of the farm from June 2010 to June 2011, and B) averagegrowth 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-nificantly higher AGRL at stations at the salmon farm compared to the reference station.** indicates a significantly higher AGRL at the reference station compared to stations atthe salmon farm within months (pb0.05).


reference stations in October, followed by weight losses in Novemberand December (Fig. 6A,B). Occasionally, increases were found in theperiod from January to May and a major decrease associated withspawning was evident at the FW, FE and the FE100 stations in June.This decrease left the mussels at the reference station with a signifi-cantly higher DW′ compared to that at the fish farm (pb0.05), as op-posed to for the length growth, thus contributing to a significantcorrelation between the SGRDW′ and the growth in length (r=0.46)(pb0.05).

The DW′was significantly positively correlated to the use of feed atthe fish farm (r=0.53) (pb0.05), and the DW′ of mussels at one ormore of the stations at the fish farm was higher compared to the DW′

of mussels at the reference station in August (at the FW station),September (at the FW, FE and F100 stations), October (at the FE sta-tion), December ( at the FW, FE and F100 stations) and February (atthe FE station) (pb0.05). The average SGRDW′was positive at all the sta-tions in summer and negative during autumn. The mussels at the fishfarm stations displayed a negative SGRDW′ in winter and spring whilea positive SGRDW′ was found for mussels at the reference station.

3.4. Incorporation of fatty acids in mussel tissues

3.4.1. PCAThe PCA of fatty acid (FA) profiles indicated a seasonal-dependent

incorporation of salmon fish feed in digestive gland and mantle tissuein mussels, identified by an increased content of percent 18:1 (n-9) oftotal fatty acids. The PCA also revealed an increase in 20:1 (n-9) thatcould be partly related to the incorporation of fish feed. Mussels at thefish farm was weakly separated from mussels at the reference stationin August and strongly in February (Fig. 7A), while no systematic pat-tern of variation or separation of stations at the fish farm from thereference station was found in June (Fig. 7B). The score plot (Fig. 7A,upper panel) for the digestive gland tissue showed that 92% of the var-iance in the data was explained by the two first principal components.

A similar pattern of variation as in the digestive gland tissue wasalso found for the mantle tissue. The fatty acid profile changed in thedirection of the salmon feed profile from the start in June to Augustand February (Fig. 7C), whereas no systematic pattern of variation orseparation of stations at the fish farm from the reference station wasfound in June (Fig. 7D). The changes were more pronounced in the di-rection of the salmon feed signature in February compared to August,although no clear separation was found between the reference stationand the stations at the fish farm. The score plot (Fig. 7C, upper panel)showed that 83% of the variance in the data was explained by the twofirst principal components.

In the digestive gland samples, the loading plots (Fig. 7A, lowerpanel) confirmed the incorporation of 18:1 (n-9) and 20:1 (n-9) inAugust and February. 20:5 (n-3) (eicosapentaenoic acid, EPA) and16:1 (n-7) were the dominant fatty acids at the start, while 18:4 (n-3)and 14:0 contributed more to the total FA profile in mussels in August.

image of Fig.�6


22:6 (n-3) (docosahexaenoic acid, DHA) contributed more to the totalFA profile in mussels at the reference station in February, thereby sepa-rating the mussels in February from the mussels in August togetherwith 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 atthe 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 digestivegland samples (Fig. 7). The FA profile was dominated by EPA and 16:0at the start, while 20:1 (n-9), 18:2 (n-6) and 18:4 (n-3) contributedmore to the total FA profile in mussels in August. As for the digestivegland samples, DHA contributed more to the total FA profile in musselsin February, separating mussels in February from mussels in August incombination with 16:1 (n-7) and 18:1 (n-9).

3.4.2. Digestive glandThegeneral pattern of variation of the total FA content (mg/g),which

reflects the content of total lipids, demonstrated an increase from thestart in June until August, before a decrease was found in February andat the end of the sampling period in June (Fig. 8A). The seasonal changeswere significant at the FE, FE100 and the reference stations (pb0.05). Nodifferences were found for the total FA content in mussels at any of thestations in August and February. The total FA content was also higher atthe FW compared to the FE and the FE100 stations (pb0.05), while no

Fig. 7. A, C) Principal component analysis of fatty acid profiles in digestive gland and mantleand at the reference station (RS) 4 km south of the farm in June 2010, August and February, aloading plots for the corresponding fatty acids' contribution to the score plot. Numbers atexplained by principal components 1 and 2.

statistical differenceswere found between the total FA content of the di-gestive gland tissue ofmussels at the FWand the reference station at theend of the sampling period.

The PCA particularly identified 18:1 (n-9), 20:1 (n-9), DHA, EPA and18:4 (n-3) as the single fatty acids that were most responsible for thedifference between the digestive gland tissue of mussels at the start inJune 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 infish feed, exhibited a similar pattern of variation as the total FA (orlipid) content of the digestive gland tissue over the year (Fig. 8A). Thecontent of 18:1 (n-9) in digestive gland tissue was significantly higherin mussels at the FE station compared to the reference station inFebruary, and significantly higher in mussels at the FW station com-pared to mussels at the FE, FE100 and the reference stations at theend of the sampling period in June (pb0.05). In contrast, the contentof 20:1 (n-9) was significantly higher in the digestive gland tissue ofmussels at the FE and the FE100 stations compared to mussels at theFW and the reference stations in June (p=0.05), while the content of18:2 (n-6) was significantly higher in mussels at the FW station com-pared tomussels at the reference station in February (pb0.05) (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 thisFA 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

tissue of mussels at the west (FW) and east (FE) side of the farm, 100 m east (FE100)nd B, D) June 2011. The upper panels show the score plot, while the lower panels showthe x (PC-1)- and y-axis (PC-2) are the percentages of variance in fatty acid profiles

Fig. 7 (continued).


in February. 20:1 (n-9) increased from 1.3±0.0% to an average of4.5±2.2% for all stations in February, exceeding that of the fish feed(3.1±0%).

3.4.3. MantleA similar pattern of variation of 18:1 (n-9), 20:1 (n-9) and 18:2 (n-6)

aswas found for the digestive gland tissuewas also found for themantletissue, thoughwith some greater variation (Fig. 8B). The total FA contentof mussels at the FW station remained stable over the year, while an in-crease was found for mussels at the FE and FE100 stations, whichresulted in a significantly higher FA content compared to that ofmusselsat the FW and the reference stations at the end of the sampling period(pb0.05).

4. Discussion

4.1. Food availability

The concentrations of suspended particulate matter at all stationsranged consistently above the threshold level of 4 mg L−1 for pseudo-feces production in mussels of 1 g of soft tissue dry matter (Widdowset al., 1979), suggesting that the SPM concentrations did not restrictmussel growth at any time of the year. Furthermore, the significantcorrelation between SPM and the feed use at the fish farm during theautumn–winter (October–February) period suggested that themussels'food availability could be associated with the release of fish feedwastesduring this period. The organic content of the SPM, particularly the car-bon, is a feed variable that largely determines the amount of surplusenergy available for growth (Bayne et al., 1987; Hawkins et al., 1997;

Navarro et al., 2003), and because mussels have shown the sameabsorption efficiency for particulate organic C, N and P, respectively,their growth will depend on the nutritional composition of theabsorbed organic matter and how this meets the mussels' nutritionalrequirements (Hawkins et al., 1997).

As was found for SPM, the POC concentrations correlated well tothe use of feed in winter. According to an estimated minimum feedrequirement 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 ofsoft tissue matter from this population (Handå et al., in press), thePOC concentrations were found to support weight maintenanceand/or growth over the entire year. Even the minimum POC concen-trations in January (95±11 μg C L−1) would leave the mussels witha feed intake of 247 μg C ind−1 h−1, given a clearance rate of 2.6 Lind−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% lowertemperature-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 interms of Chl a might not have met the mussels' energy requirementsas a zero net energy balance is found to be sustained in M. edulis byChl 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; Riisgårdand Larsen, 2001), whereas in a recent study by Strohmeier et al.(2009), it was demonstrated thatM. edulis is capable of clearing particlesout of suspension at Chl a concentrations down to 0.01 μg Chl aL−1,

18:1 (n-9)

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Fig. 8. A) Fatty acid content (mg g−1 dryweight tissue) and contribution of selected fatty acids (% of total FA) to the total fatty acid composition ofmantle and digestive gland ofmussels atthe 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 (pb0.05).


image of Fig.�8


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 salmonfish feed in digestive gland and mantle tissues. This was evident fromthe increased relative content of 18:1 (n-9) in August and February.The response was significantly higher in the digestive gland tissueof mussels at the stations located at the fish farm compared to thatat 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 thanat the reference station in June, whereas a similar contribution tothe 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 moreefficiently in August and February, when phytoplankton concentra-tions were low, compared to after the spring bloom of phytoplanktonin June which provided mussels with their primary food source.

Phytoplankton is a natural part of seston that is selected for byM. edulis prior to ingestion (Kiørboe and Møhlenberg, 1981), andmussels exhibit clearance and selected incorporation among variousphytoplankton 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 andNavarro, 2003). The criteria for selection are not fully known, althoughchemical composition, shape and size have all been suggested to play arole (Jørgensen, 1996; Ward and Targett, 1989).

The selection of phytoplankton over other organic matter in thisstudy can be identified from the incorporation of certain fatty acidsthat 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 and16:0 and EPA in mantle tissue at start in June and the high content of18:4 (n-3) in August, reflected the typical phytoplankton compositionof the spring and an autumn bloom in the Trondheimsfjord area(Sakshaug andMyklestad, 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 inMay in connection with the spring flood of river discharges that wereevident 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 tofreshwater discharge and vertical mixing and tends to be dominatedby dinoflagellates and other small flagellates (Sakshaug and Myklestad,1973; Sakshaug and Olsen, 1986). EPA, 16:1 (n-7) and 16:0 are typicalfatty 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 ishigh in dinoflagellates (Harrington et al., 1970). Accordingly, the highcontent of 16:1 (n-7) in digestive gland tissue, 16:0 in mantle tissueand EPA in digestive gland and mantle tissue at the start suggestedthat diatoms accounted for the larger part of the diet in spring, whilethe increased content of 18:4 (n-3) in digestive gland tissue in Augustsuggested a shift towards a dianoflagellate-dominated diet during sum-mer. The significantly higher content of 18:1 (n-9) in the digestive glandtissue of mussels at the FE and of 18:2 (n-6) at the FW station comparedto the reference station in February suggested an incorporation of fishfeed in mussels at the fish farm in winter, whereas the general increaseof 18:2 (n-6) as well as 18:4 (n-3) in August could be related to musselsfeeding onflagellates, whichhas a high content of these FA (Hammet al.,2001; Reitan et al., 1994) and which has been found in high densities inthe Trondheimsfjord (Haug et al., 1973).

The high content of DHA in the digestive gland tissue of mussels atthe reference station station in February suggested that DHA did notoriginate from the fish feed. The high content of 18:1 (n-9) and 20:1

(n-9) in August could also originate from phytoplankton and even zoo-plankton, in which these FA can be present in high amounts (Sargent etal., 1981 and references therein). However, althoughmussels have beenfound to filter out various sizes of nauplii and copepodite stages of zoo-plankton (Davenport et al., 2000; Lehane and Davenport, 2002; LehaneandDavenport, 2004, 2006;Molloy et al., 2011), it should be questionedand 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 thatphytoplankton 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) andthat other organic particles may also constitute an important part ofthe 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, themussels se-lect for particles with a high organic content (e.g. phytoplankton>fishfeed>feces), resulting in an increased organic content in the consumedfeed 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 foodhas a poororganic content, which leaves mussels feeding on both organic and in-organic materials. Although feces from fish has been suggested to beless suitable for supporting mussel growth compared to fish feed(Handå et al., submitted for publication), mussels are likely to have alow selection coefficient in winter, leaving both fish feed and feces tobe filtered out with a high efficiency.

4.3. Growth in length and soft tissue

Themaximum growth in lengthwas foundwhen thewater temper-ature peaked in August–September and was accompanied by strongvertical mixing and a corresponding autumn bloom of phytoplankton,after which the growth decreased in autumn and remained low inwinter. 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 andthe 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 thepreviously reported growth rate for farmed mussels of a similar length(~38–65 μm day−1) during this period of the year in the landlockedKoet Bay, located close to the study area (Handå et al., 2011).

The growth in length was strongly correlated to temperature andweakly to SPM over the entire year, whereas a significant correlationwas found to the feed use at the fish farm in the autumn–winter period(October–February), hence supporting the results from the PCA of thefatty acid composition showing that fish feed contributed most to themussels' 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 growingon the west side (FW) of the farm in spring compared to the otherstations close to the farm (FE and FE100) and at the reference station,while mussels at the reference station grew faster than mussels at thefish farm during the summer. A comparison of growth in length overthe entire year revealed that mussels at the FE station exhibited equalgrowth rates compared to the mussels at the reference station, whilemussels at the reference station grew faster than the mussels at theFW and the FE100 stations, which was mainly due to the significantlyfaster growth at the reference station in June–July.

Mussels at the reference station grew significantly faster than themussels 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 theyear. Moreover, mussels at thewest side (FW) grew faster thanmussels


at the FE100 station in autumn, winter and spring. The results suggeststhat the placement of mussels should be firmly located in IMTA systemsand that the distance between the fish and mussels should probably beless than the 120 m, as was the distance to the FE100 station, to enablemussels to perform bioremediative services on salmon farm wastesunder environmental conditions such as the ones studied.

In agreement with the growth in length, the specific growth rate ofDW′ 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 andthe general pattern of variation found showed a higher DW′ formusselsat the fish farm in autumn and winter, while the DW′ of mussels at thefish farm and the reference station was more equal in spring andhighest at the reference station in June, most likely because of a moredistinct spawning in mussels at the fish farm and thus a more negativeSGRDW′ compared tomussels at the reference station in spring. Further-more, the significantly higher DW′ at the FE at the beginning of thewin-ter period resulted in a negative SGRDW′ for mussels at this station inwinter, although the DW′ of mussels at the FE station was significantlyhigher than that of the mussels at the reference station both in Decem-ber and February. This suggested that the monthly measured DW′ wasmore representative for growth in weight than the average of the fourseasons (SGRDW′) due to large fluctuations within each period, whilethe four seasons represented the growth in length in a good way. TheDW′ of mussels at the fish farm was particularly higher compared tothat of mussels at the reference station at the FW station in August,the FW, FE and FE100 stations in September and December and at theFE station in October and February, thereby suggesting that themusselsat these stations at the fish farm used less of their energy storage in theautumn and winter months compared to mussels at the referencestation.

4.4. Implications for integrated multi-trophic aquaculture in Norwegiancoastal waters

The results of our study suggested a higher soft tissue content ofmussels cultivated in integrationwith salmon farming than inmonocul-tures during autumn and winter when ambient food availability interms of Chl a are low. This is in agreement with Stirling and Okumus(1995) who examined blue mussels in two lochs in western Scotlandand found that growth in both soft tissue and shell length of musselskept in close proximity to salmon farms were slightly, but significantlyhigher compared to control mussels located further away from thefarms, 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 Norwaygrew faster and did not show marked growth-stoppage rings duringwinter compared to mussels cultivated without any influence fromsalmon farming, while Sarà et al. examined Mytilus galloprovincialisgrown up- and downstream a sea bass (Dicentrarchus labrax) and seabream (Sparus aurata) farm in the Mediterranean and found a fastergrowth in shell length and an increase in total biomass of the musselssituated downstream of the farm compared to mussels at upstream lo-cations associated with significantly higher organic matter and Chl aconcentrations downstream the farm. In contrast, Taylor et al. (1992)studied the influence of salmon farms on growth of M. edulis in BritishColumbia and found that the distance from the salmon farm did nothave any significant influence on the mussel's food availability. Exceptfor that the incorporation of 18:1 (n-9), which was found in highamounts in fish feed, suggested that salmon fish feed constituted a larg-er part of themussel's diet inwinter than during spring and summer, noincreased concentrations of suspended particulatematter or Chl a at thefish farm compared to the reference station was neither found in ourstudy. In another study of co-cultivation of salmon and mussels (M.

edulis) in Australia, Cheshuk et al. (2003) found only some minor andnot significant differences in growth of mussels situated in 70 and100 m distance from salmon cages compared to mussels cultivated 500and 1200 m away. Navarrete-Mier et al. (2010) studied co-cultivationof oyster (Ostrea edulis) and mussels (M. galloprovincialis) cultivated inclose proximity to a sea bass (D. labrax) and sea bream (S. aurata) farmin the Mediterranean and found no differences in growth in length orsoft tissue of mussels cultivated at a distance of 0 to 1800 m away fromthe farm. They did neitherfind any increase in food availability nor incor-poration of components of fish feed in mussel tissue when using stableisotope ratios as tracers. Some possible explanations for this lack ofmeasureable interactions of the co-cultivation have been addressed byTroell et al. (2011). Notwithstanding, despite the many case studies ofthe combined cultivation of fish and bivalves, there seem to bemore 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 assimilativecapacities of farm-derived wastes by filter feeders under ambient culti-vation conditions may explain why, although IMTA has been practicedfor centuries in Asian countries to increase the carrying capacity of in-tensively cultured sea areas, there is still a wait-and-see attitude tothis concept of ecological engineering for the purpose of reducing theenvironmental impact of intensive fish farming in open water in thewestern world (Chopin et al., 2008). The reluctance is reflected by theabsence of continuous research and technological development aimingat designing sophisticated systems for integration of species at lowertrophic levels with today's intensively fed monocultures of fish. Basedon the existing literature it seems that up-scaling of pilot experimentsis a prerequisite for thequantification of thepotential for bioremediativeservices of co-cultivation under various environmental conditions. Bluemussels 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 demonstratean incorporation of fish feed components in bivalves (Gao et al., 2006;Redmond et al., 2010). Redmond et al. (2010) showed, by using stableisotopes and fatty acids as tracers, that blue mussels can incorporatecomponents of salmon fish feed, and several studies have identifiedthe incorporation of fish farm-derivedwaste products in bivalves, there-by suggesting that bivalves can perform bioremediating services whenintegrated with fish farming (e.g. Gao et al., 2006; Mazzola and Sara,2001; Peharda et al., 2007; Soto andMena, 1999). Accordingly, the capa-bility of bivalves to incorporate components of fish feed has been welldocumented, while, on the other hand, little is known about the incor-poration of components of fish feces. The waste particulate food sourcefor mussels to feed on in IMTA with salmon has been seen as the partic-ulate part of both feed and feces. In this studywe only focused on the in-corporation of components of the fish feed and not of feces. Consideringthat feed wastes probably account for less than 5% of the feed use inmodern cage aquaculture of salmon (Mente et al., 2006), and thatmost 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 inclose proximity to the fish suggesting that a part of the feed waste isavailable for mussels to feed on. The largest salmon farms are currentlyproducing 12,000 t of fish per year, with a corresponding feed use of13,800 t (feed conversion ratio=1.15). Given a theoretical 5% feed lossconstitutes 690 t of particles or 345 t particulate organic carbon from asingle farm from which a part can be utilized by mussels. Moreover, a5% feed loss from the Norwegian salmon production of 0.84 million tonsin 2009 (FAO, 2011) comprises 49,500 t of particles, which have thepossibility to be utilized by filter- and deposit feeders in IMTA. Further-more, on a single-farm scale, the bioremediative capacities of musselsmust be considered according to their capability of filtering out fishfeed and feces. On a regional scale, mussels can still contribute to bal-ancing the nutrient concentrations in, e.g. a fjord system, by filtering


out phytoplankton that has accumulated anthropogenic N from fishfarming. Sheltered sites, e.g. fjords with a low current velocity, uniformcurrents and a longwater retention time, have the potential for increasedphytoplankton growth within the IMTA system. However, a low currentspeed is a disadvantage regarding feed wastes in that it will sink rapidlybelow thefish cages, thus constituting anegligible contribution tomusselgrowth at such sites. On the other hand, the feed particles at exposedsites will form a larger part of the food availability for mussels, whereasthe currents will dilute and transport waste nutrients away so quicklythat phytoplankton growth will take place outside the IMTA system. Inany 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 atequal amounts to that of the harvested biomass from mussel farms(Lindahl et al., 2005). The careful monitoring of Chl a levels, in combina-tionwithmodeling of the local current conditions and the correspondingnutrient dispersal patterns downstream from salmon farms, can be auseful tool to localize possibly high productive areas with increased phy-toplankton growth at a distance from the fish farm.Mussel production insuch areas has the potential to contribute in equal terms to traditionalIMTA 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 amountsin fish feed, suggested that salmon fish feed constituted a larger partof the mussel's diet in winter than during spring and summer. Thegrowth in length and soft tissuematter of themussels was closely relat-ed to season while the localization of mussels at the fish farm versus atthe reference stationwas ofminor importance to the result.Meanwhile,five months during autumn and winter with a higher soft tissue weightfor mussels at the fish farm supported a seasonally-dependent utiliza-tion of salmon farm wastes for maintenance and growth of soft tissuematter. The incorporation of components of salmon fish feed andfeces 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 experimentaldesign involving only a limited amount of mussels not allowing for ageneral consideration of the potential contribution of a combined pro-ductionofmussels and salmon tomitigate a potential environmental ef-fect of particulate nutrient wastes from salmon farming. Accordingly,the upscaling of cultures at lower trophic levels in IMTA with salmonis essential to further assess the potential for mitigating the environ-mental effects of farm-derived nutrient wastes, in addition to obtainingincreased growth of species at lower trophic levels in IMTA in e.g. cooltemperate North Atlantic waters. For example, the upscaling can takeplace at existing salmon farms: anchoring frames for fish cages are typ-ically 100×100 m, and provide a 1 ha submerged frame that can easilybe modified to provide anchoring at desired depths fromwhich a float-ing structure, e.g. a collar forfish nets, can beused to producemussels orseaweed 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 Langeat AquaCulture Engineering (ACE) for kindly providing research facil-ities and data on monthly fish biomass and feed usage, and to KjerstiRennan at the Norwegian University of Science and Technology(NTNU) for her fatty acid analysis. The hydrodynamic model for the

Tristein area was set up in the Research Council of Norway project no.199391/I10 (MACROBIOMASS).

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