Aquaculture Nutrition 2003 9; 287^293
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Seasonally changing metabolism in Atlantic salmon
(Salmo salar L.) I – Growth and feed conversion ratio
U. NORDGARDEN1, F. OPPEDAL1, G.L. TARANGER1, G.-I. HEMRE2 & T. HANSEN1
1
Department of Aquaculture, Institute of Marine Research, Matre Aquaculture Research Station, Matredal, Norway; 2 National
Institute of Nutrition and Seafood Research, Bergen, Norway
Abstract
To determine seasonal variation in growth and feed conversion ratio (FCR), Atlantic salmon postsmolts (Salmo salar
L.) were exposed to either simulated natural photoperiod
(SNP) for 12 months or continuous light (LL) from January
to June followed by SNP until December. Feed was given to
excess and uneaten feed pellets were collected after every
meal for estimation of feed intake and calculation of FCR.
Body weight increased from 1086 ± 9 g (mean ± SEM) in
January to 4970 ± 7 g (SNP) and 5190 ± 23 g (LL) in
December. Specific growth rate (SGR), condition factor and
feed intake displayed strong seasonal variation in both
groups. Measurements of the thermal growth coefficient
correlated highly with SGR (r ¼ 0.98, P < 0.05), indicating
that the seasonal variation in SGR was independent of
temperature and fish size. Continuous light treatment resulted in increased growth from spring, while the fish exposed
to simulated natural light had increased growth rate in late
summer. Furthermore, LL improved FCR. Periods of high
SGR were concurrent with periods of low FCR in both
groups.
KEY WORDS:
feed conversion ratio, growth, Salmo salar,
season
Received 13 August 2002; accepted 3 December 2002
Correspondence: Ulla Nordgarden, Department of Aquaculture, Institute of
Marine Research, Matre Aquaculture Research Station, N-5984 Matredal
Norway. E-mail: [email protected]
Introduction
Atlantic salmon reared in seawater under ambient conditions
display seasonal changes in appetite and growth (Smith et al.
1993; Taranger 1993; Forsberg 1995; Kadri et al. 1997). It
has been proposed that temperature and photoperiod are
acting as major seasonal cues (Brett 1979; Busacker et al.
1990; Wootton 1990), and as a consequence, growth of
Atlantic salmon in seawater is affected by daylength (Smith
et al. 1993; Taranger 1993; Forsberg 1995) and artificial light
treatment (Endal et al. 2000).
By changing the photoperiod to continuous light (LL)
during winter, the fish exhibit increased growth rate (Saunders & Harmon 1988; Endal et al. 1991, 2000; Kråkenes et al.
1991; Taranger et al. 1991, 1995; Hansen et al. 1992;
Taranger 1993; Oppedal et al. 1997; Duncan et al. 1999;
Porter et al. 1999) compared with those exposed to a natural
photoperiod. Long-term growth enhancement under long
photoperiods may be due to a photoperiodic alteration of
seasonal growth patterns, or to a direct photo-stimulation of
growth (Saunders & Harmon 1988; Kråkenes et al. 1991;
Hansen et al. 1992). More recently, Endal et al. (2000) concluded that the major effect of the photoperiod was to act as
a ÔzeitgeberÕ adjusting circannual growth. These results are
also supported by the work of Oppedal et al. (1997, 1999)
who found distinct shifts in the seasonal patterns of specific
growth rate and condition factor following the switching on
or off of artificial light. In addition, increased daylength has
been suggested to increase appetite (Taranger et al. 1995) and
improve feed conversion ratio (FCR) (Gross et al. 1965;
Woiwode & Adelman 1991; Jobling 1994); both contributing
to enhanced growth.
The aims of this work were to study seasonal growth
patterns and FCR in Atlantic salmon reared under natural
and continuous light. This paper presents parts of the results
from a large study, which also includes seasonal influence on
muscle quality (Nordgarden, U., Ørnsrud, B., Hansen, T. &
Hemre, G.-I., Aq.Nutr., in press), lipid metabolism (Nordgarden, U., Torstensen, B., Frøyland, L., Hansen, T. &
Hemre, G.-I., Aq.Nutr., in press) and growth endocrinology
(unpublished).
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2003 Blackwell Publishing Ltd
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U. Nordgarden et al.
Materials and methods
Fish stock and rearing conditions
On 19 January 1999, 1200 individually tagged Atlantic salmon (Trovan tag ID100/01, LID 500 Hand Held Reader,
Trovan, BTS Scandinavia AB) with initial weight of
1086 ± 9 g (mean ± SE) were distributed among six
indoor, seawater tanks (D ¼ 5 m, d ¼ 1 m, 20 m3) at the
Institute of Marine Research, Department of Aquaculture,
Matre Aquaculture Research Station (61N, western
Norway). The fish had been reared indoor under simulated
natural photoperiod (SNP) since first feeding in February
1997. In May 1998, being 1+ smolts, they were transferred
to indoor, seawater tanks similar to the experimental tanks,
where they were reared until start of the experiment.
Three tanks were given SNP for 12 months and three tanks
were given LL from January to June, followed by SNP
throughout the experiment (Fig. 1). The LL treatment is
shown to reduce sexual maturation in adult Atlantic salmon
(Taranger et al. 1998). Therefore, this photoperiod regime
was chosen in addition to an SNP, to evaluate growth and
FCR.
Artificial illumination was provided by one asymmetric
metal halogen lamp per tank (EUROFLOOD by Siemens
AS, Trondheim, Norway. Bulbs: Osram, Lysaker, Norway
HQI-TS 150W/NDL) mounted on the side of the tank, 4 m
above the surface giving an illumination of 105 ± 7 lux, irradiance of 6.0 · 10)5 Wcm)2, and a flux of approx.
1.8 · 1014 photons s)1 cm)2 at the bottom of the tank. The
light had a normal spectral distribution with maximum irradiance at 535 and 592 nm.
Seawater was pumped from the fjord 20 m below surface,
resulting in natural temperature variations for the area
12.5
24
LL
11.0
18
10.5
16
10.0
14
9.5
9.0
SNP
12
Temperature (˚C)
11.5
20
(Fig. 1). Oxygen content of the water was above 8 mg L)1
during the whole experiment. Salinity varied between 24.5
and 30 g L)1.
Fish were fed in excess twice per day, 5 days week)1
(Monday–Friday, similarly in both treatment groups) with
commercial dry feed (Bio-Optimal 28/45, BioMar AS, Myre,
Norway; pellet size 7, 23.7 kJ g)1, Table 1). Each meal lasted
60 min (09:00–10:00 and 14:00–15:00 hours), and all uneaten
feed pellets were collected after every meal for calculation of
daily feed intake. The uneaten feed pellets were sampled on a
grating at the water effluent (faeces were washed off) and
collected 15 min after termination of each meal.
Measurements of weight and length
Every sixth week, fork length (to the nearest 0.5 cm) and live
body weight (to the nearest gram) of all fish in each tank were
measured. Fish were anaesthetized with metomidate hydrochloride (7 lg L)1, Wild-life Pharmaceuticals, CO, USA)
according to Olsen et al. (1995) to facilitate sampling.
Calculations
Condition factor (K) from all individuals was calculated
using:
K ¼ ðWL3 Þ100
where W is live body weight (g) and L is fork length (cm) of
each fish (Busacker et al. 1990). Specific growth rate (SGR,
% day)1) and specific length growth (SLG, % day)1) from all
individuals were calculated from the formula:
SGR/SLG ¼ ðeg 1Þ100
(Houde & Scheckter 1981), where g ¼ [ln(W2))ln(W1)]/
(t2)t1) (Bagenal & Tesch 1978) and where W2 and W1 were
Table 1 Experimental diet composition
12.0
22
Day length (h)
288
Formulations1
Fish meal, Fish oil, Suprex wheat,Vitamins/minerals2, Pigment3
Proximate diet composition (gkg)1 dw)4
Protein
Fat
Dry matter
501
270
954
8.5
10
8.0
SNP
8
J
F
7.5
M
A
M
J
J
A
S
O
N
D
Figure 1 Photoperiod treatments (solid lines) and temperature variations (dotted line) during the experiment.
1
From Biomar feed tables on feed composition.
Vitamins per kg diet: vitamin A, 6000 IU; vitamin D3, 3000 IU; vitamin
E, 180 mg; vitamin C, 100 mg. Minerals per kg diet: CuSO4, 10 mg; Na2
SeO3, 0.4 mg; KI, 1.0 mg; MnSO4, 50 mg; Zn2SO4, 150 mg.
3
Astaxanthin, 60 mg kg)1.
4
Proximate diet composition analysed in association with the present
study.
2
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2003 Blackwell Publishing Ltd Aquaculture Nutrition 9; 287^293
Seasonal changes in growth and feed conversion in Atlantic salmon
the average live body weights (g) or body lengths (cm) at
times t2 and t1, respectively. Thermal growth-unit coefficient
(TGC) was calculated using:
1
(a)
1
ðA ADM =100Þ ðW WDM =RÞ
ADM =100
where A is weight of feed pellets (g), ADM is dry matter
content of feed (%), W is weight of uneaten feed collected (g),
WDM is dry matter content of uneaten feed (%) and R is
recovery of dry matter of uneaten feed (%), calculated as
R(%) ¼ 100 · W · WDM/A · ADM (Helland et al. 1996).
Feed intake (FI) was defined as daily feed eaten expressed in
terms of percentage of live body mass, calculated from the
mean daily feed eaten, over a 2-week interval, divided by the
estimated biomass in each tank during that period, multiplied
by 100. Biomass increase after the 2-week interval was estimated using the FCR value for the specific period.
*
4500
Weight (g)
4000
*
3500
3000
*
2500
*
2000
*
1500
1000
(b)
LL
SNP
0.9
0.8
When comparing photoperiod treatments, data obtained on
SGR, SLG, K and body weight were subjected to nested
analysis of variance, with three parallel tanks as the random
factor nested into the dependent factor photoperiod. Data
obtained from estimated FCR and FI were subjected to a
one-way ANOVA (Sokal & Rohlf 1995). Correlations were
performed by Pearson product-moment correlation and
regression analysis by multiple regressions. Significant differences among treatment groups are indicated by asterisks
(*) at significance level P < 0.05. Data analysis was performed using the Statistica 5.1 (StatSoft, Inc., Tulsa, OK,
USA) software package.
Results
Growth
Mean body weight increased from 1086 ± 9 g in January to
5190 ± 23 g (LL) and 4970 ± 7 g (SNP) in December
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2003 Blackwell Publishing Ltd Aquaculture Nutrition 9; 287^293
*
*
*
0.6
*
0.5
0.4
0.3
*
0.2
0.1
0.0
–0.1
J
Statistics
*
*
0.7
SGR
Air-dry feed eaten (g) ¼
*
5000
TGC ¼ ðW23 W13 Þ 1000=ðday degreesÞ
where W2 and W1 were the average live body weights (g) at
the start and end of a 6-week period, specified by its daydegrees (Cho 1992; Mørkøre & Rørvik 2001).
The FCR for each tank was calculated as: g feed eaten
divided by g biomass increase obtained for the 6-week period
between samplings. Daily feed intake was estimated from dry
matter content (drying in 105 C, 24 h) of the uneaten feed,
calculated from the formula:
LL
SNP
5500
F
M
A
M
J
J
A
S
O
N
D
Figure 2 Weight increase (a) and specific growth rate (percentage
day)1) (b) for Atlantic salmon reared under continuous light (LL) or
simulated natural photoperiod (SNP). Data are presented as tank
means ± SEM. Statistical differences (P < 0.05) among photoregime groups are marked by asterisks (*).
(Fig. 2a). As a consequence of a significantly higher SGR
(SNP: 0.15 ± 0.04 vs. LL: )0.07 ± 0.05, P < 0.05) during
the first 6 weeks (Fig. 2b), the SNP group was significantly
heavier than the LL group in early March. The SGR
increased in both groups during spring. However, the SGR in
LL group increased more steeply, compared with the SNP
group. Highest SGR was seen in late April–May in the LL
group (0.82 ± 0.02) compared with July–August in the SNP
group (0.77 ± 0.03). The significantly higher SGR in the LL
compared with the SNP group during spring gave the LL
group a significantly higher body weight from late May until
early November. The TGC (Fig. 3) and SGR correlated with
r ¼ 0.98, P < 0.05.
Condition factor (K) displayed a changing pattern with
season, involving a general decrease during spring, an
289
U. Nordgarden et al.
*
4.0
LL
*
3.5
*
0.24
3.0
*
*
0.21
*
2.5
*
0.18
SLG
TGC
LL
SNP
0.27
SNP
2.0
1.5
*
0.15
0.12
1.0
*
0.09
0.5
0.06
0.0
0.03
–0.5
J
F
M
A
M
J
J
A
S
O
N
D
Figure 3 Thermal growth-unit coefficient for Atlantic salmon reared
under continuous light (LL) or simulated natural photoperiod
(SNP). See Fig. 2 for further details.
increase during summer and autumn, and a decrease from
November (Fig. 4). However, the pattern was advanced in
the LL group with a spring low in early March (K ¼ 1.05)
compared with mid-April in the SNP group (K ¼ 1.13).
Further, K in the LL group increased during spring while K
in the SNP group was still low, resulting in a significantly
higher K in the LL group between late May and late September, compared with the SNP group. Both groups had
decreasing K from November.
Specific length growth increased until April in both groups.
Thereafter the SNP group ceased its length growth for several months, while the LL group continued increasing until
May (LL: 0.19 ± 0.00 vs. SNP: 0.13 ± 0.01) (Fig. 5). Both
groups had highest length growth in August, followed by a
gradual decrease for the rest of the experiment. There were
no differences between parallel tanks.
*
LL
SNP
1.40
*
1.35
*
*
1.30
*
1.25
K
290
1.20
*
1.15
1.10
1.05
J
F
M
A
M
J
J
A
S
O
N
J
F
M
A
M
J
J
A
S
O
N
D
Figure 5 Specific length growth (percentage day)1) for Atlantic salmon reared under continuous light (LL) or simulated natural
photoperiod (SNP). See Fig. 2 for further details.
Feed intake
Feed intake correlated well with SGR (LL: r ¼ 0.86,
P < 0.05, SNP: r ¼ 0.88, P < 0.05). The FI increased in
February in both groups (Fig. 6a). Initially the LL group had
lower FI compared with the SNP group, but from April the
LL group exceeded the SNP group. The LL group reached
highest FI in May, while FI increased more slowly in the
SNP group and reached highest level in August–September.
From August until end of the experiment the LL group
consumed less than the SNP group.
Feed conversion ratio from the first 6 weeks was not
calculated as sampling of uneaten feed started 12 days after
the initial sampling and measurements of length and weight
of fish. The LL group had low FCR compared with the
SNP group in March and April (LL: 0.68 ± 0.04 vs. SNP:
0.98 ± 0.00) (Fig. 6b). The SNP group had lower FCR
compared with the LL group from May to June (LL:
1.02 ± 0.02 vs. SNP: 0.80 ± 0.02). From June until the end
of the experiment no differences between the groups were
detected.
The SGR correlated negatively with FCR in the LL group
(r ¼ )0.76, P < 0.05) and the SNP group (r ¼ )0.64,
P < 0.05) (Fig. 7); FCR and temperature covaried significantly, with FCR as the dependent variable (LL: r2 ¼ 0.35,
SNP: r2 ¼ 0.25, P < 0.05). Both mortality and sexual
maturation were low (<5%) with no difference between the
groups.
D
Discussion
Figure 4 Condition factor for Atlantic salmon reared under continuous light (LL) or simulated natural photoperiod (SNP). See
Fig. 2 for further details.
The SNP group displayed strong seasonal variation in
growth rate, condition factor and FI. When exposed to LL
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2003 Blackwell Publishing Ltd Aquaculture Nutrition 9; 287^293
Seasonal changes in growth and feed conversion in Atlantic salmon
FI
(a)
FCR
(b)
1.4
1.3
1.2
1.1
1.0
0.9
0.8
0.7
0.6
0.5
0.4
0.3
0.2
0.1
LL
SNP
LL
SNP
May
0.8
Aug
Jun
Aug
Sep
Jun
Apr
SGR
0.6
0.4
*
*
*
*
* *
Sep
*
Apr
Dec
0.2
*
0.6
*
1.0
1.2
1.4
1.6
1.8
Figure 7 Specific growth factor (SGR) plotted against feed conversion ratio (FCR) in Atlantic salmon reared under continous light
(LL) (underlined) and simulated natural photoperiod (SNP). (Each
point illustrates the mean value of three replicate tanks for the SGR/
FCR correlation at the samplings in Apr ¼ April, May ¼ May,
Jun ¼ June, Aug ¼ August, Sep ¼ September, Nov ¼ November,
Dec ¼ December.)
LL
SNP
*
*
F
0.8
FCR
*
1.9
1.8
1.7
1.6
1.5
1.4
1.3
1.2
1.1
1.0
0.9
0.8
0.7
0.6
Dec
Nov
*
* *
* *
Nov
May
M
A
*
M
J
J
A
S
O
N
D
Figure 6 Feed intake (percentage of biomass) (a) and feed conversion ratio (b) in Atlantic salmon reared under continuous light (LL) or
simulated natural photoperiod (SNP). See Fig. 2 for further details.
from January an advanced seasonal growth pattern was
observed, where the group exposed to LL grew better at an
earlier time, compared with the fish exposed to SNP. These
results are in accordance with several earlier studies (Saunders & Harmon 1988; Endal et al. 1991, 2000; Kråkenes et al.
1991; Taranger et al. 1991, 1995; Hansen et al. 1992;
Taranger 1993; Oppedal et al. 1997; Duncan et al. 1999;
Porter et al. 1999).
Initially, low levels in somatic growth and condition factor,
concurrent with low appetite, were found when the fish were
abrupt changed to LL. This is supported by previous studies
indicating reduced appetite (Taranger et al. 1995) and
growth (Hansen et al. 1992; Endal et al. 2000) in the first
period following an abrupt change to LL of salmon in seawater. The initial reduction in condition factor might be
caused by a seasonal elevation of length growth some time
prior to a seasonal elevation in weight growth (Oppedal
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2003 Blackwell Publishing Ltd Aquaculture Nutrition 9; 287^293
2003). The present study did not support this hypothesis. We
suggest that the low FI resulted in low weight growth compared with length growth, as weight growth is easily influenced by reduced FI (Klontz et al. 1991; Einen et al. 1999),
while length growth proceeds a long time after reduced FI (T.
Hansen & B.T. Björnsson unpublished data).
The initial growth/appetite depression in seawater was
probably a consequence of either stress, caused by the
changing environment, or a postulated phase advancement
of a circannual growth rhythm (Eriksson & Lundquist 1982)
involving reduced winter growth adjusted by photoperiod
(Endal et al. 2000). Atlantic salmon postsmolts appear to
have a period of reduced growth during the winter months
even when maintained at stable temperatures in sea water
tanks on natural photoperiods, indicating a photoperiodic
down-regulation of growth (Taranger 1993; Forsberg 1995).
Exposure to LL may have advanced and/or compressed such
a period. The decrease in growth and condition factor was
followed by a subsequent earlier growth improvement in the
LL group compared with that reared under natural conditions.
Specific growth rate declines with fish size and increases
with temperature within the optimum temperature range of a
species (Brett 1979). To evaluate the effect of photoperiod on
SGR the TGC was calculated. The TGC is a calculation of
growth that corrects for changes in temperature and fish size
over the experimental period (Cho 1992, Mørkøre & Rørvik
2001). As TGC correlated highly with SGR, the hypothesis
that photoperiod is the predominant cue affecting the SGR
rhythm is strengthened in this study.
291
292
U. Nordgarden et al.
A close relationship is suggested between growth rate and
FCR, as FCR like SGR, depends highly on temperature
and fish size. An exceptionally low FCR was obtained for
a short period preceding a period of notable growth
improvement in the LL group. A probable explanation
might be that as the fish had gained length during winter
(causing low K), further deposition (weight increase because
of muscle and lipid deposition) required less energy. Similar
values are reported from industrial experiments under
optimal feed and rearing conditions. The FCR declines with
temperature and increases with fish size (Brett 1979), causing a negative correlation with SGR. The SGR/FCR
interactions are established in a few studies (Gross et al.
1965; Jobling 1987) but not in Atlantic salmon of larger
sizes. This experiment has shown a correlation between
growth rate and FCR in both photoperiod groups, where
periods of high growth concurred with periods of improved
feed conversion. Generally FCR and SGR correlate as the
calculation of FCR involves the calculation of growth. On
the contrary, growth may be improved without improved
FCR, as increased appetite may stimulate growth alone.
Because of this, both parameters should be measured
to separate growth as a consequence of improved feed
utilization or increased FI.
Acknowledgements
The authors wish to thank Arnor Gullanger and the rest of
the staff at Matre Aquaculture Research Station for technical
assistance. This study was financially supported by the
Research Council of Norway (No. 122825/122), and Biomar
contributed feed.
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