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In this study, we investigated if juvenile European lobsters Homarus gammarus would eat waste from Atlantic salmon Salmo salar cages in a coastal integrated multi-trophic aquaculture (IMTA) setup and if there were any impacts on growth. Trophic interactions between salmon and lobsters were assessed using δ ¹⁵ N and δ ¹³ C stable isotope analysis and fatty acid profiling from fish feed as indicators of nutrient flow. Analysis revealed that lobsters directly utilised particulate waste from salmon production, as levels of indicator fatty acids from salmon feed were significantly higher in lobster tissues near the fish cages compared to the control site. Route of uptake may have been direct consumption of waste feed or faecal material or indirectly through fouling organisms. Stable isotope analysis did not indicate nutrient transfer to lobsters, suggesting that the duration of the study and/or the amount of waste consumed was not sufficient for stable isotope analysis. Lobsters grew significantly over the trial period at both sites, but there was no significant difference in lobster growth between the sites. Our results show a trophic relationship between salmon and lobsters within this IMTA system, with no apparent advantage or disadvantage to growth.
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Aquacult Environ Interact
Vol. 12: 485– 494, 2020 Published November 5
The European lobster Homarus gammarus (Lin-
naeus, 1758) is an important economic decapod
crusta cean, with a natural distribution ranging from
Morocco to northern Norway (Wilson 2008). Global
demand for lobster is increasing, but over the past few
decades wild stocks have been decreasing (Drengstig
& Bergheim 2013, Ellis et al. 2015, Nillos Kleiven et
al. 2019), prompting research into commercial hatch-
ery production of larvae for restocking purposes
(Addison et al. 1994, Schmalenbach et al. 2011).
However, lobsters grown in land-based hatcheries
and then directly released into the environment are
known to be vulnerable to immediate predation as
they have limited exposure to environmental stimuli
(Agnalt et al. 2017). To improve survivability, sea-
based containers have been used successfully to ac -
climatise juvenile lobsters to environmental condi-
tions before final release (Beal et al. 2002, Perez
Benavente et al. 2010, Beal & Protopopescu 2012,
Daniels et al. 2015, Halswell et al. 2016). At the
release stage, juvenile lobsters form small burrows in
sediment and feed on zooplankton and organic mat-
ter particles suspended in the water column, using
currents created by their pleopods (swimmerets).
The particle sizes consumed at this stage are nor-
mally between 60 and 100 µm (Lavalli & Barshaw
1989), suggesting that they are able to consume fine
particulate wastes from fish farms.
Atlantic salmon Salmo salar cage farms are gener-
ally sited in coastal environments and release nutrient-
© The authors 2020. Open Access under Creative Commons by
Attribution Licence. Use, distribution and reproduction are un -
restricted. Authors and original publication must be credited.
Publisher: Inter-Research ·
*Corresponding author:
European lobsters utilise Atlantic salmon wastes
in coastal integrated multi-trophic aquaculture
A. Baltadakis1,*, J. Casserly2, L. Falconer1, M. Sprague1, T. C. Telfer1
1Institute of Aquaculture, Faculty of Natural Sciences, University of Stirling, Stirling FK9 4LA, UK
2Marine Institute, Rinville, Oranmore H91 R673, Ireland
ABSTRACT: In this study, we investigated if juvenile European lobsters Homarus gammarus would
eat waste from Atlantic salmon Salmo salar cages in a coastal integrated multi-trophic aquacul-
ture (IMTA) setup and if there were any impacts on growth. Trophic interactions between salmon
and lobsters were assessed using δ15N and δ13C stable isotope analysis and fatty acid profiling
from fish feed as indicators of nutrient flow. Analysis revealed that lobsters directly utilised partic-
ulate waste from salmon production, as levels of indicator fatty acids from salmon feed were sig-
nificantly higher in lobster tissues near the fish cages compared to the control site. Route of uptake
may have been direct consumption of waste feed or faecal material or indirectly through fouling
organisms. Stable isotope analysis did not indicate nutrient transfer to lobsters, suggesting that
the duration of the study and/or the amount of waste consumed was not sufficient for stable isotope
analysis. Lobsters grew significantly over the trial period at both sites, but there was no significant
difference in lobster growth between the sites. Our results show a trophic relationship between
salmon and lobsters within this IMTA system, with no apparent advantage or disadvantage to
KEY WORDS: Integrated multi-trophic aquaculture · IMTA · Lobster · Salmon · Fatty acids ·
Stable isotopes · Ecosystem services
486 Aquacult Environ Interact 12: 485–494, 2020
rich particulate and dissolved wastes such organic
carbon and nitrogen from uneaten food and faecal
wastes and excreted soluble nitrogen into the sur-
rounding environment (Wang et al. 2012). The con-
cept of integrated multi-trophic aquaculture (IMTA)
endeavours to utilise these wastes, thereby increasing
the resource efficiency of trophically linked co-cultured
species to improve nutrient uti lisation for environ-
mental mitigation while producing additional organ-
isms (Chopin et al. 2012). Placing lobsters in sea-
based containers next to fish cages may provide a
regular food supply, together with other potentially
beneficial conditions (e.g. shelter, co-location for effi-
ciency improvements), for improved growth and
management. This may also function as an ecosystem
service from salmon aquaculture and provide positive
societal benefits; for example, if there is improve-
ment of growth and better survival when released, it
could aid enhancement of local lobster populations
and any re sulting fishery.
Performance of IMTA can be measured empirically
by comparing growth or nutrient uptake by the con-
sumer species between the culture site and a refer-
ence location. This approach has been used to assess
shellfish growth (Sarà et al. 2009, Lander et al. 2013)
and nutrient uptake and growth of seaweeds (Blouin
et al. 2007, Abreu et al. 2009). Direct nutrient transfer
between species is commonly in vestigated using bio-
chemical tracers, such as fatty acids (FAs) and stable
isotopes (Redmond et al. 2010, Colombo et al. 2016,
White et al. 2019, Sardenne et al. 2020).
FAs have been used to assess the dispersal of par-
ticulate-derived waste, both spatially and through
food webs, with studies assessing the level of influ-
ence aquaculture has on wild fish and benthic com-
munities (e.g. Fernandez-Jover et al. 2009, 2011,
White et al. 2017, 2019, Woodcock et al. 2018). How-
ever, assessing the performance of an IMTA system
with FAs is dependent on the target species, as there
have been variable results using blue mussels Mytilus
edulis (Redmond et al. 2010, Irisarri et al. 2015),
although more consistency has been found for zoo-
plankton (Fernandez-Jover et al. 2009), shrimp (Olsen
et al. 2012) and sea urchins (George & Parrish 2015).
Stable isotopes of carbon and nitrogen have been
used widely to assess the flow of nutrients through
food webs, and more recently, to trace waste products
from aquaculture (Marín Leal et al. 2008, Deudero et
al. 2012). Stable isotopes assimilate within the tissues
of consumers, with heavier isotopes, 13C and 15N, re-
maining longer in animal tissues than lighter ones, 12C
and 14N, which are rapidly utilised during metabolism
(Marín Leal et al. 2008). Consequently, the tissues of
organisms tend to adopt the same stable isotopic signa-
ture as their food source (Paulet et al. 2006). δ13C
and δ15N ratios have been applied for nutrient tracking
within IMTA systems with fish and mussels in the
Bay of Fundy, Canada (Irisarri et al. 2015), fish with
oysters and mussels (Navarrete-Mier et al. 2010) and
in multiple farms with fish and mussels in the Western
Mediterranean (Sanz-Lazaro & Sanchez-Jerez 2017).
The aim of this study was to investigate if juvenile
European lobsters would consume wastes from salmon
cages by assessing the nutrient transfer between
salmon waste and lobsters within a pilot-scale coastal
site and whether there were any positive or negative
effects on growth. FA analysis and stable isotopes were
used as tracers of nutrient transfer, and growth was
determined as an increase in carapace length (CL).
2.1. Experimental site and data collection
The study was conducted at the Lehanagh Pool
marine research site, a small-scale experimental IMTA
site in Bertraghboy Bay, Connemara, County Galway,
Ireland (Fig. 1), between January 2018 and March
2019. The site comprised 2 polar circle cages (50 m
circumference and 8 m deep) at a water depth of 21 m.
These were stocked in April 2018 with 7660 Atlantic
salmon post-smolts (5360 and 2300 in the 2 cages), aver-
aging 90 to 100 g. In addition, 400 lumpfish Cyclopetrus
lumpus, averaging 40−50 g, were also stocked into
each cage as a preventative method for controlling
sea lice as per commercial standards. The fish were
hand-fed a maintenance diet according to the manu-
facturer’s feeding tables. The site was managed ac-
cording to organic farm standards, with no prescrip-
tion medicines or antifoulants used. A control site for
the study was set up approximately 300 m west of the
cages. European lobsters (Stage IV juveniles, n = 204)
were deployed in May 2018 (108 at the cage site, 96 at
the control site) within sea-based container culture
(SBCC) structures (see Daniels et al. 2015). Lobsters (n
= 36) were housed individually and labelled in each
stack suspended from the cages at 2 m depth and
from a longline at the control site at the same depth.
Particulate organic matter loading from the salmon
cages was modelled with a spreadsheet-based partic-
ulate dispersion model (Telfer et al. 2006) to assess the
organic load dispersal and deposition around the cages
and ensure that the SBCC structures were situated
in locations where the lobsters would be ex posed to
salmon waste and that the control site was far enough
Baltadakis et al.: Lobsters and integrated multi-trophic aquaculture
away not to be influenced by particu-
late wastes. The model was run using
data from fish production and measured
current speeds and directions collected
using a MIDAS ECM self-re cording
electromagnetic current meter (Vale-
port) deployed at 2 depths (9 and 14 m)
within 50 m of the cages between 1 and
15 July 2018.
During this time, 3 sediment traps
were positioned to assess the numerical
and distributional accuracy of the model.
Two sediment traps were placed at a
depth of 19 m, one 0 m and one 5 m from
the south-west cage; the latter was be-
tween the 2 cages. The third sediment
trap was deployed at the control site at
5 m depth. Each sediment trap had 4
cylinders with a height:diameter ratio
7.5:1 (60:8 cm) secured vertically on a
gimballed stainless steel frame. A clear
container (plastic fixed pot) was
screwed onto the bottom of every cylinder. The design
of the sediment traps was based on specifications in
Blomqvist & Hakanson (1981). Total sedimentation
rate per m2over 15 d was calculated by dry weight
(DW). Model outputs were compared to amount of
waste material collected in deployed sediment traps
next to the cages to assess model accuracy.
2.2. Lobster growth
Lobsters were deployed in SBCCs at the cage site
at the beginning of April 2018, and growth measure-
ments commenced after a period of 1 mo. Growth of
lobsters was as sessed by measuring CL (mm) on 9
occasions over a 319 d period, between May 2018 and
March 2019. Due to variable weather conditions, be -
tween 20 and 60 lobsters were randomly subsampled
from the cage and control sites, at each sampling
event. Each lobster was re moved from the SBCC unit
and placed on gridded paper. A digital image was
taken at 90 degrees to each specimen. The lobster
was then returned to its container and to the water.
CL was measured from the images using Digi mizer
image analysis software (MedCalc Software).
CL gain (CLG) was used as an indicator of growth
at the cage and control sites and was calculated as:
CLG = CLtCL0(1)
where CLtis final CL and CL0is initial CL.
A von Bertalanffy growth curve (von Bertalanffy
1938) was fitted to the mean CL measurements during
the trial:
where L(t) is CL (mm) as a function of time (t), Lis the
largest lobster CL, and Kis the growth coefficient
2.3. Lipid and FA analysis
At the end of the trial (March 2019), 20 juvenile
lobsters were sampled and stored in a freezer (−20°C)
overnight. The next day, samples were shipped on
ice to the University of Stirling for analysis. Ten indi-
vidual juvenile lobsters from the control and 10 from
the cage location, and a sample of the salmon aqua -
feed used at the cage site were individually homo -
genised and subjected to lipid extraction.
Total lipids were extracted from 0.5−1.0 g of feed
and lobster tissue in ice-cold chloroform:methanol
solution (ratio 2:1, v/v). Extraction of lobster tissue
was achieved using 20 ml of solution and feed using
36 ml of solution. The samples were homogenised in
an Ultra-Turrax tissue disruptor (Fisher Scientific).
Lipid content was determined gravimetrically (Folch
et al. 1957).
FA methyl esters (FAMEs) were separated from
total lipids by acid-catalysed transmethylation at 50°C
( ) {1 exp[– ( )]}
Lt L Kt t=∞−
Fig. 1. Bertraghboy Bay, Ireland, and the location of the marine research site.
The photograph shows the cage site and the sea-based container culture
(SBCC) structures. The black circle indicates the location of the experimental
site in relation to the Irish West Coast
Aquacult Environ Interact 12: 485–494, 2020
for 16 h using 2 ml of 1% (v/v) sulphuric acid (95%,
Aristar®, BDH Chemicals) in methanol and 1 ml
toluene (Christie 1993). FAMEs (6 ml) were extracted
and purified by adsorption chromatography using
500 mg sorbent acid washed solid-phase extraction
cartridges (Clean-up® silica extraction columns; UCT).
Cartridges were pre-conditioned with 5 ml of iso-
hexane before the sample was added and the FAMEs
eluted with 10 ml isohexane:diethyl ether (95:5, v/v)
and separated and quantified by gas-liquid chromato -
graphy using a Fisons GC-8160 (Thermo Scientific)
equipped with a 30 m × 0.32 mm i.d. × 0.25 µm ZB-wax
column (Phenomenex). Hydrogen was used as the
carrier gas with an initial oven gradient of 50 to 150°C at
40°C min−1 to a final temperature of 230°C at 2°C min−1.
Individual FAMEs were identified by comparison to
standards (SupelcoTM 37- FAME mix; Sigma-Aldrich).
All data were collected and processed using Chrom-
CardTM for Windows (Version 1.19; Thermoquest Italia)
software. 17:0 heptadecanoic acid was used as inter-
nal standard to calculate FA content per g of tissue.
Predominant FAs measured within the salmon feed
were used as tracers. A total of 5 FAs were selected.
Three FAs, oleic acid (OA, 18:1n-9), linoleic acid (LA,
18:2n-6) and α-linolenic acid (ALA, 18:3n-3), were
based on the in creased ‘terrestrial’ FAs derived from
an increasing inclusion level of vegetable oil used
within salmon feed (Sprague et al. 2016). Cetoleic acid
(22:1n-11) and eicosenoic acid (20:1n-9) were also cho-
sen, as they tend to be typically found in higher quan-
tities within salmon feed and have consequently been
observed in fish farm waste (Henderson et al. 1997).
2.4. Stable isotope analysis
Five samples of lobster leg muscle from each site
(n = 5 control site, n = 5 cage site) and 2 samples of
salmon feed were subjected to stable isotope analysis.
Each sample was frozen at −20°C prior to lyophilisa-
tion in a Christ Alpha 1-4 LSC freeze-drier (Martin
Christ Gefriertrocknungsanlagen). For the analysis,
0.7 mg of lobster leg muscle and 1.5 mg of feed were
weighted into 3 × 5 mm tin capsules and loaded onto
an Elementar Procure analyser, which converted
organic N and C in the samples to N2and CO2for
measurement of δ15N and δ13C, respectively, on a
Thermo-Fisher-Scientific Delta XP Plus isotope ratio
mass spectrometer.
Units of isotope ratios were expressed in δ15N
and δ13C:
where Xis 13C or 15N, and Ris either the 13C:12C ratio
or the 15N:14N ratio. In-house reference materials
used were: gelatine solution, alanine-gelatine solu-
tion spiked with 13C-alanine, and glycine-gelatine
solution, each dried for 2 h at 70°C. Four USGS 40
glutamic acid standards (Qi et al. 2003, Coplen et al.
2006) were used as independent checks of accuracy.
2.5. Statistical analyses
FA percentages for each sample were arcsine
transformed prior to statistical analysis to correct for
the binomial distribution of proportional data (Sokal
& Rohlf 1995). FAs occupying more than 0.1% of the
feed FA profile were compared between the cage
and the control site, using a 2-sample Student’s t-test.
Statistical tests were performed using MinitabTM sta-
tistical software. Principal component analysis (PCA)
was used to classify and discriminate between the FA
profiles of the lobster samples at different locations.
PCA creates 2 orthogonal values (principal compo-
nents, PCs) which are representative of the original
variables. The higher the PC value is, the more re -
presentative of the data set it is. PCA was per-
formed using MVSP statistical software (KCS). A
non-parametric multivariate ANOSIM was performed
with PRIMER 5 (Clark & Gorley 2001) to detect sig-
nificant differences be tween a priori sources of vari-
ation for the cage site and control site results (as
defined factors) using a Bray-Curtis similarity matrix.
Stable isotopes (δ13C and δ15N) for lobster leg mus-
cle were compared between the 2 locations using a
2-sample Student’s t-test, using Minitab software.
Growth was compared between the 2 locations
over time with a repeated-measures ANOVA, using
SPSS Ver 26 software (IBM). As sphericity is an im -
portant assumption of a repeated-measures ANOVA
(where the variances of the differences between all
possible pairs of within-subject conditions are equal),
the growth data were tested using Mauchly’s test of
3.1. Waste dispersion and current flow at
the cage site
The hydrographic data collected by the current
meter showed that the cage site was characterised by
moderate to slow average current speeds of 0.040 m
s−1 in mid-water and 0.028 m s−1 near the seabed. The
1 1000
Baltadakis et al.: Lobsters and integrated multi-trophic aquaculture 489
residual current flow showed a very slow movement
in a southerly direction over time. Distribution of par-
ticulate waste from the cages over the trial period
was very local to the fish cages, with only low
amounts of particulate waste travelling beyond 20 m
from the cage edge (Fig. 2).
Model predictions of sedimentation for suspended
solids near the SBCC deployment locations (100−
200 g m−2 15 d–1) showed broad agreement with aver-
age sediment trap-collected material (252 g m−2 15 d–1).
However, the model underestimated the distribu-
tion of solid waste between the cages, with modelled
values of 50 and 100 g vs. an average measured value
of 368 g m−2 15 d–1. Both model and sediment traps
illustrated that the SBCCs near the cages were placed
in areas of high particulate waste distribution of
between 100 and 200 g m−2 15 d–1. The models also
showed little possibility that much particulate waste
from the cages would reach the control lobster site
approximately 300 m to the west.
3.2. FAs
The FA profile of lobster tissues varied with loca-
tion, as the amount of FA tracers (given as % of total
lipid) showed significant differences (p < 0.05) be -
tween the cages and control stations (Table 1). Lob-
sters located near the cages had a significantly higher
total lipid content (1.22 ± 0.34 mg g−1 DW; mean ± SD)
than those at the control site (0.93 ± 0.19 mg g−1 DW)
(p < 0.05). The FA profile of the supplemented sal -
mon feed was largely characterised by OA (18:1n-9;
24.4%), eicosenoic acid (20:1n-9; 7.2%), cetoleic acid
(22:1n-11; 12.8%), LA (18:2n-6; 11.6 %) and ALA
(18:3n-3; 4%), confirming that these FAs are indica-
tive and appropriate for use as tracers. The relative
percentages of these FAs were significantly higher
(p < 0.05) in lobsters located near the cage site (Fig. 3)
than in those at the control site. Additionally, n-6
polyunsaturated FA (PUFA) levels were found to be
significantly higher at the cage site (12.24 ± 0.77%)
compared to the control (10.27 ± 0.65 %) (p < 0.05),
with LA (18:2n-6) being higher in the cage (6.3 ±1.4%)
Fig. 2. Contour plot of suspended solids settlement (g m−2
15 d–1) around cages 1 and 2, presented as output from a
spreadsheet-based dispersion model
Feed Lobsters Signifi-
Cages Control cance
Total lipid (%) 24.16 1.22 ± 0.34 0.93 ± 0.18
Fatty acids
14:0 4.6 1.2 ± 0.3 0.5 ± 0.1 ***
16:0 10.6 12.1 ± 0.5 11.8 ± 0.5 NA
18:0 1.5 4.6 ± 0.6 6.8 ± 0.4 ***
20:0 0.3 0.4 ± 0.0 0.5 ± 0.1 ***
Total saturated 17.4 19.3 ± 0.8 20.8 ± 0.5 ***
16:1n-7 3.4 3.1 ± 0.5 2.7 ± 0.4 *
18:1n-9 24.0 14.6 ± 1.6 8.4 ± 0.8 ***
18:1n-7 2.0 5.2 ± 0.4 6.3 ± 0.6 ***
20:1n-9 7.2 3.4 ± 0.5 1.5 ± 0.2 ***
22:1n-11 12.7 3.9 ± 1.2 0.1 ± 0.1 ***
24:1n-9 0.7 0.4 ± 0.1 0.1 ± 0.1 ***
Total monoenes 51.9 33.8 ± 3.6 21.6 ± 1.3 ***
18:2n-6 11.5 6.4 ± 1.4 0.9 ± 0.1 ***
20:2n-6 0.2 1.2 ± 0.2 1.4 ± 0.1 *
20:4n-6 0.3 3.6 ± 0.7 6.6 ± 0.9 ***
Total n-6 PUFAs 12.0 12.2 ± 0.8 10.3 ± 0.7 ***
18:3n-3 4.0 0.8 ± 0.1 0.5 ± 0.1 ***
18:4n-3 2.0 0.6 ± 0.2 0.4 ± 0.1 **
20:3n-3 0.1 0.4 ± 0.0 0.5 ± 0.0 ***
20:4n-3 0.3 0.5 ± 0.1 0.5 ± 0.1 NA
20:5n-3 5.0 14.9 ± 2.0 22.8 ± 1.0 ***
22:5n-3 0.6 1.2 ± 0.2 1.4 ± 0.8 NA
22:6n-3 5.5 13.8 ± 1.5 17.3 ± 1.5 ***
Total n-3 PUFAs 17.8 32.3 ± 3.0 43.3 ± 1.4 ***
Total PUFAs 30.7 44.7 ± 2.6 54.1 ± 1.4 ***
Total DMA 0.0 2.2 ± 0.5 3.4 ± 0.5 ***
Table 1. Fatty acid (FA) profile (% FA of total lipid) of lobster
muscle. Values are means (±SD). Last column indicates
level of significance between the 2 locations (***p < 0.001,
**p < 0.01, *p < 0.05). PUFA: polyunsaturated FA; DMA: di-
methyl acetal. Total saturated FAs also include 15:0, iso17:0,
anteiso17:0, iso18:0, anteiso18:0, 22:0 and 24:0; total mono -
enes also include 16:1n-9, 17:1, 20:1n-11, 20:1n-7 and 22:1n-9;
total n-6 PUFAs also include 18:3n-6, 20:3n-6, 22:4n-6 and
22:5n-6; total n-3 PUFAs also include 21:5n-3; total PUFAs
also include 16:2, 16:3 and 16:4; total DMA includes 16:0
DMA, 18:0 DMA, 18:1 DMA and 20:0 DMA. NA: not appli-
Aquacult Environ Interact 12: 485–494, 2020
compared to the control (0.9 ± 0.1 %) (p < 0.05) (see
Table 1). Overall, tracer FAs accounted for 29.08% of
the total lipid content of the cage station, which was
significantly higher when compared to the control
station (11.36%). Conversely, total n-3 PUFA levels
were significantly higher (p < 0.05) at the control site
(43.27 ± 1.38%) compared to the cage site (32.3± 3%).
FA s contributing to the difference between the con-
trol and the cage site were eicosapentaenoic acid
(EPA, 22.8 ± 1% and 14.9 ± 0.9 %) and docosa-
hexaenoic acid (DHA, 17.2 ± 1.46% and 13.8 ±1.4%),
The PCA plot (Fig. 4) indicated clear differences
between FA profiles of lobster leg muscle from the
cage site and from the control site along PC-1, which
accounted for 92.8% of the total variance in the data.
Post hoc ANOSIM confirmed the groups from control
and cage sites were significantly different (p < 0.05, R =
0.994). The FAs primarily driving this difference at
the cage site were OA (18:1n-9) and LA (18:2n-6) of
terrestrial origin, along with eicosenoic acid (20:1n-9)
and cetoleic acid (22:1n-11). These are marine oil-
based, and both were incorporated at high levels
within the salmon feed. On the other hand, EPA and
DHA together with arachidonic acid (20:4n-6) were
more dominant in defining the FA profile at the con-
trol site, making it likely that the diet of the lobsters
was primarily influenced by naturally derived marine
oils, accounting for 40.4% of total FAs compared to
28.7% for lobsters at the cages (Table 1).
3.3. Stable isotopes
The δ13C and δ15N signatures for lobster tissue at
the control and cage sites were similar, as shown by
their similar positions in the plot (Fig. 5). However,
the signature for salmon feed differed from those
found for lobsters (Fig. 5). A 2-sample Student’s t-test
Fig. 3. Contribution of selected fatty acids (% of total lipid,
mean ± SD) to the total fatty acid content in the lobster tissue
at the end of the experiment (March 2019) at the control and
cage sites. Feed levels are included for reference
–0.01–0.02–0.04–0.05 0.01 0.02 0.04 0.05 0.06
Vector scaling: 0.07
Fig. 4. Principal component analysis for fatty acid profiles
(over 0.1%) from the leg muscle of lobsters taken from the
cage and control sites. Vectors for key fatty acids responsible
for the grouping pattern are displayed
Baltadakis et al.: Lobsters and integrated multi-trophic aquaculture
indicated no significant differences for δ13C or δ15N
between cage and control sites for lobsters (t = 1.33,
df = 5, p = 0.240), and neither showed any similarity
to the signatures for the salmon feed.
3.4. Growth of lobsters
An increase in CL was observed over the trial
period at both cages and control sites. These were fit-
ted to von Bertalanffy growth curves (Fig. 6) using
calculated values of K= 0.0048, t0= −32.08 for the
cage site and K= 0.0044, t0= −0.4318 for the control
site. After Mauchly’s test showing that the data con-
formed to sphericity (W = 0.0224, p = 0.150), the
repeated-measures ANOVA indicated significant
growth in lobsters over the trial period (F = 77.5, p <
0.001) at both sites, although there was no significant
difference in lobster growth between the sites (F =
20.9, p = 0.149).
The aim of this study was to determine if juvenile
European lobsters would feed on waste from salmon
cages in a coastal IMTA setup and assess if there
was a subsequent impact on growth of the lobsters.
Other studies have shown that the flow of wastes
from coastal finfish aquaculture could potentially be
used for aquaculture-based production of extractive
species such as kelp (Fossberg et al. 2018) and
bivalves (Lander et al. 2012). In this study, we eval-
uated a novel combination of co-cultured species
wherein the juvenile lobsters would be used for re -
stocking purposes rather than as an additional eco-
nomic crop.
The results from the FA analysis showed that the
content of OA (18:1n-9), LA (18:2n-6), ALA (18:3n-3),
cetoleic acid (22:1n-11) and eicosenoic acid (20:1n-9),
which were characteristic of the salmon feed used,
were each significantly higher in the tissues of the
lobsters located near the cages than in those at the
control location. The PCA further confirmed these
results, as the lobsters at the cage and control sites
showed distinctly different FA profiles, which sug-
gests different food sources. The FA profile of lob-
sters at the cage site was clearly influenced by the
salmon feed, whereas at the control site, lobster
nutrition was dominated by natural marine oils.
In contrast, stable isotope analysis of lobster leg
muscle taken at the cage and control sites showed lit-
tle difference in the δ15N ratio between locations, nor
was there a similarity between the signature ratio for
lobster tissue and salmon feed. There may be several
reasons for the differences between the FA tracers
and the stable isotope analysis. Bethoney et al. (2011)
demonstrated that δ15N values in lobster tissue
reflect their long-term diet, so the time-period of our
study may not have been long enough. Another con-
sideration is that there may have been an insufficient
amount of waste consumed to establish an isotopic
signal, as lobsters are slow and periodic feeders (Bor-
dner & Conklin 1981).
Fig. 5. Biplot of δ15N and δ13C (mean ± SD) stable isotopes
of lobster leg muscle and supplemented feed between
cage and control stations at the end of the trial in
March 2019
Fig. 6. Growth curves of lobsters between control and cage
stations, based on measured values (mean ± SD). Von Berta-
lanffy growth functions plotted by trial day and increases in
carapace length for 319 d of the trial. Parameters estimated
for the cage site were L= 9.43, K= 0.0044, t0= −0.4318, and
control site L= 8.44, K= 0.0048, t0= −0.3208
Aquacult Environ Interact 12: 485–494, 2020
Based on their FA profiles, juvenile lobsters at
the cage site consumed fish farm nutrient waste,
although it was not clear if this was direct or indirect.
The sizes of waste feed and faecal particles in the
water column from the salmon cages were not meas-
ured in this experiment, but other studies have
shown that suspended particulate organic matter
originating from cages is often between 1 and 10 µm
(Lander et al. 2013) and up to 300 µm (Law et al.
2014). As the internal mesh size of the SBCC struc-
tures was 2.5 × 2.5 mm (Daniels et al. 2015), particles
of waste this size could have entered the SBCC and
been within the size range eaten directly by juvenile
lobsters (Lavalli & Barshaw 1989). Studies have
demonstrated direct uptake of waste particles by
consumer IMTA species (Handå et al. 2012, Bergvik
et al. 2019). However, in the marine environment
there will be a wider dietary choice and a complex
food web. An in situ study showed that mussels did
not directly assimilate wastes and had a selective
diet, preferring other sources of food (Sanz-Lazaro &
Sanchez-Jerez 2017). Even within the SBCC system,
there would be a dietary choice (Daniels et al. 2015),
and the uptake of wastes by lobsters could have been
indirect via fouling organisms.
Despite the differences in the FA profiles of the
juvenile lobsters at the cage site and the reference
site, there was no significant difference in growth.
Information on growth rates of wild juvenile Euro-
pean lobsters is scarce (Mercer et al. 2001, Wahle et
al. 2013), which prevents comparison to natural con-
ditions. Stage IV is the first postlarval stage of the
life cycle, and juvenile lobsters are transitioning to
benthic organisms (Charmantier et al. 1991). There-
fore, the position of the SBCC may not have been
deep enough in the water column for their feeding
behaviour and could have influenced the results, as
other studies have shown that depth can be an
important factor in IMTA systems (Sanz-Lazaro et
al. 2018). There will always be multiple factors to
consider in designing the optimal setup and there
will often be trade-offs (Halswell et al. 2018). In this
case, the scale of the experimental site meant there
were limited options to position the SBCC within the
waste stream of the fish cage. This study focussed
on 1 cage site and 1 control site, but the dispersal of
wastes around fish cages varies depending on site
characteristics, and other locations may have had
different results. Furthermore, this research used a
pilot-scale experimental site, but the results may be
different if the research was repeated at a full-
scale commercial farm, as there would be higher
volumes of waste.
Previous studies have demonstrated the advantage
of acclimatising juvenile lobsters using in situ containers
as a way of improving survivability (Beal et al. 2002,
Perez Benavente et al. 2010, Beal & Proto po pescu 2012,
Daniels et al. 2015, Halswell et al. 2016), and locating
an SBCC next to salmon cages might offer additional
shelter from storm events. However, it is also impor-
tant to note that fish medication can be harmful to ju-
venile lobsters, and is often used to treat fish diseases
(Burridge et al. 2014, Cresci et al. 2018). The effect of
routine operations, such as disease treatment, on the
different components of an IMTA system is not only an
issue for lobsters and salmon, but is an essential con-
sideration for any combination of species in an IMTA
system. For example, lobsters could only be deployed
at sites which use non-medicinal treatments.
The interaction between salmon cages and wild
lobsters is an important area of research, especially
in Canada where studies have explored the conflict
over use of space between salmon farms and lobster
fisheries (Walters 2007, Grant et al. 2019). In Canada
and Norway, research has also focussed on the
potential impact of medicinal treatments used for
salmon aquaculture on lobsters (Burridge et al. 2014,
Cresci et al. 2018). This present study focussed on
potential benefits of having lobsters in an IMTA sys-
tem alongside salmon cages prior to release into the
wild for restocking purposes. The results clearly
demonstrated utilisation of wastes from the salmon
cages, but this had no obvious impact on growth.
Other potential implications for lobster physiology,
metabolic processes and behaviour were not ex -
plored. Sardenne et al. (2020) suggested that a diet
shift toward waste fish feed may have an influence
on reproductive success in some wild crustaceans.
Therefore, although a trophic connection has been
established within this system, further research and
trials will be required to determine if a coastal
salmon−lobster IMTA setup would be appropriate as
a stage in lobster restocking programmes.
Acknowledgements. This work received funding from the
European Union’s Horizon 2020 research and innovation
programme under Grant Agreement No. 678396 (Tools for
Assessment and Planning of Aquaculture Sustainability,
TAPAS). We are grateful to Dr. Ronan Browne, Bord Ias-
caigh Mhara and to the staff of the Marine Institute, par-
ticularly Frank Kane, for kindly providing administrative
management and practical support through the sampling
campaign. We also thank Dr. Carly Daniels and the staff
of the National Lobster Hatchery for their support; the
Nutritional Analytical Services, University of Stirling, for
providing analytical facilities; and Maria Scolamacchia
and Jessica Di Toro for providing training support on FA
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Editorial responsibility: Philippe Archambault,
Rimouski, Québec, Canada
Submitted: January 27, 2020; Accepted: September 7, 2020
Proofs received from author(s): October 30, 2020
... gammarus) were held for 319 days close to salmon sea cages. 169 The study showed that the lobsters utilised the salmon waste residues as a food source through stable isotope analysis; however, growth performance was not improved or decreased by this farming strategy. The co-culture dependency would add to the production time scale to achieve the optimal harvest weight of lobsters and would likely be challenging in practice, e.g., disease outbreaks and treatments on the salmon and changing water temperatures. ...
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... The spatial arrangement of the IMTA setup at the farm site ( Fig. 1C) was based on the output of a particulate depositional model Baltadakis et al., 2020). The spreadsheet-based model uses production information, hydrography, and empirically derived measurements to determine the amount of organic carbon and the form of waste that is dispersed from the fish farm to the environment. ...
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Responsible aquaculture, the farming of aquatic organisms, is a sustainable strategic sector for land and coastal communities. It significantly contributes to food security and enhancement of economic development; it provides employment opportunities and often contributes to the ecological services provided by the environment. According to the Food and Agriculture Organization of the United Nations (FAO), the contribution of aquaculture to the global food security is widely demonstrated by an astounding industry growth of 7.5% per year since 1970. In 2018, aquaculture reached the all-time highest production of 114.5 million tonnes in live weight with a total farm gate sale value of USD 263.6 billion. This makes aquaculture a key player within the Blue Growth concept and a strong contributor to some of its key Sustainable Development Goals (SDG). This is particularly true in geographical areas where dependence of local economies on fishery products is high, and yet access to sustainable landings is hampered by ecological barriers. One such area is represented by the Black Sea basin. Whilst the Black Sea annual capture fishery production has varied considerably since 1990 and its current landings are significant, growing attention is currently given to boost aquaculture development along the Black Sea bordering countries, with marine aquaculture being considered as an important contributor to the total fisheries production. Nonetheless, aquaculture development in this region is not homogenous and its development has, so far, been limited by environmental, economic, social, and more generally governance issues. This paper, for the first time, attempts to provide a comprehensive fresh outlook of the aquaculture sector in the Black Sea, stressing the importance of regional cooperation as an essential pillar to support the sustainable development of the industry. The paper addresses aquaculture in the Black Sea from different perspectives: it outlines the key characteristics of the Black Sea environment; it discusses the most common farmed aquatic species and the potential for new ones; it frames the national approaches to aquaculture development, sharing information about success stories, while shedding light on the main challenges and priorities ahead. This collective endeavour will represent a helpful contribution to Black Sea riparian countries to answer the many questions they have, and expectations they hold from the aquaculture sector.
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The European lobster (Homarus gammarus) has been the subject of aquaculture and related research for the last 150 years, due to both the wild fishery and cultural value of the species. Since the middle of the 20th century, increasing anthropogenic pressure has led to a severe decline in wild fish and shellfish stocks, including H. gammarus, with some fisheries yet to recover. H. gammarus is amongst the most exclusive and valuable European shellfish products, and whilst management measures have been implemented to safeguard stocks, H. gammarus aquaculture is an increasingly credible approach to help to secure sustainable lobster supply. Historically, this has been achieved by relatively small scale release of hatchery reared juveniles during stock enhancement programmes. Until recently, commercial attempts at farming have not been viable, mainly due to cost prohibitive technical challenges. At present, there are several promising approaches to overcome bottlenecks hampering commercialisation of lobster aquaculture. This review summarises new technical and husbandry innovations in H. gammarus culture since the start of the 21st century, including technological innovations, husbandry and expansion of the stock enhancement (release) and farming (production)sectors. Additionally, likely directions for both sectors in the coming decades are summarised, knowledge gaps identified, and the societal support required to achieve further potential are discussed.
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Rock crab Cancer irroratus and American lobster Homarus americanus are important commercial species in coastal areas where intensive salmon aquaculture occurs in eastern Canada. Such aquaculture releases organic wastes, especially feed waste (i.e. food pellets made in part from terrestrial feed ingredients). Terrestrial compounds from feed wastes were used to trace their consumption by the two decapods in the Bay of Fundy, Canada. Both species were collected in farms and reference sites and their fatty acid profiles evaluated. Individuals in close proximity to salmon farms were found to consume waste feed (high proportions of 18:1n-9 and 18:2n-6 and low proportions of 20:5n-3 and 22:6n-3). This consumption is associated with a reduction in diet diversity and a trend of increased lipid content in rock crab, suggesting that this species is more receptive to the waste feed than the American lobster, which did not show evidence of diet diversity loss and of increased lipid content. Fatty acid profiles from rock crab ovaries were also affected by the diet shift toward waste feed (low proportion of long-chain essential fatty acids), suggesting a potential influence on crab reproductive success. However, this remains to be assessed. Resulting effects of diet shifts on the ecosystem (e.g. reduction in the consumption of primary consumers and change of fatty acids transferred to predatory fish or gulls through decapods) should be evaluated to assess the spatial and temporal scales of the salmon aquaculture footprint. If the assessment reveals a strong footprint, measures to reduce wastes could be considered (e.g. pellets with greater buoyancy or with different recipe).
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Marine protected areas (MPAs) are considered viable fisheries management tools due to their potential benefits of adult spillover and recruitment subsidy to nearby fisheries. However, before–after control–impact studies that explore the biological and fishery effects of MPAs to surrounding fisheries are scarce. We present results from a fine-scale spatial gradient study conducted before and after the implementation of a 5 km2 lobster MPA in southern Norway. A significant nonlinear response in lobster abundance, estimated as catch-per-unit-effort (CPUE) from experimental fishing, was detected within 2 years of protection. After 4 years, CPUE values inside the MPA had increased by a magnitude of 2.6 compared to before-protection values. CPUE showed a significant nonlinear decline from the centre of the MPA, with a depression immediately outside the border and a plateau in fished areas. Overall fishing pressure almost doubled over the course of the study. The highest increase in fishing pressure (by a magnitude of 3) was recorded within 1 km of the MPA border, providing a plausible cause for the depression in CPUE. Taken together, these results demonstrate the need to regulate fishing pressure in surrounding areas when MPAs are implemented as fishery management tools.
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Juvenile scallops of Pecten maximus were studied to see the capability to clear out and incorporate salmon feed and feces (30 μg L⁻¹). Algae were also given, in a low and high concentration in addition to feed and feces, to mimic a winter and summer situation in Norwegian waters. Rhodomonas baltica and Chaetoseris muelleri were provided in a concentration of 50 μg L⁻¹ and 300 μg L⁻¹. The feeding trial lasted for 27 days. Clearance rate was measured to study filtration characteristics, while fatty acid profiling and stable isotopes of nitrogen and carbon were used to trace the uptake of salmon feed and feces in the digestive gland and muscle of juvenile scallops (30-35 mm shell height). The results show that the scallops could clear out and retain both salmon feed and feces particles, although at a statistically lower clearance rate than the algae. Fatty acid profiling revealed that the scallops assimilated and incorporated the consumed salmon feed and feces, given with either high or low algae concentrations, in their tissues, where the fatty acid C18:1n9 was used as a tracer fatty acid. The digestive gland of the scallops that were fed salmon feed and feces contained a higher share of C18:1n9 than those that were only fed algae. The digestive gland reflected the fatty acid composition of the diet, while the fatty acid composition of the muscle, which also changed, reflected a more complex relation between diet and metabolic processes in the tissue. The use of stable isotopes of carbon and nitrogen to trace food sources was inconclusive in this study due to low differences between samples fed different feeds. Fatty acid profiling was a more sensitive method for tracing low concentrations of salmon feed and feces in the algae diet of scallops. Our results suggest that P. maximus could be a candidate for integrated multitrophic aquaculture (IMTA) and that scallops have the potential to utilize small particles of wasted salmon feed and feces during a winter situation with low phytoplankton concentration and during an algal bloom in Norwegian waters.
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Integrated multi-trophic aquaculture (IMTA) has the potential of reducing open-cage fish farming impacts on the environment while also introducing new value chains. The aim of this study was to investigate the growth and composition of the kelp Saccharina latissima in salmon-driven IMTA, and to assess the spatial extent of the influence of salmon derived nitrogen in order to evaluate the upscaling potential for IMTA. S. latissima was cultivated 100, 200, and 1,000 m east and 1,000 m west of a 5,000 tons salmon farm in Western Norway from February to September 2013. The proportion of salmon derived nitrogen available for the kelp showed a clear decline with distance from the farm. Accordingly, the kelp cultivated near the salmon cages grew faster during the spring season, and growth rate decreased with increasing distance from the farm. A spatially explicit numerical model system (SINMOD), including compartments for dissolved nutrients and kelp growth, was tuned to the field data and used to investigate the potential for upscaling IMTA production. The model was used to introduce a new metric—the impacted area IA—for the areal effects of IMTA in terms of the increase in production by IMTA. The model showed that a 25 hectare kelp farm in the vicinity of the studied salmon farm could take up 1.6 of the 13.5 tons of dissolved inorganic nitrogen released during kelp cultivation, amounting to almost 12% of the ammonia released during the cultivation period from February to June. The 25 hectare kelp farm would have a production yield of 1,125 tons fresh weight (FW), being 60% more than that of a non-IMTA kelp farm, while a 20% increase of kelp FW could be obtained over a 110 hectar area in salmon-driven IMTA. To achieve an even mass balance, an area of approximately 220 ha−1 would be needed to cultivate enough kelp to fix an equivalent of the nitrogen released by the fish.
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Sea Based Container Culture (SBCC) is a mariculture technique that relies on the natural maintenance of environmental conditions, such as Dissolved Oxygen (DO) concentration and feed availability. This paper discusses a framework to evaluate the rearing success of European Lobsters (Homarus gammarus) in SBCC based on temporal and spatial variations of external parameters, including current velocity, wave velocity, turbulent fluctuations and dissolved oxygen concentrations. The temporal variations considered annual changes to the environment and the effect of biofouling growth, and the spatial variations considered the geographical location (case study of Falmouth bay, Cornwall) and vertical position in the water column. The internal parameters of the containers were modelled using transfer functions derived from previous experimental data. The internal parameters were compared to rearing limitations selected from available literature, which included foraging and mobility behaviours, and DO consumption. The time that internal parameters exceeded the rearing limitations was quantified, allowing rearing success to be predicted. This paper uses a case study of external parameters measured in Cornish waters, UK, to demonstrate the framework methodology. The framework showed that in situ measurements of current, wave and turbulence could be used to predict the internal parameters of SBCC containers, which can be used to predict theoretical rearing success based on rearing limitations. The framework indicated that DO concentrations within the containers should not affect rearing success; however, the foraging and mobility limits were exceeded by 0 to 30% of the time (depending on vertical position in the water column and assessment method). The paper aims to demonstrate the generic framework methodology and understands its limitations in predicting rearing success. The framework provides a tool to optimise the SBCC design for spatial and temporal varying conditions related to a geographical location or (vice versa) identify suitable mariculture sites based on SBCC design and environmental conditions. Additionally, the framework can optimise the vertical position of the SBCC in the water column and identify, from parameters considered, those that are most likely to affect rearing success.
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Bivalve cultivation, in single cultivation or in polyculture (including integrated multitrophic aquaculture; IMTA), is generally limited to eutrophic waters. We carried out a modeling study to test if, under meso- and oligotrophic conditions, depth could be a key factor for bivalve productivity associated to IMTA and other polyculture strategies. We applied the model Farm Aquaculture Resource Management (FARM) at three strata of the water column in two coastal fish farm areas in the Mediterranean Sea, using water column variables sampled seasonally to estimate the potential mussel production. According to FARM, mussel production was high in both areas and, in some cases, almost doubled when mussels were cultured below 25-m depth compared to shallower levels. Phytoplankton abundance is expected to notably influence mussel production compared to particulate organic matter. Thus, in meso- and oligotrophic stratified waters, where chlorophyll maximum is relatively deep, depth can be a key factor for the productivity of mussel cultivation. The obtained results could help to maximize the production of suspension-feeding bivalve cultivation and, therefore, the expansion and development of sustainable aquaculture in non-eutrophic marine waters.
Wild lobster (Homarus americanus) abundance was monitored before, during, and after salmon (Salmo salar) aquaculture production in a bay on Grand Manan Island, New Brunswick, Canada, in an 8-year survey, 2008 to 2015. Diver transects and free-area spot-dives were used to measure the carapace length and determine sex (including berried state) of each lobster encountered both inside (farm) and outside (reference) the lease boundaries. In pairwise comparisons of each sampling date, there was no significant difference between the number of lobsters inside the salmon farming area versus a nearby reference site and no significant difference in the number of berried females inside or out of the farm lease area. Combining data from all lobster surveys (farm and reference sites) indicated an increase over 8 years, similar in slope to the increase of the trap fishery in Lobster Fishing Area (LFA) 38. These results indicate that the fish farm had no obvious impact on lobster density at any point in the salmon production cycle and that inshore lobster abundance followed trends similar to those of the general fishery of LFA 38.
Organic waste released from fin-fish aquaculture is being dispersed further as industry growth has led to the expansion of open net cages in dynamic coastal locations. Here we investigate the response of three mobile epibenthic invertebrates (brittle stars, urchins and brown crabs), whose natural habitats overlap with large scale coastal salmon farming. Using fatty acids and stable isotopes, we found these organisms displayed decreases in δ13C and δ15N and elevated levels of C18fatty acids reflective of terrestrial components of fin-fish feeds. Furthermore, we found these three species consume aquaculture organic waste not only directly adjacent to the farm vicinity (0-20 m from cage edge) but up to 1 km away in the case of brittle stars and brown crabs. As aquaculture feeds shift to contain more terrestrial ingredients, the biochemistry of fauna feeding on organic waste is also being shifted, the result of these changes is currently unclear.
Waste from open-cage aquaculture flows directly into the marine environment from uneaten feeds, faecal material and dissolved nutrients. Sustainable management outcomes are regularly based on the dispersal patterns of the waste, with biochemical tracing a key tool in understanding the footprint of aquaculture. We examined the use of fatty acid (FA) analysis to trace aquaculture waste for this purpose, with the aim of identifying specific biomarkers for environmental applications, as well as identifying challenges that are regularly encountered. Overall, the widespread use of terrestrial-based oils in the production of marine aquaculture feeds has increased the use of FA biomarkers to trace aquaculture waste across benthic and pelagic systems, in vertebrates, invertebrates and environmental samples such as sediment and seston. A combination of linoleic acid (LA), oleic acid (OA) and α-linolenic acid (ALA), which are dominant C18 FA in terrestrial seed and animal oils, is the most commonly used biomarkers, along with overall shifts in FA profile related to diet. A challenge regularly encountered, particularly in lower trophic species, was the capacity of an organism to biomodify or selectively spare certain dietary FA, which can mask assimilation of aquaculture-derived FA. In these species, controlled feeding studies are needed to properly understand FA metabolism and to ensure correct interpretation of FA data collected from wild samples. Overall, as FA biomarkers have the capacity to link aquaculture waste in the environment with potential effect, they are a valuable and increasingly applied tool for examining the overall influence of aquaculture in marine ecosystems.