T.

Boujard
M. Mambrini, F. Mdale, M.P. Sanchez, B. Recalde, B. Chevassus, L. Labb, E. Quillet and
maintenance and growth requirements
Selection for growth in brown trout increases feed intake capacity without affecting
2004, 82:2865-2875. J ANIM SCI
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Selection for growth in brown trout increases feed intake capacity
without affecting maintenance and growth requirements
1
M. Mambrini*
2
, F. Me dale, M.-P. Sanchez*
3
, B. Recalde, B. Chevassus*,
L. Labbe , E. Quillet*, and T. Boujard*
*INRA, Laboratoire de Genetique des Poissons, 78350 Jouy-en-Josas, France; Unite Nutrition,
Aquaculture et Genomique, 64310 Saint Pee sur Nivelle, France; and SEMII, 29450 Sizun, France
ABSTRACT: The correlated responses in feed intake
and G:F ratio with selection for increased growth rate
were evaluated by comparing selected (S) and control
(C) brown trout (Salmo trutta) reared under conditions
known to affect feed efciency: feed restriction and peri-
ods of compensatory growth. Nitrogen and energy re-
quirements for maintenance and growth were also mea-
sured. Trout were allotted at comparable BW (3.7
0.06 and 3.8 0.04 g, for C and S respectively) to tripli-
cate groups per treatment. The experiment lasted a
total of 198 d, during which animals were successively
submitted to a 116-d feeding phase and fed 10, 30, 50,
70, 100, and 140% of their usual daily ration (UDR), a
35-d phase of food deprivation, and a 47-d refeeding
phase. The G:Fof Cand Swere comparable inall experi-
mental conditions tested. During the feeding phase, S
grew better than C only when fed 100 and 140% UDR
(P < 0.001). This was explained by a higher feed intake
Key Words: Correlated Responses, Energy Requirements, Feed Intake, Growth Rate, Salmo trutta, Selection
2004 American Society of Animal Science. All rights reserved. J. Anim. Sci. 2004. 82:28652875
Introduction
Selection for growth in sh using familial or individ-
ual procedures leads to relatively high genetic gains
(10 to 20% per generation; Gjedrem, 1998; Vandeputte
et al., 2002). Although selection for growth is more re-
cent than in other farmed animals, the selected lines
of sh are now sufciently divergent to carry out an
analysis of the correlated responses. As in higher verte-
1
The authors thank I. Queau for the daily care of the sh and the
team at the SEMII sh farm for their help. The technical assistance
of D. Blanc and M. J. Borthaire is also gratefully acknowledged. We
also wish to thank J. B. Denis for his statistical expertise.
2
Correspondence: Domaine de Vilvert (phone: 33 1 34 65 27 05;
fax: 01 34 65 23 90; e-mail: mambrini@jouy.inra.fr).
3
Present address: INRA, Station de Genetique Quantitative et
Appliquee, Domaine de Vilvert, 78352 Jouy-en-Josas Cedex, France.
Received December 17, 2003.
Accepted June 2, 2004.
2865
capacity. The requirements for growth and mainte-
nance were similar among the lines, which is in
agreement with their comparable loss of weight (mean
energy loss of 53 and 55 kJ/(kgd) for C and S, respec-
tively; P > 0.38) observed during the feed deprivation
phase and the lack of differences in carcass composition
(fat, P > 0.35; protein, P > 0.54). During the refeeding
phase, growth performance and G:F were high in all
groups. The daily growth coefcient was higher in S
than in C (P < 0.001) because of a higher feed intake
(P < 0.001). An increase in absolute individual variabil-
ity in nal BW and length was associated with the
level of food restriction in both lines; however, it always
remained lower in S than in C. In conclusion, sh se-
lected for growth under ad libitum conditions will only
exhibit growth superiority when fed diets close to ad
libitum, and there was no evidence that selection was
associated with an improvement in efciency of mainte-
nance nor in retention of body tissues.
brates (Rauw et al., 1998), the enhanced growth rates
are explained by an increased feed intake associated
(Thodesen et al., 1999) or not associated (Sanchez et
al., 2001) with improved G:F. Response variability may
be explained by the different selection procedures (fa-
milial or individual), the selection criteria (BW or
length), the basis of comparisons (wild or domesticated
control lines), and the ways sh are fed and feed intake
is measured. In sh, the group level is generally the
experimental unit. This implies specic experimental
designs, particularly when intake is considered.
Brown trout have been selected by an enhanced indi-
vidual procedure since 1987 (Chevassus et al., 1992),
and a control line has been maintained. It seems that
selected sh exhibit their growth potential when fed ad
libitum only (Sanchez et al., 2001), and G:F may not be
affected by selection. This suggests that the nutritional
requirements are not different between the lines. The
objective of this study was to verify that G:F is not
affected by selection. Our strategy was to test the ro-
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Mambrini et al. 2866
bustness of the response by analyzing the genotype
environment interactions when the lines are reared
under conditions known to affect feed efciency: feed
restriction (Cho, 1992) and conditions for compensatory
growth (Dobson and Holmes, 1984). The specic effects
of such rearing conditions are not well known in brown
trout, so they will be described rst in the controls.
The specic effect of selection will then be assessed.
In addition, the experiment was designed to compare
maintenance and growth requirements of both lines.
Indeed, the specic effect of selection for growth on
nutritional requirements has never been described in
sh.
Materials and Methods
Animals
A specic strain of brown trout (Salmo trutta) was
selected by an individual selection process for ve gen-
erations in our experimental sh farm (SEMII, Sizun,
Brittany, France). This strain (population reared in
northern France) was chosen because of its better
growth performance compared with the other brown
trout strains initially tested (French and Danish reared
and wild populations). The criterion of selection was
fork length (L, sh length measured at the clearance
of the caudal n), mainly because it is easier to measure
than weight (Chevassus et al., 1992). From the same
initial population, a control line (C) was maintained
under the same rearing conditions. With a selection
pressure on L of approximately 5% (proportion of sh
selected), the correlated weight gain at 1 yr of age was
approximately 24% per generation (on average over
four generations) for the selected line (S) compared with
the C (Vandeputte et al., 2002). The S and C groups of
the current study were produced by in vitro fertilization
of 34 S females crossed with 11 S males and 27 C fe-
males crossed with 37 C males. To obtain selected and
control offspring reaching a similar weight of approxi-
mately 4 g at the beginning of the experiment, we took
into account the value of the growth rate usually ob-
served for such lines (our unpublished data; Sanchez
et al., 2001) and calculated that C had to be fertilized
12 d before S.
After hatching, ngerlings were reared in two tanks
per line supplied with 11C ow-through water. They
were fed ad libitum a commercial dry feed (Biomar
Ecolife 18 (Nersac, France) containing 51%CPand 18%
lipid (data fromthe manufacturer) by automatic feeders
delivering food 12 h/d until the beginning of the experi-
ment. The day before allotment, the distribution of
length of the two populations was analyzed to optimize
the constitution of the experimental groups. This was
based on individual L of 580 C (range recorded = 55 to
81 mm) and 782 S (range recorded = 55 to 91 mm) sh.
The individual BWwere also recorded. Trout were then
sorted to obtain homogeneous groups with L between
60 and 80 mm. The effect of the sorting was assessed
after controlling the distribution of BW and L in the
sorted populations (299 C and 302 S). Each line was
divided into nine sets of 100 and nine sets of 150 sh
reared in 180 L ow-through tanks supplied with bore
hole water (temperature 11 to 12C).
The experiment was conducted in a manner compati-
ble with national legislation on animal care. In applica-
tion of the French penal and rural code, M. Mambrini
and T. Boujard have personal authorization delivered
by the French Agricultural Ministry for conducting ani-
mal experiments (Authorizations 5625 and 5635) and
ensured that all procedures used in this experiment
were ethically acceptable and followed the procedures
stipulated by the French Ministry of Research.
Experiment
The experiment was divided into three successive
phases: 1) the feeding phase, where sh were fed six
different feeding levels; 2) the feed deprivation phase;
and 3) the refeeding phase, where all groups of sh
were fed in excess.
During the feeding phase, groups of 150 sh were fed
at 10, 30, or 50%, whereas groups of 100 sh were fed
at 70, 100, or 140% of the usual daily ration (UDR,
calculated using the prediction software Ecureuil, de-
veloped at the SEMII sh farm, taking into account the
sh species, the water temperature and the weight of
the sh). The group size was chosen so that the biomass
expected at the end of the experiment remained much
lower than 100 kg/m
3
, a biomass under which growth
performance remains optimal in salmonids (Boujard et
al., 2002). The number of individuals in the more feed
restricted groups was higher compared with the other
groups because of the expected mortality. Moreover,
the induced difference in density does not affect the
behavior of the sh at this biomass level (Boujard et
al., 2002). The sh were fed by automatic feeders in a
2 6 3 factorial design (line feeding level repli-
cates). The uneaten food was collected at the outlet of
each tank three times per week, dried, and weighed,
and this weight was subtracted from the amount of
food distributed to calculate the actual amount of feed
consumed. Fish were fed for 116 d, except those fed 10
and 30% UDR, for which the experiment was stopped
after 82 d. As a higher mortality was expected in those
groups, plans were implemented to stop a feeding level
if mortality was close to 10%of the assignedindividuals.
Only the sh fed 50 to 140% UDR were included in the
next two phases of the experiment.
The phase of feed deprivation lasted for 35 d. During
the refeeding phase, sh were all fed 140% UDR for 47
d. As during the feeding phase, sh were fed by auto-
matic feeders and the actual amount of feed consumed
was deducted, taking into account the uneaten food.
The diet used throughout the experiment contained
(DM basis) 49.4% CP, 25% crude fat, and 23.7 kJ of
GE/g. This high-protein, high-energy diet consisted of
extruded pellets of different diameters that were kept
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Selection for growth of brown trout 2867
at 4C until use. Pellet size was chosen according to
the sh size.
Measurements and Calculations
Mortality was recorded daily throughout the experi-
ment and the weight of the dead sh was taken into
account for weight gain calculations. At the end of each
experimental phase (feeding, feed deprived, and refeed-
ing) for the groups initially fed 50 to 140%of their UDR,
and on d 82 only for those fed 10 and 30% UDR, the
sh were counted and weighed by group after 1 d of
fasting. Growth coefcients were calculated according
to Cho (1992), using the daily growth coefcient (DGC),
a value independent of the BW. Gain:feed ratios were
calculated taking into account the actual feed con-
sumed. Individual weights (grams, noneviscerated) and
fork lengths (to the nearest millimeter) were recorded
for all sh. Coefcients of variation of weight, length,
and the conformation coefcient (K-factor) were calcu-
lated within each tank.
Twenty sh were initially sampled for whole body
composition. The whole body samples were frozen
(20C), ground, and freeze dried. At the end of the
feeding and feed deprivation phases, 10 sh per tank
were sampled and immediately frozen for subsequent
analysis. The following analyses were performed on the
diet and whole carcasses: DM, CP (N 6.25), GE, and
fat (AOAC, 1990). The water content was calculated by
weight loss after drying at 110C for 24 h in a forced-air
oven. Nitrogenanalysis of all samples was performed by
the Kjeldahl method. The GE content of the diet was
determined with an adiabatic bomb calorimeter (IKA,
Staufen, Germany). Fat content was calculated after
extraction in a Soxhlet apparatus using petroleum
ether as solvent.
Proteinandenergy gains were plottedagainst protein
and energy intake expressed as g/(kg BW
0.75
d) and kJ/
(kg BW
0.75
d), respectively, to estimate maintenance
and growth requirements. Data were adjusted using
linear model and saturation kinetics model (Mercer,
1982), whichbothled to similar estimates. Maintenance
requirements were interpolated using the linear model,
as the amount of protein and energy intake resulting
in protein and energy gain equal to zero (x-intercept),
and requirements for growth were estimated as the
inverse of the slope. In addition, for feeding levels
higher than 30% UDR, protein and energy use for body
accretion were calculated as the intake of protein and
energy per kilogramof wet weight gain during the feed-
ing phase. Nutrient losses during the food deprivation
phase were deducted from the body composition data.
Statistical Analyses
Statistical analyses were based on a completely ran-
dom experimental design. Group data were compared
using an analysis of covariance, including the effects
of line, feeding level, and interaction between these
two factors, which were tested using the tanks as the
experimental unit (three replicates per treatment). Per-
centage data were transformed (arcsine square root)
before being subjected to the analysis.
For the group growth data, the covariate included in
the model was the initial BW of each experimental
phase. For the feeding phase, the initial BW was taken
into account because of a slight difference between the
two groups (see results). For the feed deprivation and
the refeeding phases, the mean BW at the end of the
previous phases were used as a covariate. For the body
composition data, the covariate included in the model
was the nal BW because it is accepted that body com-
position greatly inuences BW (Shearer, 1994).
Individual data were compared using an ANOVA in-
cluding the effects of the line, the feeding level, the
interaction between these two factors, and the effect
of the tank nested into this interaction (100 to 150
individuals per tank, with three replicates per
treatment).
Probabilities of differences between treatments and
residual standard deviation were generated after AN-
OVA was performed using the GLM procedure of SAS
(SAS Inst., Inc., Cary, NC). When the interaction was
signicant, the respective effects of the line and the
feeding level were tested separately withone-factor AN-
OVA. The means were subsequently compared using
the test of Newman and Keuls (with P < 0.05).
To compare the extent of the absolute variation for
each individual variable (BW, length, K-factor), they
were transformed to logarithms, and the equality of
the absolute deviates in each class was controlled. The
absolute deviate was calculated as (|lnY
ij
lnY

j
|), where
Y
ij
is the jth term in the ith sample, and lnY

i
is the
mean logarithm of the ith sample. The scatter of the
absolute deviates was markedly unequal, indicating
that a nonparametric test has to be applied (Sokal and
Braumann, 1980). The CV were thus compared with
the nonparametric test of Kruskal-Wallis using the
NPAR1WAY procedure of SAS. The line and feeding
level effects were tested separately (three replicates
per treatment).
Results
Allotment
Before the allotment, and although S were fertilized
after C, S were unexpectedly heavier and longer than
C (BW = 3.8 vs. 4.4 g, L = 67 vs. 70 mm for C and S,
respectively; P < 0.001). Conversely, the K-factor was
not different between the two lines (1.27 and 1.26 for
C and S respectively, P > 0.87). The mean L was not
affected by the sorting out, and C remained shorter
than S (6.8 and 7.0 cm for C and S, respectively, P <
0.001). The sorting out tended to lead to a decrease in
the mean BW, although C remained lighter than S (3.7
and 3.8 g for C and S, respectively; P < 0.001). As a
consequence, the sorting induced a decrease in the K-
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Mambrini et al. 2868
Table 1. Growth and nal body composition of brown trout selected for growth (S) or controls (C) fed at 10 and 30%
of the usual intake (as-fed basis) for 82 d
a
Feeding level and line
P-value
b
10% 30%
Measurements C S C S SEM L F L F Tank
Tank records
c
Initial mean BW, g 3.7 3.8 3.6 3.8
Cumulative intake, g/sh 1.3 1.3 3.1 3.1 0.01 0.87 0.001 0.75
Daily growth coefcient, %/d
d
0.11 0.08 0.51 0.48 0.008 0.96 0.001 0.90
G:F 0.53 0.39 1.27 1.22 0.031 0.67 0.001 0.53
Final body composition, % or kJ/g BW
e
Water 74.5 74.2 74.2 74.0 0.28 0.70 0.68 0.99
Protein 15.3 16.1 14.6 14.8 0.66 0.20 0.72 0.52
Fat 5.0 4.3 6.7 6.8 1.18 0.32 0.08 0.11
Energy 6.1 6.1 6.4 6.6 0.53 0.32 0.11 0.48
Individual records nested by tanks
f
Final BW, g 4.1 4.4 7.1 7.2 0.11 0.31 0.001 0.90 0.001
Final length, cm 7.3 7.6* 8.3 8.5* 0.04 0.006 0.001 0.63 0.001
K-factor, g/cm
3g
1.04 1.00* 1.12 1.10* 0.006 0.006 0.001 0.61 0.001
CV, %
h
Final BW 31.7 28.3 49.9 45.5 0.45 0.001
Final length 8.5 8.3 14.7 13.8 0.81 0.001
K-factor 15.7 15.3 14.5 12.9 0.21 0.46
a
Data were obtained on three tanks per treatment, with 150 sh in each tank. Tank records are means of measurements performed on
each tank. Individual records are means and CV of measurements performed on each individual within each tank. When the line feeding
method interaction was signicant (P < 0.05), separate variance analyses testing the effect of the line within a feeding level were performed.
*Indicates when S was different (P < 0.05) from C at the corresponding feeding level.
b
Probability for the effects of line (L), feeding level (F), the line feeding level (L F) interaction and the tank effect.
c
Analysis of covariance.
d
100(Final BW

Initial BW

)/d.
e
Whole body initial composition: (for S) 76.8% water, 13.9% protein, 5.3% fat, 5.8% energy; (for C) 77.4% water, 13.6% protein, 5.1% fat,
5.5 kJ/g energy.
f
ANOVA.
g
100(BW/fork length
3
).
h
Kruskal-Wallis test separate analysis.
factor, which was more important for S than for C (1.12
and 1.17 respectively, P < 0.001). Thus, there was a
slight but signicant difference of BW, L, and K-factor
between S and C at the beginning of the experimental
period, which was taken into account in further
analyses.
Survival rate at the end of the experiment was higher
than 95% in groups fed at least 50% UDR. For groups
fed less than 50% UDR, the experiment lasted only for
82 d, and mortality ranged between 88 and 90%.
Feeding Phase
During the feeding phase, the effect of the line on
daily growth coefcient and feed intake depended on
feeding level (Tables 1 and 2). Daily growth coefcient
was signicantly different (P < 0.001) between lines
only when they were fed 100 and 140%UDR. For groups
fed 10 to 70% UDR, no uneaten feed was detected, so
it was considered that all the feed distributed was
eaten. At these feeding levels, cumulative feed intake
was not different between C and S (Tables 1 and 2). At
100% UDR, uneaten feed was observed for C only (8.2
2.3% of the distributed feed). At 140% UDR, the pro-
portion of distributed feed that was uneaten was higher
in C (14.9 3.2%) than in S (9.4 0.9%). Thus, the
main differences between lines in sh fed 100 and 140%
UDR was in their respective cumulative feed intake
(Table 2). Gain:feed ratio was affected by the feeding
level, being lower at the lowest feeding levels (10, 30,
and 50% UDR) and maximal at 100% UDR. Whatever
the feeding level, G:Fwas never different betweenlines.
Regarding the nal body composition, proteincontent
values were comparable among the lines and the feed-
ing levels. Fat content values increased withthe feeding
level, but this was only because of differences in BW.
Indeed there was no signicant effect of the treatments
when nal BW was included as a covariate (Tables 1
and 2).
The protein and energy gains increased linearly with
the protein and energy intake, respectively (Figure 1),
without any differences between lines. The estimated
maintenance requirements were similar among the
lines: 8.1 and 8.5 g of CP/(kg BW
0.75
d) and 446 and 433
kJ of GE/(kg BW
0.75
d) for S and C lines, respectively.
The growth requirements were also comparable be-
tween the lines: 1.53 and 1.44 g of CP/g of protein gain
and 1.37 and 1.35 kJ of GE/kJ of energy gain for S
and C lines, respectively. The amounts of CP and GE
utilized to produce 1 kg of wet weight gain were also
similar for both lines at each feeding level tested (Table
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Selection for growth of brown trout 2869
Table 2. Growth and nal body composition of brown trout selected for growth (S) or controls (C) fed at 50, 70, 100,
and 140% of the usual intake (as-fed basis) for 116 d
a
Feeding level and line
P-value
b
50% 70% 100% 140%
Measurements C S C S C S C S SEM L F L F Tank
Tank records
c
Initial mean BW, g 3.6 3.8 3.7 3.8 3.7 3.8 3.7 3.8
Cumulative intake, g/sh 10.3 10.5 16.6 17.0 23.4 30.5* 26.3 41.4* 0.20 0.001 0.001 0.001
Daily growth coefcient, %/d
d
0.88 0.87 1.26 1.25 1.55 1.77* 1.59 2.03* 0.008 0.001 0.001 0.001
G:F 1.31 1.32 1.44 1.39 1.46 1.47 1.36 1.40 0.007 0.55 0.001 0.32
Final body composition, % or kJ/g BW
e
Water 72.3 72.4 70.7 70.6 69.5 69.2 69.7 69.3 0.17 0.76 0.31 0.98
Protein 15.4 15.6 16.1 15.8 16.4 16.3 15.9 15.9 0.07 0.54 0.22 0.74
Fat 7.8 7.8 9.1 9.1 9.9 10.3 9.9 10.9 0.05 0.35 0.13 0.82
Energy 7.1 7.0 7.7 7.8 8.1 8.2 8.0 8.3 0.04 0.35 0.25 0.71
Protein and energy utilization for body accretion
Crude protein, g/kg 354 369 324 335 317 318 340 333 1.79 0.15 0.001 0.14
Gross energy, kJ/kg 16.9 17.7 15.6 16.1 15.3 15.3 16.4 16.0 0.08 0.18 0.001 0.14
Individual records nested by tanks
f
Final BW, g 16.8 17.2 27.5 27.1 37.6 48.1* 39.4 60.9* 0.02 0.001 0.001 0.001 0.001
Final length, cm 11.2 11.5* 13.0 13.1* 14.2 15.6* 14.4 16.6* 0.14 0.001 0.001 0.001 0.001
K-factor, g/cm
3g
1.15 1.10* 1.24 1.17* 1.29 1.26* 1.30 1.31* 0.002 0.001 0.001 0.001 0.001
CV, %
h
Final BW 29.2 30.5 22.6 22.9 21.5 18.3 22.0 16.7 0.001 0.002
Final length 9.7 10.3 7.4 7.5 7.0 6.2 7.0 5.5 0.007 0.001
K-factor 7.7 9.2 6.1 7.6 7.0 6.3 7.8 6.5 0.36 0.17
a
Data were obtained on three tanks per treatment, with 150 individuals in each tank for the 50% feeding level, or 100 individuals for the
feeding levels of 70, 100, and 140%. Tank records are means of measurements performed on each tank. Individual records are means and
CV of measurements performed on each individual within each tank. When the line feeding method interaction was signicant (P < 0.05),
separate variance analyses testing the effect of the line within a feeding level were performed. *Indicates when S was different (P < 0.05)
from C at the corresponding feeding level.
b
Probability for the effects of line (L), feeding level (F), the line feeding level (L F) interaction and the tank effect.
c
Analysis of covariance.
d
100(Final BW

Initial BW

)/d.
e
Whole body initial composition: (for S) 76.8% water, 13.9% protein, 5.3% fat, 5.8% energy; (for C) 77.4% water, 13.6% protein, 5.1% fat,
5.5 kJ/g energy.
f
ANOVA.
e
100(BW/fork length
3
).
h
Kruskal-Wallis test separate analysis.
2). The values were the lowest at 100% UDR, and the
highest at 50 and 140% UDR for both lines.
Individual nal BW were different (P < 0.001) be-
tween lines when they were fed 100 and 140% UDR
only (Tables 1 and 2). Regardless of the feeding level,
S was always longer (P < 0.001) than C. Except for sh
fed 140% UDR, the K-factor was always lower (P <
0.001) in S than in C. The apparent discrepancy at
140% UDR could be attributed to the large difference
(P < 0.001) in feed intake and nal BW between the C
and S.
Variability of the nal BW and L was higher in sh
fed 30% than in those fed 10% UDR (Table 1). For
higher feeding levels (Table 2), the variability decreased
with the level of feed intake. In addition, at the highest
feeding levels (100 and 140%UDR), BWand L variabil-
ity were lower in S than in C. Because maximal intake
was higher for S than for C, the CV in weight were
plotted against the observed level of feed restriction
(cumulative intake at a given feeding level/cumulative
intake measured at 140% UDR; Figure 2). This shows
that the variability in the nal weight of S is always
lower than that of C at the same restriction level.
Feed Deprivation Phase
During the feed deprivation phase (Table 3), the rela-
tive loss of BW was not signicantly affected (P > 0.07)
by either the line or the previous feeding level (P >
0.18). The relative daily loss of BW was only slightly
higher in S than in C for a previous feeding level of
140% UDR. Body composition was not affected by the
previous feeding level or by the line. Relative losses of
nutrients (protein loss, 0.97 gkg
1
d
1
for C and S, P
> 0.57; lipid loss, 0.58 and 0.67 gkg
1
d
1
for C and
S, respectively, P> 0.22; energy loss, 53 and 55 kJkg

1
d
1
for C and S, respectively, P > 0.38) also were unaf-
fected by feeding level and line. The K factor values
were much lower at the end of the feed deprivation
phase than at the end of the feeding phase. The line and
the previous feeding level affected body conformation in
a way similar to that at the end of the rst experimental
period. This indicates that there was no interaction
between the effect of 35 d of feed deprivation and the
line or the previous feeding level. Briey, S sh re-
mained slightly leaner than C sh when previously
fed restricted rations, whereas they were fatter than C
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Mambrini et al. 2870
Figure 1. Whole body protein (a) and energy (b) incre-
ments related to intake in selected (S) and control (C)
brown trout lines at the end of the growth phase. Data
at zero intake were obtained at the end of the feed depri-
vation phase. Maintenance requirements correspond to
the x-intercept of the slope.
when previously fed 140% UDR. The tendency for a
higher heterogeneity in BW (P < 0.001) and L (P <
0.007) in C than in S remained after this period of
feed deprivation.
Refeeding Phase
During the refeeding phase (Table 4), sh were fed
140% UDR, and uneaten feed was recovered in each
tank. This indicates that all the groups were fed in
excess; thus, the cumulative feed intake reects maxi-
Figure 2. Coefcients of variation in individual weight
of each group of sh related to feed intake (expressed
relatively to the maximal intake) in selected (S) and con-
trol (C) brown trout lines at the end of the growth phase.
The curves correspond to the t to polynomial second-
order models.
mal voluntary intake. Growth performance was high
in all groups and signicantly better for S than for C.
This was largely explained by the higher cumulative
intake (P < 0.001) of S compared with C. The lower
the previous feeding level, the higher the growth rate
during the refeeding period. There was no clear effect
of the line on G:F. At the end of the refeeding period,
S was still longer than C (P < 0.001). The K-factor was
much higher compared with the values observed at the
end of the feed deprivation phase, but no clear differ-
ences appeared between the lines. With the exception
of the sh previously fed 50% UDR, the CV in BW and
L were lower for S than for C.
Discussion
Control Fish
In C sh, growth rate and G:F increased with the
feeding level until 100% UDR. Cumulative feed intake
was similar between 100 and 140% UDR because of an
increase in uneaten feed. This suggests that, as in other
sh species studied (de la Higuera, 2002), maximal feed
intake of brown trout is tightly regulated. A slight de-
crease in G:F was seen at the 140%UDR(i.e., in overfed
sh). This negative effect of a high feeding level on
G:F has already been observed in other sh species
(Storebakken and Austreng, 1987a,b; Ballestrazzi et
al., 1998; Valente et al., 2001). It has been assumed to
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Selection for growth of brown trout 2871
Table 3. Mean body weight and weight loss of brown trout selected for growth (S) or controls (C) deprived of food
for 35 d and previously fed at 50, 70, 100, and 140% of the usual intake for 116 d
a
Feeding level and line
P-value
b
50% 70% 100% 140%
Measurements C S C S C S C S SEM L F L F Tank
Tank records
c
Initial mean BW, g
d
16.9 17.0 27.6 27.4 37.9 48.3 39.4 61.4
Daily growth coefcient, %/d
e
0.49 0.49 0.51 0.48 0.49 0.48 0.52 0.56 0.009 0.07 0.12 0.39
Final body composition, % or kJ/g BW
Water 72.3 73.6 71.2 72.5 70.5 70.1 70.9 70.5 0.16 0.48 0.44 0.84
Protein 15.9 15.7 16.2 16.1 16.4 16.1 16.4 15.6 0.65 0.45 0.64 0.90
Fat 8.5 7.5 9.3 8.3 9.7 10.3 9.5 10.7 0.03 0.27 0.45 0.73
Energy 7.3 6.7 7.6 7.2 7.9 8.1 7.8 8.1 0.06 0.37 0.63 0.73
Individual records nested by tanks
f
Final BW, g 13.8 14.0 23.1 23.2 32.5 42.1* 33.6 53.0* 0.02 0.001 0.001 0.001 0.001
Final length, cm 11.2 11.4* 13.0 13.2* 14.4 15.8* 14.5 16.9* 0.14 0.001 0.001 0.001 0.001
K-factor, g/cm
3g
0.94 0.90* 1.03 0.98* 1.06 1.05 1.08 1.09* 0.002 0.001 0.001 0.001 0.002
CV, %
h
Final BW 32.5 33.7 25.8 25.2 22.6 19.0 22.5 18.1 0.39 0.001
Final length 9.9 1.9 8.2 8.0 7.2 6.6 7.5 6.0 0.40 0.001
K-factor 1.9 1.9 7.7 7.8 5.9 6.2 5.8 6.2 0.64 0.002
a
Data were obtained on three tanks per treatment, with 150 individuals in each tank for the 50% feeding level, or 100 individuals for the
feeding levels of 70, 100, and 140%. Tank records are means of measurements performed on each tank. Individual records are means and
CV of measurements performed on each individual within each tank. When the line feeding method interaction was signicant (P < 0.05),
separate variance analyses testing the effect of the line within a feeding level were performed. *Indicates when S was different (P < 0.05)
from C at the corresponding feeding level.
b
Probability for the effects of line (L), previous feeding level (F), the line previous feeding level (L F) interaction and the tank effect.
c
Analysis of covariance.
d
Initial BW differed from the nal BW indicated at the end of the growth phase (see Table 1) because 10 sh were slaughtered between
the two experimental phases.
e
100(Final BW

Initial BW

)/d.
f
ANOVA.
g
100(BW/fork length
3
).
h
Kruskal-Wallis test separate analysis.
result from increased energy expenditure, namely a
higher heat increment of feeding to sustain protein and
fat deposition(Storebakkenet al., 1991). Another expla-
nation is that it is difcult to assess with accuracy the
amount of uneaten feed in water running out of the
tank when feed is distributed in excess. As discussed
further, the amounts of uneaten feed were much lower
for selected sh fed 100 and 140% UDR than for the
controls, whereas the G:F were similar among the two
lines, which is in favor of a negative effect of high feed-
ing levels on feed efciency. Indeed, dietary protein and
energy use efciencies were negatively affected when
sh were fed in excess.
A negative relationship between feed intake and BW
heterogeneity was observed. It is well known that in
salmonids, when the access to food is qualitatively or
quantitatively restricted at the group level, the interin-
dividual variability of feed intake, and thus variability
in individual growth performance, is increased (McCar-
thy et al., 1992; Jobling and Koskela, 1996; Gelineau
et al., 1998; Kristiansen, 1999). The observed weight
heterogeneity in feed-restricted groups may be ex-
plained by individual intake heterogeneity. Other re-
sults obtained in the current study support this as-
sumption. At the end of the feed deprivation phase, BW
and length variabilities were similar to those observed
at the end of the feeding period. When the sh were
refed, the heterogeneity of the groups previously re-
stricted was largely reduced, whereas it remained simi-
lar for the groups previously unrestricted. One might
argue that the variability in individual intake is linked,
at least in salmonids, to increased competition for food
when sh are restricted (Davis and Olla, 1987). How-
ever, the share of food may depend on the strength of
social interactions. They seem to play a larger role in
brown trout than in rainbow trout (Kristiansen, 1999).
Increased feed intake led to a carcass fat concentra-
tion increase, and this is also reected by a K-factor
increase. At the end of the feed-deprivation phase, the
K-factor was largely diminished and sh have lost
about the same relative BW (approximately 16%), re-
gardless of the previous feeding level. In addition, there
was no effect of the previous feeding level on the extent
of lipid and energy losses. This is in line with the fact
that in our experiment, there was no link between the
carcass fat concentration at the beginning of the feed-
deprivation phase and the extent of weight loss. These
results are surprising because during fasting, brown
trout are knownto mobilize inpriority their perivisceral
fat (Navarro et al., 1992). One might suggest that in the
present experiment, the length of the feed deprivation
phase was too short to observe any effect of fattening
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Mambrini et al. 2872
Table 4. Growth and feed intake of brown trout selected for growth (S) or controls (C) fed at 140% of the usual intake
(as-fed basis) for 47 d after an experimental phase of food deprivation of 35 d (previous feeding level refers to the
situation before feed deprivation)
a
Feeding level and line
P-value
b
50% 70% 100% 140%
Measurements C S C S C S C S SEM L F L F Tank
Tank records
c
Initial mean BW, g
d
13.8 14.0 23.1 23.2 32.5 42.1 33.6 53.0
Cumulative intake, g/sh 21.7 29.5* 27.2 39.5* 28.6 44.2* 27.4 47.5* 0.17 0.001 0.001 0.003
Daily growth coefcient, %/d
e
2.40 2.85* 2.16 2.82* 2.11 2.60 2.00 2.52 0.014 0.001 0.04 0.017
G:F 1.51 1.43 1.37 1.37 1.53 1.51 1.52 1.54 0.013 0.04 0.005 0.28
Individual records nested by tanks
f
Final BW, g 46.0 55.5* 60.4 76.6* 76.0 108.4* 75.1 125.8* 0.03 0.001 0.001 0.001 0.001
Final length, cm 14.8 15.8* 16.4 17.7* 17.7 20.0* 17.7 21.0* 0.41 0.001 0.001 0.001 0.001
K-factor, g/cm
3g
1.38 1.37* 1.35 1.38* 1.35 1.34 1.32 1.35* 0.002 0.001 0.03 0.001 0.82
CV, %
h
Final BW 26.4 28.1 27.2 22.9 25.9 20.9 24.7 19.2 0.015 0.05
Final length 8.9 9.8 8.9 7.5 8.6 7.2 8.3 6.5 0.08 0.02
K-factor 6.0 6.4 5.3 6.0 6.3 5.7 5.9 6.1 0.25 0.51
a
Data were obtained on three tanks per treatment, with 150 individuals in each tank for the 50% feeding level, or 100 individuals for the
feeding levels of 70, 100, and 140%. Tank records are means of measurements performed on each tank. Individual records are means and
CV of measurements performed on each individual within each tank. When the line feeding method interaction was signicant (P < 0.05),
separate variance analyses testing the effect of the line within a feeding level were performed. *Indicates when S was different (P < 0.05)
from C at the corresponding feeding level.
b
Probability for the effects of line (L), previous feeding level (F), the line previous feeding level (L F) interaction and the tank effect.
c
Analysis of covariance.
d
Initial BW differed from the nal BW indicated at the end of the growth phase (see Table 1) because 10 sh were slaughtered between
the two experimental phases.
e
100(Final BW

Initial BW

)/d.
f
ANOVA.
g
100(BW/fork length
3
).
h
Kruskal-Wallis test separate analysis.
on weight loss. Indeed, brown trout are still able to
mobilize the perivisceral fat after 50 d of feed depriva-
tion (Navarro et al., 1992). These losses were in the
same range as values reported for other salmonid spe-
cies, as were the maintenance requirements (Cho and
Bureau, 1995). Concerning the requirements for
growth, we were unable to compare our results with
published data because they were obtained on sh of
different sizes andreared at different temperatures (Ar-
zel et al., 1992). They seemlower than the recommenda-
tions given for rainbow trout (NRC, 1993). There are
slight differences in the way brown trout and rainbow
trout utilize nutrients for growth (Arzel et al., 1992,
1994). Our results indicate that brown trout may be
more efcient than rainbow trout.
Growth rates exhibited during the refeeding phase
were much higher than those observed during the feed-
ing phase. Compensatory growth capacities have been
demonstrated in several salmonid species (Dobson and
Holmes, 1984; Jobling et al., 1994; Jobling and Koskela,
1996), and our results indicate that it is also the case for
brown trout. In our experiment, as is usually observed,
compensatory growth was achieved by a burst in both
feed intake and G:F. In addition, the extent to which
feed intake relative to BW increased was correlated
to the strength of the feed restriction before the feed
deprivation phase. Voluntary feed intake of sh may
be affected by their past nutritional history, in particu-
lar the previous level of feed restriction (Boujard et al.,
2000) and the duration of feed deprivation (Hayward
et al., 1997). Taken together, these data show that in
brown trout, feed intake is a key factor for the compen-
satory growth phenomenon.
Selected Fish
This study conrms that the main factor affected by
our selection procedure for increased body length is
feed intake. In selected lines, feed refusals were only
observed at 140%UDR. At this feeding level, sh exhib-
ited their best growth potential and reached a BW 55%
higher than that of the control at the end of the feeding
phase. This is in line with the values of the genetic gain
expected at this age considering the average genetic
gain obtained with this selection procedure (Sanchez
et al., 2001; Vandeputte et al., 2002). This is also in
agreement with the results obtained with other selec-
tion protocols for growth in salmonids (Gjedrem, 1998).
At 100% UDR, selected sh were slightly restricted (no
uneaten feed recovered, lower growth rates than when
fed 140% UDR), showing that the level of voluntary
feed intake was higher than in the control line. During
the refeeding phase, the feed intake capacities of S were
always higher than for C, and as observed in controls,
intake relative to BWwas all the higher as the previous
restriction level was high, even though the feed intake
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Selection for growth of brown trout 2873
capacities were always higher for S than for C. This
high intake capacity appears to be a feature of the S
line, remaining evident even after a period of feed re-
striction.
Whenfeed intake was restricted, the S lines exhibited
the same growth rate as the C line. The G:F remained
comparable among the lines regardless of the feeding
level, conrming on a larger scale our previous results
(Sanchez et al., 2001). The main response correlated to
this selection procedure was an increased intake capac-
ity. In higher vertebrates, most of the heritable varia-
tion in BW is associated with differences in feed intake
(Rauw et al., 1998). This also seems to be the case
in sh taking into account estimates of heritabilities,
which are not signicantly different from zero for feed
efciency (Kinghorn, 1983) and range between 0.15 and
0.40 for feed intake (Kinghorn, 1983; Gjoen et al., 1991).
Salmon selected with a familial procedure when com-
pared with wild sh exhibit increases in both daily feed
consumption and feed efciency (Smith et al., 1988;
Thodesen et al., 1999), but in these studies, the results
merge the gains due to both genetics and domestication.
The lack of variability in feed efciency is in line
withthe constancy of the body compositionand nutrient
retention among the lines. In addition, both lines seem
to have the same needs for protein and energy gains,
at least for the range of weights tested in the current
study. Moreover, the maintenance needs were similar
among the lines. This is also illustrated by the fact that
selected and control sh lost the same relative weight
and the same amount of protein, lipid, and energy dur-
ing the feed-deprivation phase. Our selection procedure
affected neither the nutrient requirements nor nutrient
use efciency. The increase in feed intake of the selected
line in the current study is therefore disconnected from
modications of maintenance and growth require-
ments. In broilers, selection for increased BW was
shown to damage the hypothalamic satiety mechanism,
not to diminish hunger drive, and to lead to overeating
(Burkhart et al., 1983; Denbow et al., 1986). Broilers
are able to consume more than required until reaching
the highest limit of their gastrointestinal capacity (Bar-
bato et al., 1984) because of a higher rate of food gastro-
intestinal transit or because of increased digestion pro-
cesses (Dunnington and Siegel, 1995). Such parameters
could be specically studied in our lines; however, their
inuence on feed intake is still largely unknown be-
cause in sh, the mechanisms governing feed intake
regulationare marginally understood. Lines involvedin
this study might be good models for such investigations.
Intake in sh is measured on groups and, as exempli-
ed in the current study, the food sharing and individ-
ual intake are affected by feeding level, whereas social
interactions may inuence individual intake. It may be
that selection has affected the overall behavior. The
interindividual variability of BW was lower in S than
in C, regardless of the restriction level. This points to
less competition for food in S sh. However, the de-
crease in the phenotypic variability of the selected trait
has been observed in poultry after several generations
of selection (Kawahara et al., 1974; Metodiev and
Drbohlav, 1998). In our case, it does not seem to be
linked to the genetic variability, which, based on enzy-
matic and microsatellite markers, was not affected by
the selection procedure (B. Chevassus, unpublished re-
sults). Rather, the lower variability of individual BW
of the selected line seems to be the result of decreased
sensitivity to environmental factors. This may have pos-
itive implications in production because sh have to be
re-sorted regularly due to their high interindividual
BW heterogeneity.
The rearing management during selectionmay partly
explain why selection for growth mainly increased in-
take capacities. During the selection process, sh were
always fed in excess. Mice selected for growth under ad
libitum feeding conditions exhibited increased intake
capacities, whereas under feed restriction conditions,
selection for growth decreased their appetite (Hetzel
and Nicholas, 1978). The other important factor that
may have inuenced the results is that sh were se-
lected based on length, and not weight. These two vari-
ables are closely linked, as indicated by the relative
constancy of the K-factor in salmonids, at least when
they are in the fast growing phase. Heavy but fatty
sh might not have been retained during the selection
procedure, which may explain the relative constancy of
body composition. It has beendemonstrated in pigs that
a greater growth rate is achieved when animals are
selected for lean growth efciency (Chen et al., 2003;
Fabian et al., 2003). Our results show that it may be
difcult to improve metabolic efciency with a selection
for growth in sh. In higher vertebrates, the strategy
was to select on residual feed intake (individual devia-
tions from the regression of feed intake on BW gains).
This selection procedure implies both that individual
intake is accurately measured and that growth models
have been correctly established (Kennedy et al., 1993).
These conditions are still not fullled in sh. Individual
feed intake cannot be measured in a continuous manner
(Jobling et al., 2001). Growth models are only available
for a fewspecies. They are not commonly used and must
integrate the constant improvements of the rearing per-
formance observed in recently domesticated species.
Then, a specic selection procedure is needed and indi-
rect criteria, such as lean deposition, may be con-
sidered.
Implications
The main correlated response to our selection proce-
dure for increased body length was an increase in feed
intake capacity. Requirements for growth and mainte-
nance were identical betweenselected and control lines.
Thus, selected sh will only exhibit their full growth
potential when their appetite is satised. Fish selected
for growth require a higher feeding allowance. Whereas
this will not reduce feed costs, it will shorten rearing
duration, with no increase in body fat content, at least
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Mambrini et al. 2874
within the range of weight tested. Lower body weight
variability in the selected line may decrease the fre-
quency with whichsh need to be re-sorted into similar-
size groups. The effect of the selection procedure on
feed intake capacity may result froma more even share
of food due to behavioral differences at the group level
and to a higher appetite at the individual level. These
lines constitute good models for gaining better insight
into the physiological basis, as well as some genetic
determinants, of feed intake regulation in sh.
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