Aquaculture Research, 2015, 46, 1369–1383
12291
Effects of stocking density on survival, growth and
biochemical composition of cultured mussels (Mytilus
galloprovincialis, Lamarck 1819) from an offshore
submerged longline system
ucel1, Meryem Yesßim C
Sedat Karay€ _
ß elik1, Ismihan
ucel1, Recep Ozt€
Karay€
2
Bora Ey€
ubo
glu
1
Faculty of Fisheries and Aquaculture, Sinop University, Sinop, Turkey
2
School of Fisheries and Aquaculture, Sinop University, Sinop, Turkey
ß elik, Faculty of Fisheries and Aquaculture, Sinop University, Sinop 57100, Turkey.
Correspondence: M Y C
E-mail: yesimcelik@yahoo.com.tr
Abstract
This study examined an offshore submerged mus-
sel longline system, in the Black Sea, from May
2009 to May 2010. The system was allowed
1 year for spat collection. After a 1-year spat col-
lection period, some spat collectors were left
untouched (NS), and some spat collectors were
grazed and socked (S) for a grow-out study in May
2009. The effects of stocking density on the
growth and survival of the S and NS mussels were
examined. The biochemical composition of the mus-
sels was also determined. Environmental factors
including temperature, salinity, chlorophyll a, total
suspended matter, inorganic matter and organic
matter were monitored monthly during the experi-
mental period. In May 2010, the mean length and
live weight of the S and NS mussels were
60.46
0.60 mm and 53.34
0.37 mm, respec-
tively, and 20.50
0.50 g and 13.11
0.26 g
respectively. Mean moisture and ash were 82.35

0.47% and 6.67
0.44% respectively. Mean car-
bohydrate, protein and lipid were 27.74
2.40%,
57.68
2.15% and 7.91
0.68% respectively.
These results indicate that a submerged offshore
mussel culture system in the Black Sea can be
commercially convenient. In addition, stock man-
agement via thinning out of the spat can consider-
ably increase the marketable size of mussels,
reduce harvest time and produce better growth.
Keywords: Mussel, offshore, density, growth,
survival, biochemical
© 2013 John Wiley & Sons Ltd
doi:10.1111/are.
€ urk1 &
Introduction
United Nations Food and Agricultural Organiza-
tion (FAO) statistics indicates that mussels are one
of the most popular cultured species. The culturing
of mussels has increased from 1307 thousand
tonnes to 1812 thousand tonnes in the last few
decades (FAO/Fishstat Plus 2012).
For a long time, mussel farms have been limited
to sheltered coastal lagoons (Burbridge, Hendrick,
Roth & Rosenthal 2001). According to Danioux,
Loste and Paquotte (1997), coastal lagoons have
rich and easily accessible but fragile environments
that have been exploited to their maximum spatial
and biological capacity. These researchers have
also stated that several risk factors, at times simul-
taneously, have limited the expansion of the
mussel farming activity in the restricted lagoon
environment: (i) the necessary intensification of
production to reduce production costs; (ii) pollu-
tion from industrial and domestic sources, which
produces high mortality at times and (iii) the
limited renewal of the environment due to a lack
of strong tides, which brings with it a dystrophic
crisis and anoxia risk. Inshore sites have also
proven to have lower growth and higher disease
rates, with greater risks of contamination from
overuse and other activities. Due to these chal-
lenges, to date, the mussel production achieved
has not increased enough to meet demand. As a
result, offshore mussel culture has been suggested
as a solution to meet the growing demand
(Langan 2008).
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Offshore mussel culture in the Black Sea region S Karay€ucel et al.
Currently, technological developments in the
aquaculture sector have made it possible to estab-
lish open-sea mussel culture systems. The offshore
systems available for aquaculture have been
designed through the modification in coastal struc-
tures or techniques such as longlines or rafts
(Stevens, Plew, Hartstein & Fredriksson 2008).
Many studies have determined that the most con-
venient offshore system would be longline systems
(Danioux et al. 1997; Langan & Horton 2003; Buck
2007a; Brenner 2009). In addition, the growth
rate of mussels has been reported to be better
using longline systems because mussels on the
longline are fully suspended in the water and,
therefore, flushed by phytoplankton-rich sea water
(Buck 2007a).
The survival and growth rates of mussels is
directly related to environmental conditions
included temperature, salinity, total particulate
matter, organic matter, inorganic matter and chlo-
rophyll a of the seawater they are growing in
(Dickie, Boudreau & Freeman 1984; Jones &
Iwama 1991; Karay€ ucel & Karay€ucel 1999, 2001;
Manoj Nair & Appukuttan 2003; Ren & Ross
2005). In addition, many studies have stated
that mussel density negatively affects feeding and
loss rate because of increasing competition for
food and space (Alfaro 2006). Comeau, Drapeau,
Landry and Davidson (2008) reported that there
was a strong relationship between the time to
reach market size and mussel density, and culti-
vated mussels grow better because of better feed-
ing. However, some authors have reported that
offshore farms allow higher growth rates, better
meat yield and heavier production compared with
inshore farms due to lower stress, reduced turbid-
ity and better water exchange (Langan & Horton
2003; Brenner 2009).
In addition to aiding in assuring healthy food
and safe consumption, the quality of mussel meat
mainly depends on the quality of the aquatic envi-
ronment (Karakoltsidis, Zotos & Constantinides
1995). The nutritional and commercial value of
mussels is determined according to their moisture,
protein level, lipid level, carbohydrate level and con-
dition index. Knowledge of the mussel reproductive
period and biochemical composition is very impor-
tant for successful mussel cultivation. Seasonal
biochemical composition is related to water temper-
ature, food availability, gonadal maturation and
spawning (Okumus & Stirling 1998; Karay€ ucel,
Erdem, Uyan, Saygun & Karay€ ucel 2002; Orban,
1370
Aquaculture Research, 2015, 46, 1369–1383
Dilena, Nevigato, Casini, Marzetti & Caproni 2002).
In general, when food is abundant, reserves
accumulate prior to gametogenesis in the form of
glycogen, lipid and protein. These reserves are sub-
sequently utilized in the production of gametes
when metabolic demand is high (Dridi, Romdhane
& Elcafsi 2007; Serdar & L€ok 2009).
In Turkey, mussel (Mytilus galloprovincialis) is
the only shellfish species cultured in coastal areas
and cultivation was only 87 tonnes per year in
2009 (FAO/Fishstat Plus 2012). There are no
studies available for offshore submerged design to
serve as models for entrepreneurs interested in
mussel longline cultivation, and no data are avail-
able on the condition index and biochemical com-
position of mussels harvested from offshore sites in
the Mediterranean, Black and Aegean seas. This is
the first experiment in Turkish waters where a
submerged longline design was installed to resist
offshore site conditions, evaluate system strength
and focus on site selection criteria. Furthermore,
mussel growth and production were evaluated
from thinning out to harvest in a longline system,
in both socked rope-type and untouched rope-type
collectors in open-sea conditions. The biochemical
content (protein, lipid, carbohydrate, ash and dry
matter levels) and condition index of the cultivated
mussels from the offshore submerged longline
system were investigated.
Materials and methods
Study area and construction of the submerged
longline system
The study was carried in Sinop at a depth 25–27 m
at an offshore site in the Black Sea region between
May 2009 and May 2010 (Fig. 1). This area was
chosen due to harsh weather conditions, and a
longline system was designed according to site
conditions.
The system was established at 10 m below the
water surface to maintain the system despite strong
currents and waves. The 50-m-long mainline and
the anchor lines of the system comprised 32-mm-
diameter polypropylene rope. In addition, 330-L
surface buoys were manufactured from superior
quality high-density polyethylene (HDPE), filled
with polyurethane foam and had dipped galvanized
steel construction. The buoys were then fixed with
a chain (15 mm in diameter) at each end and the
middle of the mainline. Thirty L marker buoys
© 2013 John Wiley & Sons Ltd, Aquaculture Research, 46, 1369–1383
Aquaculture Research, 2015, 46, 1369–1383
were used on the edges of the experimental area to
mark and protect the site for navigation purposes.
The longline was fixed with four plug anchors
(250 kg), and a 50-kg concrete block also placed
in the middle of the longline system. These anchor
types were selected for the use on the muddy sea
bottom for long-term durability. Two plug anchors,
which were vertically below the mainline, were
tied without chain, and another two, which were
below the marker buoys, were connected with
chain (38 mm in diameter and 7 m in length) to
the anchor line to provide flexibility to the mooring
system of the longline. All connection points were
Figure 1 The study area.
Figure 2 Design of the submerged
longline system.
© 2013 John Wiley & Sons Ltd, Aquaculture Research, 46, 1369–1383
Offshore mussel culture in the Black Sea region S Karay€
ucel et al.
connected using omega shackles, galvanized thim-
bles and swivels. The longline system had a strong
configuration to resist all harsh weather condi-
tions. Furthermore, two flashing lights with a
waterproof body were placed on buoys (330 L) at
each end of the mainline for marking purposes and
to establish the edges of the experiment area to
mark and also protect the site for navigation
(Fig. 2). After installation of the system was
completed, polypropylene experimental ropes were
hung to the longline system. To prevent the
collapse of the mainline due to growth of mussels,
20-L floats were tied to the mainline.
1371
Offshore mussel culture in the Black Sea region S Karay€ucel et al.
Experimental design and sampling procedure
The system was allowed 1 year for spat collection.
After the 1-year spat collection, some of the spat
collectors were left untouched, and some spat col-
lectors were grazed and socked for a grow-out
study. The average density was 2116.67
44.10
individuals m1 (ind.m1) with a mean length of
39.21
0.67 mm and mean weight of 5.57

0.23 g for the untouched, and the average density
was 467.33
19.77 ind.m1 with a mean length
of 40.90
0.23 mm and mean weight of 6.52

0.08 g for socked mussels respectively. The small
spats dropped through a mesh (sock had an 11 cm
width and a 4 cm mesh size) during sock filling.
Approximately one spat collector had enough mus-
sels to fill three socks for grow-out. These were used
to compare two different treatments, thinned out
(S type) and without thinning out (NS type), to eval-
uate the effects of mussel densities on growth, time
to reaching market size and production.
The experiment was initiated using 10 hung
spatted ropes each for the NS and S treatments in
the submerged longline system (Fig. 2). From May
2009 to May 2010, the system was balanced and
checked every couple of weeks. Additional flotation
was added to the mainline for maintaining balance
of longline system to offset the growing mussels.
Temperature, salinity, chlorophyll a (ch-a), total
suspended matter (TSM), organic matter (OM) and
inorganic matter (IM) were measured monthly
during the experimental period. Seawater samples
were taken from a 13 m depth using a Nansen
bottle at the experimental site, and water tempera-
ture and salinity were measured using a probe
(6600 V2 Sonde manufactured by YSI). The water
samples were transferred to a laboratory, and trip-
licate water samples (3 L) were filtered onto What-
man GF/C filters to determine chlorophyll a (ch-a)
(lg L1), total suspended matter (TSM) (mg L1),
organic matter (OM) (mg L1) and inorganic
matter (IM) (mg L1) concentration according to
the method described by Stirling (1985).
The determination of growth and loss rate and
production
Monthly triplicate mussel samples were taken by
divers grazing S and NS mussels that were at least
30 cm in length. The mussels were transferred to
the laboratory and into a 50-L tank filled with sea
water. After cleaning the mussels to ensure no
1372
Aquaculture Research, 2015, 46, 1369–1383
contamination from fouling organisms, the samples
were counted to determine densities (ind.m1).
Monthly losses were determined according to the
following equation:
Losses ð%Þ ¼ ðNt =N0 Þ  100
where Nt is the number of mussels remaining after
time t, and N0 is the number of mussels at the
beginning of the time period.
Subsamples were taken from the main samples for
biometric measurements. The individual mussel
weight and length of 150–200 mussels were mea-
sured for each treatment type, and the growth rate
was estimated from changes in shell length. Live
weight (total weight of mussel) was obtained by blot-
ting animals with tissue paper and weighing to the
nearest 0.001 g. Shell length (maximum anterior–
posterior axis) was measured to the nearest 0.1 mm
with a calliper (Seed 1969).The monthly specific
growth rate (SGR%) was found by following formula:
SGR ð%Þ ¼ ½ðln L2  L1 Þ=ðT2  T1 Þ  100
where L1 and L2 are the mean shell lengths at
times T1 and T2 (Chatterji, Ansari, Ingole &
Parulekar 1984).
At the end of the study, the production was esti-
mated using the following formula:
Production ¼ N  W
where N is the number of mussels per m at t time and
W is the mean live weight (g) at t time (Crisp 1984).
The determination of meat yield and condition
index
Monthly during the study, 30 individuals were
randomly subsampled into mussel samples compris-
ing a combination of the counted S and NS mussels.
To determine the condition indices, the volume of
three groups of 10 mussels was determined using
100- and 500-mL measuring cylinders (Lutz 1980).
The mussels were opened and blotted with tissue
paper, and then put into a measuring cylinder, and
their volume was measured by direct water
displacement. The shell volume was estimated in
the same manner. The shell cavity volume was
estimated from the difference between the whole
animal volume and the shell volume. The wet meat
condition index (CIV) was assessed by measuring
the volume of the shell cavity and the volume of
meat. The dry weight condition index (CID) was
© 2013 John Wiley & Sons Ltd, Aquaculture Research, 46, 1369–1383
Aquaculture Research, 2015, 46, 1369–1383
calculated after drying the wet meat using the
following equations (Lutz 1980):
Shell cavity = Total volume  shell volume,
wet meat condition index
= [volume of soft tissue (mL)/
volume of shell cavity (mL)] 9 100
and
Dry weight condition index = [weight of dry tissue
(g)/volume of shell
cavity (mL)] 9 100.
Meat yield (MY) was estimated using the following
formula:
Meat yield (%) = [wet meat weight (g)/
total weight (g)] 9 100.
Biochemical composition
The soft tissues were dried at 105°C for 20 h to
obtain their dry weight and moisture content. Dried
meat samples were used for protein and lipid analy-
ses (AOAC 1990). Ash weight was determined by
combusting a known dry weight of tissue at 500°C
for 15 h in a muffle furnace and reweighing.
The following formula was used for determining
carbohydrate content: Carbohydrate (%) = 100 
[lipid (%) + protein (%) + ash (%)].
Statistical analyses
At the end of the study, all data percentages were
transformed by arcsine transformation prior to the
ANOVA and reversed afterwards because all data
percentage should be transformed to arcsine data
before statistical analyses (Zar 1984). The varia-
tions were analysed using one-way ANOVA followed
by a Tukey tests for means comparison. A correla-
tion matrix was used to determine the relation-
ships between the environmental factors and
growth parameters. The statistical analysis was
conducting using MINITAB 13A software.
Results
Durability of submerged longline system
The design of the submerged longline system did
not cause any problem for mussel culture activity
© 2013 John Wiley & Sons Ltd, Aquaculture Research, 46, 1369–1383
Offshore mussel culture in the Black Sea region S Karay€
ucel et al.
despite facing the harsh conditions of the Black
Sea because of the appropriate buoys, anchors and
other materials used in the strong installation of
the system. There were no abrasions or punctures
on the buoys, but there was seaweed settlement at
the bottom of the buoys; however, seaweed clean-
ing did not cause any reduction in buoyant force.
Thinning of the 32-mm-diameter polypropylene
rope of the mainline was observed towards the
end of the study. In addition, the 32-mm-diameter
polypropylene rope of the mooring system without
a chain detached from the anchor connection,
producing friction as a result of abrasion.
The plug anchors were evaluated in terms of
interoperability; observations made a month after
system installation indicated that the anchors were
well seated into the seabed because of the mud
structure. This seating prevented slippage of the
longline system. The culture system established in
an area of heavy vessel traffic produced no inter-
ference with shipping, and did not prevent any
tourism activity or cause any visual pollution due
to its submerged design.
Environmental parameters
The recorded monthly environmental parameters
are shown in Fig. 3. The monthly seawater tem-
perature varied from 7.83°C in March to 23.34°C
in July with a mean of 15.47
1.57°C during
the study. Salinity ranged from 17.30 psu in
February to 18 psu in May 2010 with a mean of
17.68
0.50 psu, and there was not a clear
seasonal pattern.
The minimum TSM concentration was 7.38 mg L1
in May 2009, and the maximum value was
13.93 mg L1 (November). The minimum OM value
was 2.93 mg L1 in March, and the maximum value
was 5.77 mg L1 in July. IM ranged from
3.25 mg L1 in May 2009 to 8.50 mg L1 with a
mean of 6.95
0.37 mg L1. Ch-a varied between
0.8 lg L1 (June and October) and 4.14 lg L1
(February).
There was a significant positive relationship
between TSM and OM and IM (P ≤ 0.01). The
ch-a level did not display significant seasonal
changes (P ≤ 0.05). A peak in ch-a was observed in
February (4.14 lg L1), and ch-a decreased to its
lowest value in June and October (0.80 lg L1),
with a mean of 1.72
0.25 lg L1. There was
no correlation between ch-a and OM or TSM
(P > 0.05).
1373
Offshore mussel culture in the Black Sea region S Karay€ucel et al. Aquaculture Research, 2015, 46, 1369–1383

Temperature Salinity
(a)
25 18
Temperature (°C)

Salinity (psu)
20 17.5

15 17

10 16.5

5 16
M J J A S O N D J F M A M

(b) OM IM TSM
OM and IM (mgL–1)

10 14

TSM (mgL–1)
8 12
6
10
4
8
2
0 6
M J J A S O N D J F M A M

(c)
Chlorophyll-a (µgL–1)

5
4
3
2
Figure 3 Monthly distribution of
1 mean temperature, salinity (a),
0 OM: organic matter, IM: inorganic
M J J A S O N D J F M A M matter, TSM: total suspended mat-
Months ter (b) and chlorophyll a (c).

Growth and density Losses and production

At the end of the study, the mean shell length and Monthly losses were computed as changes in pop-
live weight were 60.40
0.60 mm and 20.50
ulation density (expressed as the mean number of
0.50 g for S treatment and 53.31
0.37 mm mussels per metre of rope). Monthly losses ranged
and 13.11
0.26 g for the NS treatment. The from 0.23% (August) to 7.62% (October) for S mus-
mean monthly SGR% of the S and NS treatment sels and 0.24% (April and May 2010) to 19.23%
was 3.62
0.88% and 2.85
0.69% respec- (October) for NS mussels. The cumulative losses of
tively (Fig. 4). In addition, TSM had a positive cor- the initial number of mussels were 36.56% for S
relation with the growth rate of mussels (SGR%) mussels and 89.10% for NS mussels (Fig. 6).
for both the S and NS culture treatment types The production and marketable yield (kg m1)
(P < 0.05). for S and NS mussels is given in Table 1. There
Length frequencies of S and NS mussels for May was a considerable difference in production
(2009) (a), September (b), January (c) and May between the two culture-type rope groups. At the
2010 (d) are shown in Fig. 5. end of the study, the average production per metre
The monthly mussel densities for the S and NS for the S and NS mussels was 6.58

mussels were 467.67
16.67 and 2116.67
0.25 kg m1 and 10.59
0.36 kg m1 respec-
44.10 ind.m1 at the beginning of the study, tively. Furthermore, when the mussels reached
respectively, and 321
25.13 and 808.33
marketable size and production was considered,
52.39 ind.m1 at the end of the study respectively. the S mussels had a more marketable yield than
Mussel densities decreased depending on winds and NS mussels at the end of the study. The data were
natural death towards the end of the experiment. analysed from the perspective of reaching harvest

1374 © 2013 John Wiley & Sons Ltd, Aquaculture Research, 46, 1369–1383
Aquaculture Research, 2015, 46, 1369–1383 Offshore mussel culture in the Black Sea region S Karay€
ucel et al.

(a) 62 NS type S type

Shell length (mm)

58
54
50
46
42
38
M J J A S O N D J F M A M

(b) 23
20

Live weight (g)

17
14
11
8
5
M J J A S O N D J F M A M

(c) 12
10
SGR (%)

8
6
4
Figure 4 Monthly mean shell 2
length (a), live weight (b) and 0
SGR: specific growth rate (c) of S J J A S O N D J F M A M
and NS mussels. Month

time. The S mussels reached market size
(53.78
0.81 mm) in November 2009
(19 months), whereas the NS mussels reached
market size (51.03
0.73 mm) in February 2010
(22 months).
Meat yield and condition indices
CIV and CID ranged from 25.23% (May 2009) to
37.33% (March) with a mean of 29.17
0.86%
and 4.50% (April) to 5.71% (August) with a mean
of 4.95
0.08% respectively (Fig. 7). Meat yield
varied between 19.79 (May 2010) and 29.04%
(March) with a mean of 23.61
0.76%. Meat
yield positively correlated with CIV (P < 0.01).
Biochemical composition
The composition of the meat was expressed as the
percentage of proteins, lipids, carbohydrates and
ash of the dry weight of the mussel meat. The
monthly mussel values of lipids, proteins, carbohy-
drates, ash and moisture ranged from 2.85 (April)
to 10.73% (October), 46.51 (July) to 69.42%
(January), 14.97 (January) to 40.36% (July), 4.51
(July) to 8.72% (February) and 78.60 (August) to
84.4% (January) respectively (Fig. 8).
A significant negative relationship was observed
between OM and ash (%) (P < 0.001). There was
also a strong positive relationship between lipids,
temperature and OM (%) (P < 0.01). In addition,
the statistical analyses indicated that protein level
was negatively correlated with the carbohydrate
level (P > 0.05).
Discussion
Submersible longline system
Offshore aquaculture system equipment must be
strong, lightweight, abrasion resistant, inexpen-
sive, easy to work on, durable against fouling and
environmental effects and easily repaired for use in
offshore farming activities (Stevens et al. 2008). In
this study, the polypropylene ropes were selected
because of high durability against any impact and
low cost. In addition, several studies have reported
that polypropylene is the most common rope

© 2013 John Wiley & Sons Ltd, Aquaculture Research, 46, 1369–1383 1375
Offshore mussel culture in the Black Sea region S Karay€ucel et al. Aquaculture Research, 2015, 46, 1369–1383

(a)
40
Frequency (%)

35 NS type S type
30
25
20
15
10
5
0
29–32

33–36

37–40

41–44

45–48

49–52

53–56

57–60
(b)
35
Frequency (%)

30
25
20
15
10
5
0
38–41

42–45

46–49

50–53

54–57

58–61

62–65
(c)
30
Frequency (%)

25
20
15
10
5
0
40–43

44–47

48–51

52–55

56–59

60–63

64–67

68–71

(d)
Frequency (%)

30
25
20
15
10
5
0 Figure 5 Length frequencies of
40–43

44–47

48–51

52–55

56–59

60–63

64–67

68–71

72–75

76–79

mussels for NS and S mussels; May

(2009) (a), September (b), January
Shell length (mm) (c) and May 2010 (d).

(a) 35
30 NS type S type
Losses (%)

25
20
15
10
5
0
J J A S O N D J F M A M

(b)
Cumulative losses (%)

100

75

50

25

0 Figure 6 Monthly changes in

J J A S O N D J F M A M losses (a) and cumulative losses (b)
Months for NS and S mussels.

1376 © 2013 John Wiley & Sons Ltd, Aquaculture Research, 46, 1369–1383
Aquaculture Research, 2015, 46, 1369–1383
Table 1 Production and marketable yield (kg m1) for S and NS mussels
Culture Production
types (kg m1) Marketable (%)
NS 10.59
0.43 73.52
0.78
S 6.58
0.28 79.89
0.99
40
CIV and MY (%)
35
30
25
20
Figure 7 Monthly mean wet meat
condition index (CIV), dry weight 15
condition index (CID) and meat M J
yield (MY).
material used in open-sea mussel cultivation, and
these data increased our confidence in the material
used (Danioux et al. 1997; Buck 2007b). Towards
the end of our experiment, we observed that the
polypropylene rope, used as mainline, was thinner.
In addition, the anchor rope without chain chafed
within the inner parts of the eye loops and broke off
from the connection two times. A problem formed
as a result: the ropes of the system moved up and
down, and the chainless anchoring system did not
provide the needed flexibility. However, the longline
system tolerated this challenge due to strong instal-
lation. In light of these problems, the anchor line
should be 45–50 mm in diameter, and all anchors
of the longline should have a chain to provide flexi-
bility to the anchorage system. These findings are
similar to a study by Paul and Grosenbaugh
(2000). Many studies have suggested the use of the
plug anchor, and it is the most common anchor
type used in mud-bottom structures and open-sea
aquaculture facilities (Danioux et al. 1997; Stevens
et al. 2008). A better understanding of the problems
and more sophisticated analysis largely reduced the
risks. The encountered problems were solved in a
timely manner with controls and precautions. The
overall evaluation of the performance of this Black
Sea system found no serious problem.
The effects of density on growth, production and
time to reach market size
Several studies have shown that the survival and
growth of mussels are affected by temperature,
© 2013 John Wiley & Sons Ltd, Aquaculture Research, 46, 1369–1383
Offshore mussel culture in the Black Sea region S Karay€
ucel et al.
Marketable Total marketable Time to reach
yield (kg m1) yield (kg m1) market size (months)
7.78
0.21 7.78 22
5.25
0.14 15.75 18
CIV MY CID 6
5.5
CID (%)
5
4.5
4
J A S O N D J F M A M
Month
salinity, total suspended matter (TSM), inorganic
matter (IM) and organic matter (OM) (Dickie et al.
1984; Jones & Iwama 1991; Karay€ ucel & Karay€ucel
1999, 2001; Manoj Nair & Appukuttan 2003; Ren
& Ross 2005). These findings are supported by our
study. The mussel SGR in both culture types was
generally high when the temperature was high in
the summer and spring compared with the winter
months. Moreover, because the culture site was
10 m below the sea surface, the mussels might not
have been affected by the extreme temperature.
Therefore, this condition could have positive effects
on mussel growth rate. In the study area, the
mixing of sediment could have also caused major
effects on water turbidity due to the structure of this
study area (strong current, wave and winds). These
findings are similar to some studies that indicate
that OM depends on the availability of detritus
from sediment, not from phytoplankton avail-
ability (Resgalla, Brasil, Laitano & Reis Filho 2007;
Schmidt, Gonzalez, Lecroart, Tronczy~ nski, Billy &
Jouanneau 2007). This may explain the positive
relationship between OM and TSM. Ren (2009)
indicated that the presence of high OM in TSM
increased the nutritional quality of the seawater.
This study demonstrated that nutritional elements
in the seawater varied according to bottom cur-
rents, storms, seasons and the structure of the
region. The SGR of the S and NS mussels were also
positively related to TSM. The growth rates
decreased when TSM and OM were low quantity.
The benthic and pelagic particles that originated
from the sediment are an important nutritional
1377
Offshore mussel culture in the Black Sea region S Karay€ucel et al. Aquaculture Research, 2015, 46, 1369–1383

Moisture Ash
(a) 85 9
84
83 8
Moisture (%)

82

Ash (%)
81 7
80
79 6
78
77 5
76
75 4
M J J A S O N D J F M A M

(b)
Protein Carbonhydrate
Protein and carbonhydrate (%)

70
60
50
40
30
20
10
M J J A S O N D J F M A M

(c) 12
10
Lipid (%)

4
Figure 8 Monthly variation in
2 mean moisture and ash (a), pro-
M J J A S O N D J F M A M teins, carbohydrates (b) and lipid
Month (c).

source for mussels according to Mach as, Santos and
Peterson (2003). Our study findings were similar.
The weak positive correlation found between ch-a
and SGR for S and NS mussels resulted from a ch-a
concentration (0.8 and 2.67 lg L1) that varied to
a greater extent in the region. This result explained
that lack of relationship between ch-a and mussel
SGR, and temperature and TSM. The same situation
is found in Fangar Bay in Spain, where any correla-
tion found between the increase in shell length and
ch-a, temperature or seston is most likely due to the
wide ranges of the environmental parameters
throughout the growth cycle of the mussels (M. gal-
loprovincialis) (Ramon, Fern andez & Galimany
2007). However, our findings are different from
many studies that state that a high level of ch-a is
associated with increased mussel growth (Babarro,
Fernandez-Reiriz & Labarta 2000; Karay€ ß elik,
ucel, C
Karay€ ucel & Erik 2010).
In this study, the mussel density affected the
mussel growth and loss rate. The mussel density
for the NS mussels significantly decreased because
of high density, currents and waves towards the
end of the experiment. The loss rate for the NS
mussels between August and November was signif-
icantly higher, which could be the result of stress
related to spawning, recruitment and high densi-
ties. The differences in loss rates could depend on
high density because high density can lead to mus-
sels being dislodged from ropes and subsequent
loss. The mussels exhibited density-dependent mor-
tality and fall-off (Lauzon-Guay, Dionne Barbeau &
Hamilton 2005). Frechette and Desplan (1999)
revealed that there is a strong effect of density;
larger mussels can put pressure on smaller mussels
for food and space, and thus, smaller mussels are
more likely to dislodge. Those findings are supported
by the results of this study. The loss rate of the

1378 © 2013 John Wiley & Sons Ltd, Aquaculture Research, 46, 1369–1383
Aquaculture Research, 2015, 46, 1369–1383
mussels on the high-density rope was higher than
the loss rate associated with the lower density
rope. In addition, the negative effect of stocking
density on mussel growth was demonstrated. The
growth rate of S mussels was higher than NS mus-
sels because an increase in mussel density greatly
reduced the growth rate. Competition for food
and/or space is the likely reason for slower shell
growth. Several studies have also found a negative
relationship between growth rate and density
(Fuentes, Gregorio, Giraldez & Molares 2000;
Gosling 2003). According to Alfaro (2006), mus-
sels subjected to high-density growth compete with
each other for space and food, so the survival and
feeding rate of these mussels necessarily decreases.
There was a strong relationship between the time
to reach market size and mussel density. Cultured
mussels growing in lower density conditions pre-
sented superior growth due to less competition for
food resources (Comeau et al. 2008). Higher pro-
duction was obtained from S mussel culture ropes.
These results indicate that the thinning out of
stocks is extremely important for maximizing
growth. Thus, we can conclude that thinning out is
an important factor for achieving marketable yields
(Table 1). McMillan (1990) also reported that resoc-
king of mussels can effectively double the market-
able yield of mussels on culture ropes.
The time to reach market size (>50 mm) varied
according to mussel density on the culture ropes
in this study. The socking operation increased the
harvested number of mussels and reduced the time
to harvest. In conclusion, cultured mussel biomass
density was an important factor affecting the
increase in production and harvest time. In many
studies, the time to reach market size and produc-
tion vary by region. Others studies, made in the
coastal areas of the same region as our study,
have indicated that the period of mussel cultiva-
tion from spat settlement to harvest time was
2 years (Karay€ ucel, Karay€ ucel, Erdem, Saygun &
Uyan 2003; Karay€ ucel et al. 2010). In addition,
Karay€ ucel et al. (2010) obtained 250 ind.m1
(>55 mm) and Karay€ ucel et al. (2003) achieved
211 ind.m1 (>47 mm) in cotton socks and 532
ind.m1 in nylon socks. Langan and Horton
(2003) reported that stock density affects produc-
tion and the reaching of mussel market size. Other
studies have demonstrated that the mussel produc-
tion cycle varies according to the geographical
condition and harvest size. In other studies, the
time to reach harvest size (>50 mm) was 1.5–2
© 2013 John Wiley & Sons Ltd, Aquaculture Research, 46, 1369–1383
Offshore mussel culture in the Black Sea region S Karay€
ucel et al.

years in Croatia (Benovic 1997; Peharda, Zupan,
Bavcevic, Frankic & Klanjscek 2007), 2.5–3 years
in Scotland (Karay€ ucel 1997) and 1.5–2 years in
Canada (Drapeau, Comeau, Landry, Stryhn &
Davidson 2006).
Meat yield and condition indices
The meat yield was strongly related to tempera-
ture and OM (P < 0.05) and mussel spawning
occurred when the water temperature increased
from 7.83 (March) to 9.12°C (April). The second
spawning time of mussels also occurred in October.
Similarly, Lemaire, Pelerin, Fournier, Girault, Tam-
igneaux, Cartier and Pelletier (2006) found that
water temperature and food supply significantly
influenced mussel spawning time. Many studies
have also reported parallel results (Kautsky 1982;
Thompson 1984; Karay€ ucel et al. 2003; Cartier,
Pellerin, Fournier, Tamigneaux, Girault & Lemaire
2004). In this study, a higher mussel meat yield
(29.4%) and condition index (37.33%) were
recorded during the period (March) immediately
before spawning. The sudden drop in the condition
index and meat yield was identified in the spawn-
ing period (April 2010). Mussels increased the
meat yield and condition index after the spawning.
Thus, these findings indicate that the condition
index and meat yield of mussels were influenced
by internal and external factors such as tempera-
ture, salinity, food supply and reproduction period.
The meat yield of mussels increased twofold when
the amount of food in the seawater increased
during the spring months (Strohmeir, Duinker,
Strand & Aure 2008). Okumus and Stirling (1998)
reported that the meat yield and condition index
decrease depending on the gamete releases. Other
studies have shown that condition index and
meat yield vary according to environmental factors
and the reproduction period of mussels (Rajagopal,
Venugopalan, Nair, Van der Velde & Jenner 1998;
Orban et al. 2002; Lachowicz 2005).
The meat yield of cultured mussels in the off-
shore area varied between 19.79% and 29.04% in
this study. On the other hand, the meat yield of
natural mussels at the same time and same region
varied between 14.34% and 21.92% (C ß ulha &
T€ ß ulha 2010). The results of this study are in
urk C
agreement with many other studies. Babarro et al.
(2000) declared that the meat yield of collected
natural mussels was lower than cultured mussels
because of the necessity of having to build a
1379
Offshore mussel culture in the Black Sea region S Karay€ucel et al.
thicker shell to protect themselves from strong
waves. In another study, the meat yield of cul-
tured mussel from a longline system in the open
sea was higher than the yield of collected natural
mussels (Brenner 2009).
Harvest time is determined by taking into con-
sideration the condition index wet meat volume
(CIV) and meat yield of mussels for the different
regions (Zandee, Kluitmans, Zurburg & Pieters
1980; Kopp, Cornette & Simonne 2005; Peharda
et al. 2007). In our study, the CIV of the mussels
ranged between 27.65% and 37.33% throughout
the year. Therefore, the results of this study indi-
cate that mussels should be harvested in May
(25.23%) and June (25.79%), which are spawning
months. However, with regards to studies in the
same region, Karay€ ucel et al. (2003) suggested a
5-month harvesting period between January and
June, and C ß elik, Karayucel, Karay€ € urk and
ucel, Ozt€
Ey€uboglu (2012) reported that February and May,
when CIV was nearly 30%, were suitable for the
harvest. These differences in the same region in
harvest time are due to the relatively constant
condition of the offshore sites, which results in a
less variable mussel condition and annual envi-
ronmental conditions.
Biochemical composition
This study demonstrated that protein, lipid, carbo-
hydrate, ash and moisture values varied depending
on food supply and reproduction period. The con-
dition index reached its highest value in March,
and the lipid and protein values were at their
maximum in January. The lipid and protein values
decreased because of spawning.
In our study, the lipid and carbohydrate values
were at their highest level when OM was higher
in the spring and summer months. The mussels
required too much energy for egg maturation,
and accordingly, their metabolic energy reserves
could be affected by this energy requirement.
Thus, carbohydrate reserves were reduced due to
being used as energy for fat synthesis. Protein
and lipid levels continued to increase until
spawning. Carbohydrate and lipid reserves could
be used as an energy source during periods of
lower available nutrition. This finding is in agree-
ment with Lachowicz (2005). Protein levels
markedly decreased, but the amount of carbohy-
drate increased with spawning. These results indi-
cate that protein and carbohydrate reserves were
1380
Aquaculture Research, 2015, 46, 1369–1383
not used for the same purpose. Similar results
were reported by Karay€ ucel (1997) and Freites,
Fernandez-Reiriz and Labarta (2003). The lipid
value began to increase the month following
spawning (April). This result indicates that lipid
concentration decreased with spawning and
increased again with gonadal maturation. Our
study results suggest that lipids were an energy
source used for gonad maturation, and these find-
ings are in agreement with several other studies.
The biochemical composition cycles of mussels
indicated annual patterns of accumulation and
the use of reserves due to a complex interaction
among food availability, growth and reproduction
(Narvaez, Freites, Guevara, Mendoza, Guderley,
Lodeiros & Salazar 2008). Seasonal variations in
the biochemical composition of Mytilus edulis has
been related to energy metabolism and gameto-
genesis (Zandee et al. 1980; Karay€ ucel et al.
2002). Lachowicz (2005) reported that high lev-
els of glycogen and protein are rebuilt after
spawning, but lipid concentrations remain low
and recover slowly, as glycogen is deposited in
the mantle tissue in months when plenty of food
is available. During the reproduction phase, how-
ever, mussels heavily utilize their reserves to meet
the energetic requirements of gametogenesis and
spawning (Dridi et al. 2007; Serdar & L€ ok 2009).
Protein is the most abundant biochemical compo-
nent in mussel tissue and, if needed, protein can
be used as an alternative energy source for gonad
formation (Galap, Leboulenger & Grillot 1997).
Conclusion
Our findings indicate that a submerged longline
mussel culture system works with no serious prob-
lem in accordance with the open-sea conditions of
the Black Sea. Mussels cultivated in the submerged
offshore system presented good growth because
they were away from stresses such as strong wind,
waves, current and sudden changes in hydrological
conditions. Furthermore, stock management
through thinning out of the spat can considerably
increase the marketable size of mussels, reduce har-
vest time and facilitate better growth.
Acknowledgment
We thank The Scientific and Technological Research
Council of Turkey (TUBITAK) for providing financial
support.
© 2013 John Wiley & Sons Ltd, Aquaculture Research, 46, 1369–1383
Aquaculture Research, 2015, 46, 1369–1383 Offshore mussel culture in the Black Sea region S Karay€
ucel et al.

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