Effects of Stocking Density On Survival, Growth and

Aquaculture Research, 2015, 46, 1369–1383 doi:10.1111/are.
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 € urk1 &
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: [email protected]
Abstract Introduction
This study examined an offshore submerged mus- United Nations Food and Agricultural Organiza-
sel longline system, in the Black Sea, from May tion (FAO) statistics indicates that mussels are one
2009 to May 2010. The system was allowed of the most popular cultured species. The culturing
1 year for spat collection. After a 1-year spat col- of mussels has increased from 1307 thousand
lection period, some spat collectors were left tonnes to 1812 thousand tonnes in the last few
untouched (NS), and some spat collectors were decades (FAO/Fishstat Plus 2012).
grazed and socked (S) for a grow-out study in May For a long time, mussel farms have been limited
2009. The effects of stocking density on the to sheltered coastal lagoons (Burbridge, Hendrick,
growth and survival of the S and NS mussels were Roth & Rosenthal 2001). According to Danioux,
examined. The biochemical composition of the mus- Loste and Paquotte (1997), coastal lagoons have
sels was also determined. Environmental factors rich and easily accessible but fragile environments
including temperature, salinity, chlorophyll a, total that have been exploited to their maximum spatial
suspended matter, inorganic matter and organic and biological capacity. These researchers have
matter were monitored monthly during the experi- also stated that several risk factors, at times simul-
mental period. In May 2010, the mean length and taneously, have limited the expansion of the
live weight of the S and NS mussels were mussel farming activity in the restricted lagoon
60.46 0.60 mm and 53.34 0.37 mm, respec- environment: (i) the necessary intensification of
tively, and 20.50 0.50 g and 13.11 0.26 g production to reduce production costs; (ii) pollu-
respectively. Mean moisture and ash were 82.35 tion from industrial and domestic sources, which
0.47% and 6.67 0.44% respectively. Mean car- produces high mortality at times and (iii) the
bohydrate, protein and lipid were 27.74 2.40%, limited renewal of the environment due to a lack
57.68 2.15% and 7.91 0.68% respectively. of strong tides, which brings with it a dystrophic
These results indicate that a submerged offshore crisis and anoxia risk. Inshore sites have also
mussel culture system in the Black Sea can be proven to have lower growth and higher disease
commercially convenient. In addition, stock man- rates, with greater risks of contamination from
agement via thinning out of the spat can consider- overuse and other activities. Due to these chal-
ably increase the marketable size of mussels, lenges, to date, the mussel production achieved
reduce harvest time and produce better growth. has not increased enough to meet demand. As a
result, offshore mussel culture has been suggested
Keywords: Mussel, offshore, density, growth, as a solution to meet the growing demand
survival, biochemical (Langan 2008).
© 2013 John Wiley & Sons Ltd 1369

Offshore mussel culture in the Black Sea region S Karay€ucel et al. Aquaculture Research, 2015, 46, 1369–1383
Currently, technological developments in the Dilena, Nevigato, Casini, Marzetti & Caproni 2002).
aquaculture sector have made it possible to estab- In general, when food is abundant, reserves
lish open-sea mussel culture systems. The offshore accumulate prior to gametogenesis in the form of
systems available for aquaculture have been glycogen, lipid and protein. These reserves are sub-
designed through the modification in coastal struc- sequently utilized in the production of gametes
tures or techniques such as longlines or rafts when metabolic demand is high (Dridi, Romdhane
(Stevens, Plew, Hartstein & Fredriksson 2008). & Elcafsi 2007; Serdar & L€ok 2009).
Many studies have determined that the most con- In Turkey, mussel (Mytilus galloprovincialis) is
venient offshore system would be longline systems the only shellfish species cultured in coastal areas
(Danioux et al. 1997; Langan & Horton 2003; Buck and cultivation was only 87 tonnes per year in
2007a; Brenner 2009). In addition, the growth 2009 (FAO/Fishstat Plus 2012). There are no
rate of mussels has been reported to be better studies available for offshore submerged design to
using longline systems because mussels on the serve as models for entrepreneurs interested in
longline are fully suspended in the water and, mussel longline cultivation, and no data are avail-
therefore, flushed by phytoplankton-rich sea water able on the condition index and biochemical com-
(Buck 2007a). position of mussels harvested from offshore sites in
The survival and growth rates of mussels is the Mediterranean, Black and Aegean seas. This is
directly related to environmental conditions the first experiment in Turkish waters where a
included temperature, salinity, total particulate submerged longline design was installed to resist
matter, organic matter, inorganic matter and chlo- offshore site conditions, evaluate system strength
rophyll a of the seawater they are growing in and focus on site selection criteria. Furthermore,
(Dickie, Boudreau & Freeman 1984; Jones & mussel growth and production were evaluated
Iwama 1991; Karay€ ucel & Karay€ucel 1999, 2001; from thinning out to harvest in a longline system,
Manoj Nair & Appukuttan 2003; Ren & Ross in both socked rope-type and untouched rope-type
2005). In addition, many studies have stated collectors in open-sea conditions. The biochemical
that mussel density negatively affects feeding and content (protein, lipid, carbohydrate, ash and dry
loss rate because of increasing competition for matter levels) and condition index of the cultivated
food and space (Alfaro 2006). Comeau, Drapeau, mussels from the offshore submerged longline
Landry and Davidson (2008) reported that there system were investigated.
was a strong relationship between the time to
reach market size and mussel density, and culti-
Materials and methods
vated mussels grow better because of better feed-
ing. However, some authors have reported that
Study area and construction of the submerged
offshore farms allow higher growth rates, better
longline system
meat yield and heavier production compared with
inshore farms due to lower stress, reduced turbid- The study was carried in Sinop at a depth 25–27 m
ity and better water exchange (Langan & Horton at an offshore site in the Black Sea region between
2003; Brenner 2009). May 2009 and May 2010 (Fig. 1). This area was
In addition to aiding in assuring healthy food chosen due to harsh weather conditions, and a
and safe consumption, the quality of mussel meat longline system was designed according to site
mainly depends on the quality of the aquatic envi- conditions.
ronment (Karakoltsidis, Zotos & Constantinides The system was established at 10 m below the
1995). The nutritional and commercial value of water surface to maintain the system despite strong
mussels is determined according to their moisture, currents and waves. The 50-m-long mainline and
protein level, lipid level, carbohydrate level and con- the anchor lines of the system comprised 32-mm-
dition index. Knowledge of the mussel reproductive diameter polypropylene rope. In addition, 330-L
period and biochemical composition is very impor- surface buoys were manufactured from superior
tant for successful mussel cultivation. Seasonal quality high-density polyethylene (HDPE), filled
biochemical composition is related to water temper- with polyurethane foam and had dipped galvanized
ature, food availability, gonadal maturation and steel construction. The buoys were then fixed with
spawning (Okumus & Stirling 1998; Karay€ ucel, a chain (15 mm in diameter) at each end and the
Erdem, Uyan, Saygun & Karay€ ucel 2002; Orban, middle of the mainline. Thirty L marker buoys
1370 © 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.
were used on the edges of the experimental area to connected using omega shackles, galvanized thim-
mark and protect the site for navigation purposes. bles and swivels. The longline system had a strong
The longline was fixed with four plug anchors configuration to resist all harsh weather condi-
(250 kg), and a 50-kg concrete block also placed tions. Furthermore, two flashing lights with a
in the middle of the longline system. These anchor waterproof body were placed on buoys (330 L) at
types were selected for the use on the muddy sea each end of the mainline for marking purposes and
bottom for long-term durability. Two plug anchors, to establish the edges of the experiment area to
which were vertically below the mainline, were mark and also protect the site for navigation
tied without chain, and another two, which were (Fig. 2). After installation of the system was
below the marker buoys, were connected with completed, polypropylene experimental ropes were
chain (38 mm in diameter and 7 m in length) to hung to the longline system. To prevent the
the anchor line to provide flexibility to the mooring collapse of the mainline due to growth of mussels,
system of the longline. All connection points were 20-L floats were tied to the mainline.
Figure 1 The study area.
Figure 2 Design of the submerged

longline system.
© 2013 John Wiley & Sons Ltd, Aquaculture Research, 46, 1369–1383 1371
contamination from fouling organisms, the samples

Experimental design and sampling procedure
were counted to determine densities (ind.m1).
The system was allowed 1 year for spat collection. Monthly losses were determined according to the
After the 1-year spat collection, some of the spat following equation:
collectors were left untouched, and some spat col-
Losses ð%Þ ¼ ðNt =N0 Þ 100
lectors were grazed and socked for a grow-out
study. The average density was 2116.67 44.10 where Nt is the number of mussels remaining after
individuals m1 (ind.m1) with a mean length of time t, and N0 is the number of mussels at the
39.21 0.67 mm and mean weight of 5.57 beginning of the time period.
0.23 g for the untouched, and the average density Subsamples were taken from the main samples for
was 467.33 19.77 ind.m1 with a mean length biometric measurements. The individual mussel
of 40.90 0.23 mm and mean weight of 6.52 weight and length of 150–200 mussels were mea-
0.08 g for socked mussels respectively. The small sured for each treatment type, and the growth rate
spats dropped through a mesh (sock had an 11 cm was estimated from changes in shell length. Live
width and a 4 cm mesh size) during sock filling. weight (total weight of mussel) was obtained by blot-
Approximately one spat collector had enough mus- ting animals with tissue paper and weighing to the
sels to fill three socks for grow-out. These were used nearest 0.001 g. Shell length (maximum anterior–
to compare two different treatments, thinned out posterior axis) was measured to the nearest 0.1 mm
(S type) and without thinning out (NS type), to eval- with a calliper (Seed 1969).The monthly specific
uate the effects of mussel densities on growth, time growth rate (SGR%) was found by following formula:
to reaching market size and production.
The experiment was initiated using 10 hung SGR ð%Þ ¼ ½ðln L2 L1 Þ=ðT2 T1 Þ 100
spatted ropes each for the NS and S treatments in
where L1 and L2 are the mean shell lengths at
the submerged longline system (Fig. 2). From May
times T1 and T2 (Chatterji, Ansari, Ingole &
2009 to May 2010, the system was balanced and
Parulekar 1984).
checked every couple of weeks. Additional flotation
At the end of the study, the production was esti-
was added to the mainline for maintaining balance
mated using the following formula:
of longline system to offset the growing mussels.
Temperature, salinity, chlorophyll a (ch-a), total Production ¼ N W
suspended matter (TSM), organic matter (OM) and
inorganic matter (IM) were measured monthly where N is the number of mussels per m at t time and
during the experimental period. Seawater samples W is the mean live weight (g) at t time (Crisp 1984).
were taken from a 13 m depth using a Nansen
bottle at the experimental site, and water tempera-
The determination of meat yield and condition
ture and salinity were measured using a probe
index
(6600 V2 Sonde manufactured by YSI). The water
samples were transferred to a laboratory, and trip- Monthly during the study, 30 individuals were
licate water samples (3 L) were filtered onto What- randomly subsampled into mussel samples compris-
man GF/C filters to determine chlorophyll a (ch-a) ing a combination of the counted S and NS mussels.
(lg L1), total suspended matter (TSM) (mg L1), To determine the condition indices, the volume of
organic matter (OM) (mg L1) and inorganic three groups of 10 mussels was determined using
matter (IM) (mg L1) concentration according to 100- and 500-mL measuring cylinders (Lutz 1980).
the method described by Stirling (1985). The mussels were opened and blotted with tissue
paper, and then put into a measuring cylinder, and
their volume was measured by direct water
The determination of growth and loss rate and
displacement. The shell volume was estimated in
production
the same manner. The shell cavity volume was
Monthly triplicate mussel samples were taken by estimated from the difference between the whole
divers grazing S and NS mussels that were at least animal volume and the shell volume. The wet meat
30 cm in length. The mussels were transferred to condition index (CIV) was assessed by measuring
the laboratory and into a 50-L tank filled with sea the volume of the shell cavity and the volume of
water. After cleaning the mussels to ensure no meat. The dry weight condition index (CID) was
ucel et al.
calculated after drying the wet meat using the despite facing the harsh conditions of the Black
following equations (Lutz 1980): Sea because of the appropriate buoys, anchors and
other materials used in the strong installation of
Shell cavity = Total volume shell volume, the system. There were no abrasions or punctures
wet meat condition index on the buoys, but there was seaweed settlement at
= [volume of soft tissue (mL)/ the bottom of the buoys; however, seaweed clean-
volume of shell cavity (mL)] 9 100 ing did not cause any reduction in buoyant force.
Thinning of the 32-mm-diameter polypropylene
and rope of the mainline was observed towards the
end of the study. In addition, the 32-mm-diameter
Dry weight condition index = [weight of dry tissue polypropylene rope of the mooring system without
(g)/volume of shell a chain detached from the anchor connection,
cavity (mL)] 9 100. producing friction as a result of abrasion.
The plug anchors were evaluated in terms of
Meat yield (MY) was estimated using the following interoperability; observations made a month after
formula: system installation indicated that the anchors were
well seated into the seabed because of the mud
Meat yield (%) = [wet meat weight (g)/ structure. This seating prevented slippage of the
total weight (g)] 9 100. longline system. The culture system established in
an area of heavy vessel traffic produced no inter-
ference with shipping, and did not prevent any
Biochemical composition
tourism activity or cause any visual pollution due
The soft tissues were dried at 105°C for 20 h to to its submerged design.
obtain their dry weight and moisture content. Dried
meat samples were used for protein and lipid analy-
Environmental parameters
ses (AOAC 1990). Ash weight was determined by
combusting a known dry weight of tissue at 500°C The recorded monthly environmental parameters
for 15 h in a muffle furnace and reweighing. are shown in Fig. 3. The monthly seawater tem-
The following formula was used for determining perature varied from 7.83°C in March to 23.34°C
carbohydrate content: Carbohydrate (%) = 100 in July with a mean of 15.47 1.57°C during
[lipid (%) + protein (%) + ash (%)]. 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
Statistical analyses
seasonal pattern.
At the end of the study, all data percentages were The minimum TSM concentration was 7.38 mg L1
transformed by arcsine transformation prior to the in May 2009, and the maximum value was
ANOVA and reversed afterwards because all data 13.93 mg L1 (November). The minimum OM value
percentage should be transformed to arcsine data was 2.93 mg L1 in March, and the maximum value
before statistical analyses (Zar 1984). The varia- was 5.77 mg L1 in July. IM ranged from
tions were analysed using one-way ANOVA followed 3.25 mg L1 in May 2009 to 8.50 mg L1 with a
by a Tukey tests for means comparison. A correla- mean of 6.95 0.37 mg L1. Ch-a varied between
tion matrix was used to determine the relation- 0.8 lg L1 (June and October) and 4.14 lg L1
ships between the environmental factors and (February).
growth parameters. The statistical analysis was There was a significant positive relationship
conducting using MINITAB 13A software. 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
Results
February (4.14 lg L1), and ch-a decreased to its
lowest value in June and October (0.80 lg L1),
Durability of submerged longline system
with a mean of 1.72 0.25 lg L1. There was
The design of the submerged longline system did no correlation between ch-a and OM or TSM
not cause any problem for mussel culture activity (P > 0.05).
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
(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
ucel et al.
(a) 62 NS type S type
Shell length (mm)

58
54
50
46
42
38
(b) 23
20
Live weight (g)

17
14
11
8
5
(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 (January), 14.97 (January) to 40.36% (July), 4.51
(53.78 0.81 mm) in November 2009 (July) to 8.72% (February) and 78.60 (August) to
(19 months), whereas the NS mussels reached 84.4% (January) respectively (Fig. 8).
market size (51.03 0.73 mm) in February 2010 A significant negative relationship was observed
(22 months). between OM and ash (%) (P < 0.001). There was
also a strong positive relationship between lipids,
temperature and OM (%) (P < 0.01). In addition,
Meat yield and condition indices
the statistical analyses indicated that protein level
CIV and CID ranged from 25.23% (May 2009) to was negatively correlated with the carbohydrate
37.33% (March) with a mean of 29.17 0.86% level (P > 0.05).
and 4.50% (April) to 5.71% (August) with a mean
of 4.95 0.08% respectively (Fig. 7). Meat yield
Discussion
varied between 19.79 (May 2010) and 29.04%
(March) with a mean of 23.61 0.76%. Meat
Submersible longline system
yield positively correlated with CIV (P < 0.01).
Offshore aquaculture system equipment must be
strong, lightweight, abrasion resistant, inexpen-
sive, easy to work on, durable against fouling and
The composition of the meat was expressed as the environmental effects and easily repaired for use in
percentage of proteins, lipids, carbohydrates and offshore farming activities (Stevens et al. 2008). In
ash of the dry weight of the mussel meat. The this study, the polypropylene ropes were selected
monthly mussel values of lipids, proteins, carbohy- because of high durability against any impact and
drates, ash and moisture ranged from 2.85 (April) low cost. In addition, several studies have reported
to 10.73% (October), 46.51 (July) to 69.42% that polypropylene is the most common rope
(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.
ucel et al.
Table 1 Production and marketable yield (kg m1) for S and NS mussels
Culture Production Marketable Total marketable Time to reach

types (kg m1) Marketable (%) yield (kg m1) yield (kg m1) market size (months)
NS 10.59 0.43 73.52 0.78 7.78 0.21 7.78 22

S 6.58 0.28 79.89 0.99 5.25 0.14 15.75 18
40 CIV MY CID 6
CIV and MY (%)

35
5.5
CID (%)
30
5
25
4.5
20
Figure 7 Monthly mean wet meat
condition index (CIV), dry weight 15 4
condition index (CID) and meat M J J A S O N D J F M A M
yield (MY). Month
material used in open-sea mussel cultivation, and salinity, total suspended matter (TSM), inorganic
these data increased our confidence in the material matter (IM) and organic matter (OM) (Dickie et al.
used (Danioux et al. 1997; Buck 2007b). Towards 1984; Jones & Iwama 1991; Karay€ ucel & Karay€ucel
the end of our experiment, we observed that the 1999, 2001; Manoj Nair & Appukuttan 2003; Ren
polypropylene rope, used as mainline, was thinner. & Ross 2005). These findings are supported by our
In addition, the anchor rope without chain chafed study. The mussel SGR in both culture types was
within the inner parts of the eye loops and broke off generally high when the temperature was high in
from the connection two times. A problem formed the summer and spring compared with the winter
as a result: the ropes of the system moved up and months. Moreover, because the culture site was
down, and the chainless anchoring system did not 10 m below the sea surface, the mussels might not
provide the needed flexibility. However, the longline have been affected by the extreme temperature.
system tolerated this challenge due to strong instal- Therefore, this condition could have positive effects
lation. In light of these problems, the anchor line on mussel growth rate. In the study area, the
should be 45–50 mm in diameter, and all anchors mixing of sediment could have also caused major
of the longline should have a chain to provide flexi- effects on water turbidity due to the structure of this
bility to the anchorage system. These findings are study area (strong current, wave and winds). These
similar to a study by Paul and Grosenbaugh findings are similar to some studies that indicate
(2000). Many studies have suggested the use of the that OM depends on the availability of detritus
plug anchor, and it is the most common anchor from sediment, not from phytoplankton avail-
type used in mud-bottom structures and open-sea ability (Resgalla, Brasil, Laitano & Reis Filho 2007;
aquaculture facilities (Danioux et al. 1997; Stevens Schmidt, Gonzalez, Lecroart, Tronczy~ nski, Billy &
et al. 2008). A better understanding of the problems Jouanneau 2007). This may explain the positive
and more sophisticated analysis largely reduced the relationship between OM and TSM. Ren (2009)
risks. The encountered problems were solved in a indicated that the presence of high OM in TSM
timely manner with controls and precautions. The increased the nutritional quality of the seawater.
overall evaluation of the performance of this Black This study demonstrated that nutritional elements
Sea system found no serious problem. 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
The effects of density on growth, production and
positively related to TSM. The growth rates
time to reach market size
decreased when TSM and OM were low quantity.
Several studies have shown that the survival and The benthic and pelagic particles that originated
growth of mussels are affected by temperature, from the sediment are an important nutritional
Moisture Ash
(a) 85 9
84
83 8
Moisture (%)
82
Ash (%)
81 7
80
79 6
78
77 5
76
75 4
(b)
Protein Carbonhydrate
Protein and carbonhydrate (%)
70
60
50
40
30
20
10
(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 In this study, the mussel density affected the
Peterson (2003). Our study findings were similar. mussel growth and loss rate. The mussel density
The weak positive correlation found between ch-a for the NS mussels significantly decreased because
and SGR for S and NS mussels resulted from a ch-a of high density, currents and waves towards the
concentration (0.8 and 2.67 lg L1) that varied to end of the experiment. The loss rate for the NS
a greater extent in the region. This result explained mussels between August and November was signif-
that lack of relationship between ch-a and mussel icantly higher, which could be the result of stress
SGR, and temperature and TSM. The same situation related to spawning, recruitment and high densi-
is found in Fangar Bay in Spain, where any correla- ties. The differences in loss rates could depend on
tion found between the increase in shell length and high density because high density can lead to mus-
ch-a, temperature or seston is most likely due to the sels being dislodged from ropes and subsequent
wide ranges of the environmental parameters loss. The mussels exhibited density-dependent mor-
throughout the growth cycle of the mussels (M. gal- tality and fall-off (Lauzon-Guay, Dionne Barbeau &
loprovincialis) (Ramon, Fern andez & Galimany Hamilton 2005). Frechette and Desplan (1999)
2007). However, our findings are different from revealed that there is a strong effect of density;
many studies that state that a high level of ch-a is larger mussels can put pressure on smaller mussels
associated with increased mussel growth (Babarro, for food and space, and thus, smaller mussels are
Fernandez-Reiriz & Labarta 2000; Karay€ ß elik,
ucel, C more likely to dislodge. Those findings are supported
Karay€ ucel & Erik 2010). by the results of this study. The loss rate of the
ucel et al.
mussels on the high-density rope was higher than

years in Croatia (Benovic 1997; Peharda, Zupan,
the loss rate associated with the lower density Bavcevic, Frankic & Klanjscek 2007), 2.5–3 years
rope. In addition, the negative effect of stocking in Scotland (Karay€ ucel 1997) and 1.5–2 years in
density on mussel growth was demonstrated. The Canada (Drapeau, Comeau, Landry, Stryhn &
growth rate of S mussels was higher than NS mus- Davidson 2006).
sels because an increase in mussel density greatly
reduced the growth rate. Competition for food
Meat yield and condition indices
and/or space is the likely reason for slower shell
growth. Several studies have also found a negative The meat yield was strongly related to tempera-
relationship between growth rate and density ture and OM (P < 0.05) and mussel spawning
(Fuentes, Gregorio, Giraldez & Molares 2000; occurred when the water temperature increased
Gosling 2003). According to Alfaro (2006), mus- from 7.83 (March) to 9.12°C (April). The second
sels subjected to high-density growth compete with spawning time of mussels also occurred in October.
each other for space and food, so the survival and Similarly, Lemaire, Pelerin, Fournier, Girault, Tam-
feeding rate of these mussels necessarily decreases. igneaux, Cartier and Pelletier (2006) found that
There was a strong relationship between the time water temperature and food supply significantly
to reach market size and mussel density. Cultured influenced mussel spawning time. Many studies
mussels growing in lower density conditions pre- have also reported parallel results (Kautsky 1982;
sented superior growth due to less competition for Thompson 1984; Karay€ ucel et al. 2003; Cartier,
food resources (Comeau et al. 2008). Higher pro- Pellerin, Fournier, Tamigneaux, Girault & Lemaire
duction was obtained from S mussel culture ropes. 2004). In this study, a higher mussel meat yield
These results indicate that the thinning out of (29.4%) and condition index (37.33%) were
stocks is extremely important for maximizing recorded during the period (March) immediately
growth. Thus, we can conclude that thinning out is before spawning. The sudden drop in the condition
an important factor for achieving marketable yields index and meat yield was identified in the spawn-
(Table 1). McMillan (1990) also reported that resoc- ing period (April 2010). Mussels increased the
king of mussels can effectively double the market- meat yield and condition index after the spawning.
able yield of mussels on culture ropes. Thus, these findings indicate that the condition
The time to reach market size (>50 mm) varied index and meat yield of mussels were influenced
according to mussel density on the culture ropes by internal and external factors such as tempera-
in this study. The socking operation increased the ture, salinity, food supply and reproduction period.
harvested number of mussels and reduced the time The meat yield of mussels increased twofold when
to harvest. In conclusion, cultured mussel biomass the amount of food in the seawater increased
density was an important factor affecting the during the spring months (Strohmeir, Duinker,
increase in production and harvest time. In many Strand & Aure 2008). Okumus and Stirling (1998)
studies, the time to reach market size and produc- reported that the meat yield and condition index
tion vary by region. Others studies, made in the decrease depending on the gamete releases. Other
coastal areas of the same region as our study, studies have shown that condition index and
have indicated that the period of mussel cultiva- meat yield vary according to environmental factors
tion from spat settlement to harvest time was and the reproduction period of mussels (Rajagopal,
2 years (Karay€ ucel, Karay€ ucel, Erdem, Saygun & Venugopalan, Nair, Van der Velde & Jenner 1998;
Uyan 2003; Karay€ ucel et al. 2010). In addition, Orban et al. 2002; Lachowicz 2005).
Karay€ ucel et al. (2010) obtained 250 ind.m1 The meat yield of cultured mussels in the off-
(>55 mm) and Karay€ ucel et al. (2003) achieved shore area varied between 19.79% and 29.04% in
211 ind.m1 (>47 mm) in cotton socks and 532 this study. On the other hand, the meat yield of
ind.m1 in nylon socks. Langan and Horton natural mussels at the same time and same region
(2003) reported that stock density affects produc- varied between 14.34% and 21.92% (C ß ulha &
tion and the reaching of mussel market size. Other T€ ß ulha 2010). The results of this study are in
urk C
studies have demonstrated that the mussel produc- agreement with many other studies. Babarro et al.
tion cycle varies according to the geographical (2000) declared that the meat yield of collected
condition and harvest size. In other studies, the natural mussels was lower than cultured mussels
time to reach harvest size (>50 mm) was 1.5–2 because of the necessity of having to build a
thicker shell to protect themselves from strong not used for the same purpose. Similar results
waves. In another study, the meat yield of cul- were reported by Karay€ ucel (1997) and Freites,
tured mussel from a longline system in the open Fernandez-Reiriz and Labarta (2003). The lipid
sea was higher than the yield of collected natural value began to increase the month following
mussels (Brenner 2009). spawning (April). This result indicates that lipid
Harvest time is determined by taking into con- concentration decreased with spawning and
sideration the condition index wet meat volume increased again with gonadal maturation. Our
(CIV) and meat yield of mussels for the different study results suggest that lipids were an energy
regions (Zandee, Kluitmans, Zurburg & Pieters source used for gonad maturation, and these find-
1980; Kopp, Cornette & Simonne 2005; Peharda ings are in agreement with several other studies.
et al. 2007). In our study, the CIV of the mussels The biochemical composition cycles of mussels
ranged between 27.65% and 37.33% throughout indicated annual patterns of accumulation and
the year. Therefore, the results of this study indi- the use of reserves due to a complex interaction
cate that mussels should be harvested in May among food availability, growth and reproduction
(25.23%) and June (25.79%), which are spawning (Narvaez, Freites, Guevara, Mendoza, Guderley,
months. However, with regards to studies in the Lodeiros & Salazar 2008). Seasonal variations in
same region, Karay€ ucel et al. (2003) suggested a the biochemical composition of Mytilus edulis has
5-month harvesting period between January and been related to energy metabolism and gameto-
June, and C ß elik, Karayucel, Karay€ € urk and
ucel, Ozt€ genesis (Zandee et al. 1980; Karay€ ucel et al.
Ey€uboglu (2012) reported that February and May, 2002). Lachowicz (2005) reported that high lev-
when CIV was nearly 30%, were suitable for the els of glycogen and protein are rebuilt after
harvest. These differences in the same region in spawning, but lipid concentrations remain low
harvest time are due to the relatively constant and recover slowly, as glycogen is deposited in
condition of the offshore sites, which results in a the mantle tissue in months when plenty of food
less variable mussel condition and annual envi- is available. During the reproduction phase, how-
ronmental conditions. 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-
This study demonstrated that protein, lipid, carbo- nent in mussel tissue and, if needed, protein can
hydrate, ash and moisture values varied depending be used as an alternative energy source for gonad
on food supply and reproduction period. The con- formation (Galap, Leboulenger & Grillot 1997).
dition index reached its highest value in March,
and the lipid and protein values were at their
Conclusion
maximum in January. The lipid and protein values
decreased because of spawning. Our findings indicate that a submerged longline
In our study, the lipid and carbohydrate values mussel culture system works with no serious prob-
were at their highest level when OM was higher lem in accordance with the open-sea conditions of
in the spring and summer months. The mussels the Black Sea. Mussels cultivated in the submerged
required too much energy for egg maturation, offshore system presented good growth because
and accordingly, their metabolic energy reserves they were away from stresses such as strong wind,
could be affected by this energy requirement. waves, current and sudden changes in hydrological
Thus, carbohydrate reserves were reduced due to conditions. Furthermore, stock management
being used as energy for fat synthesis. Protein through thinning out of the spat can considerably
and lipid levels continued to increase until increase the marketable size of mussels, reduce har-
spawning. Carbohydrate and lipid reserves could vest time and facilitate better growth.
be used as an energy source during periods of
lower available nutrition. This finding is in agree-
Acknowledgment
ment with Lachowicz (2005). Protein levels
markedly decreased, but the amount of carbohy- We thank The Scientific and Technological Research
drate increased with spawning. These results indi- Council of Turkey (TUBITAK) for providing financial
cate that protein and carbohydrate reserves were support.
ucel et al.
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Aquaculture Research, 2015, 46, 1369–1383 doi:10.1111/are.

Effects of stocking density on survival, growth and

ucel1, Meryem Yesßim C

© 2013 John Wiley & Sons Ltd 1369

Figure 1 The study area.

Figure 2 Design of the submerged

contamination from fouling organisms, the samples

Growth and density Losses and production

(a) 62 NS type S type

Shell length (mm)

Live weight (g)

mussels for NS and S mussels; May

0 Figure 6 Monthly changes in

Culture Production Marketable Total marketable Time to reach

NS 10.59 0.43 73.52 0.78 7.78 0.21 7.78 22

CIV and MY (%)

mussels on the high-density rope was higher than

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