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Response of growth-selected brown trout (Salmo trutta) to challenging feeding conditions
Aquaculture 252 (2006) 429 – 440 www.elsevier.com/locate/aqua-online
Response of growth-selected brown trout (Salmo trutta) to challenging feeding conditions Muriel Mambrini a,*, Laurent Labbe´ b, Faramalala Randriamanantsoa a, Thierry Boujard a a
INRA, Laboratoire de ge´ne´tique des Poissons, 78352 Jouy en Josas Cedex, France b Station expe´rimentale mixte Inra-Ifremer, BP17, 29450 Sizun, France
Received 18 May 2005; received in revised form 6 July 2005; accepted 7 July 2005
Abstract Correlated responses for feed intake, feed utilization and growth were measured in brown trout from lines after five generations of selection on fork length (S) and in control (C). Groups of fish with the same initial weight (5 g) were constituted (500 S, 500 C, 250 S + 250 C) and were either fed ad libitum using self-feeders or were food restricted (75% ad libitum) for 87 days (2 feeding levels 3 replicates for S, C, and mixed groups). After 34 days of food deprivation, all groups were re-fed ad libitum using self-feeders for 41 days. Greater growth of S compared to C was related to higher feed intake (line effect on cumulative intake, P = 0.0041), but feed efficiency was similar (1.4 on average), irrespective of feeding level. During the food deprivation phase, S lost more weight than C ( P = 0.0024). When fish from the two lines were mixed they exhibited the same growth when fed ad libitum; when food was restricted, S grew faster than C ( P = 0.0190), suggesting that S may consume a higher proportion of the available food than C. The daily profile of feeding activity was comparable among the lines. Within groups, weight variation (assessed as CV) was lower in S than in C at all the experimental phases, suggesting that food sharing may be more homogeneous in S than in C. S fish were more slender than C, had lower hepatosomatic and viscerosomatic indices and a higher dressing %. The robustness of the response correlated to our selection procedure is discussed. D 2005 Elsevier B.V. All rights reserved. Keywords: Fish; Selection; Growth; Feed intake; Feed efficiency; Correlated response
1. Introduction
* Corresponding author. Tel.: +33 1 3465 2705; fax: +33 1 3465 2390. E-mail address: [email protected] (M. Mambrini). 0044-8486/$ - see front matter D 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.aquaculture.2005.07.001
Genetic selection for growth improvement of farmed fish has led to high genetic gains (10–20% per generation, Gjedrem, 1998), without affecting genetic variability (Hershberger et al., 1990; Chevassus et al., 2004). Correlated response that accompa-
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nies this selection is generally increased feed intake (Smith et al., 1988; Gjedrem, 1992; Thodesen et al., 1999) and sometimes, improved feed efficiency (Kinghorn, 1983a). This is comparable to what is described in higher vertebrates, even if in fish, one should pay great attention to the influence of environmental factors and dominance effects (Kestemont and Baras, 2001), as well as to the domestication status (Gjedrem, 1979), on growth performance. A genetic individual selection program for brown trout has been underway in France since 1987 (Chevassus et al., 1992), taking into account the environmental and dominance effects. The protocol has been applied to two base populations, held in two experimental fish farms. For each population, a control line has been maintained under the same rearing conditions, and thus submitted to the same domestication influences. The correlated responses to growth enhancement have been measured on one of the two selected lines using a protocol to assess feed intake and feed efficiency (Sanchez et al., 2001). The better growth of the selected population was achieved by higher feed intake; feed efficiency did not differ from that of the control (Sanchez et al., 2001). The selected fish demonstrated a more pronounced feeding rhythm and less individual growth variations than controls (Mambrini et al., 2004a). This may be driven by differences in social interactions (Robinson and Doyle, 1990; Jobling et al., 2001) and by differences in appetite. Further, the requirements for maintenance appeared comparable among the selected and control lines (Mambrini et al., 2004b), as also suggested by the lack of difference in weight loss during feed deprivation (Mambrini et al., 2004a). The objective of the present study is to measure the response to selection of the second selected population of brown trout to assess the robustness of the selection procedure. We used an improved protocol, where we measured feed intake, feeding rhythm and growth simultaneously. We added the challenging condition of rearing selected and control lines together to determine for possible differences related to a situation involving social interaction. In addition we analyzed the variations in liver mass because in higher vertebrates they indicate differences in maintenance and energy requirements (Webster, 1989; Kgwatalala and Nielsen, 2004).
2. Material and methods 2.1. Animals The base population of brown trout (Salmo trutta) was a mixture of five strains from different regions of France, chosen for good growth (Chevassus et al., 1992). Genetic selection involved an improved individual selection process (Chevassus et al., 2004), and a control line (C) was maintained under the same rearing conditions at the experimental fish farm (Gournay, France). The selection criterion was fork length (Chevassus et al., 1992). With a selection pressure of about 5% (proportion of fish selected), the improvement in weight gain for one year olds was about 6% per generation for the selected line (S) compared to C (M. Vandeputte, pers. com). The S and C fish used in the present study were offspring from the fifth generation, and they were produced by in vitro fertilization at the Gournay experimental fish farm. Fifteen females were crossed with 15 males for both lines. To obtain selected and control offspring of similar weight (approximately 5 g) at the beginning of the experiment, we fertilized C 12 days before S. The eggs were incubated at the Gournay fish farm until the eyed stage (temperature 11 F 2 8C; mean F SD). Eggs were then transferred to the SEMII fish farm (Britanny, France), where they were incubated at the same temperature. After hatching, the fish were reared in two tanks per line supplied with flow through 11 8C water. Fish were fed commercial dry feed (Biomar Ecolife 18, 51% protein and 18% lipid according to the manufacturer) provided in excess by automatic feeders, delivering food 12 h a day until the beginning of the experiment. The day before starting the experiment, body weights (BW) and lengths (fork length: L) were measured for representative samples of the C and S populations (500 individuals per tank): 5.1 F 0.9 g and 7.5 F 0.5 cm for C and 4.7 F 0.9 g and 7.4 F 0.5 cm for S. At the start of the experiment, six groups of 500 individuals per line and six mixed groups of 250 C and 250 S fish were established. During handling, the fish were lightly anaesthetized (2-phenoxy-ethanol, 0.2 ml l 1). In the mixed group, the adipose fin of S was cut to aid in recognition. The fish were reared in 2 m3 tanks with flow-through water from Lake Drennec
M. Mambrini et al. / Aquaculture 252 (2006) 429–440
(temperature 9–18 8C, water flow 4 m3 h 1, O2 saturated, NH4 b 0.01 mg l 1, pH = 6.7). The first experimental phase, referred to as the feeding phase, lasted for 87 days. During this phase, the fish in the S, C and mixed groups were fed either ad libitum or restricted to 75% of the expected ad libitum level for C (calculated using bEcureuilQ software developed on the SEMII fish farm). The two feeding levels were randomly assigned to 3 tanks of fish for each group. Feed was made available during the light phase (between 0430–2200 hours at the beginning of the experiment and 0530–2200 hours at the end) from computercontrolled self-feeders (Imetronic Sarl, France). Trigger activations were recorded for the S and C groups that were reared separately and fed ad libitum. Fish were rewarded with 2 g of food (Biomar Bioptimal, 1.5 mm, 53% protein and 16% lipid) for each demand. In the restricted feeding tanks, demands were rewarded until the prescribed ration was dispensed. Feed waste was collected in a sediment trap at the outlet of each tank and weighed for calculation of feed intake. Over the first week, uneaten feed and feces were separated by hand, and the respective proportions of each were assessed for each tank. The moisture content of the uneaten feed was also measured and taken into account when making calculations.
2.2. Measurements and calculations At the end of each phase (days 87, 121, and 162), all fish were counted (n i and n f for the initial and final number of fish, respectively) and weighed by tank (W i and W f, for initial and final weights per tank, respectively) after 1 day of fasting to ensure empty gut. In addition, fish were weighed by tank at 21 days intervals during the feeding and re-feeding phases (days 20, 41, and 61 for the feeding phase and day 142 for the re-feeding phase) and the total numbers of fish estimated, taking into account mortality which was recorded daily. For each phase, food consumption, growth and food utilization were assessed using the following: Cumulative intake (g fish feed waste) n f 1
a a
S
C mixed 75
S 100
S mixed C mixed
a a ab
75 aa b b
25
b 50 a 25
bbb Food deprivation
Food deprivation 0 0
) = (distributed food
C b b
S mixed
50
1
Restricted groups
125
C
100
IBW (g)
After the feeding phase, a 34 days feed deprivation was imposed. In the last phase, referred to as the re-feeding phase, all fish were fed ad libitum with self-feeders for 41 days. The reward level was set at 4 g (Biomar Aqua 17, 3 mm, 42% protein and 22% lipid). Feed demands were recorded for the S and C groups reared separately. Feed waste was assessed as during the feeding phase.
Unrestricted groups
125
431
20 40 60 80 100 120 140 160 180 Time (days)
0
0
20 40 60 80 100 120 140 160 180 Time (days)
Fig. 1. Evolution of the mean individual body weight (IBW, g) of brown trout selected for growth (S) or control (C) and held separated or mixed. Groups were fed unrestricted by self-feeder (left) or restricted by automatic feeders (right) until day 87 and feed-deprived until day 121. All groups were fed by self-feeders during the re-feeding phase (until day 161) that followed the phase of food deprivation. Vertical bars indicate one S.D. (a, b) represent significantly different ( P b 0.05) mean body weights on a given day.
RSD
During the re-feeding phase all groups were fed ad libitum with self-feeders, the feeding level refers to the feeding phase only. For each phase, means with different superscripts are significantly different ( P b 0.05), when an interaction was significant, DGC differences were tested after separate analyses of variance. a,b indicate significant differences between lines, x,y between feeding levels and i,j between single and mixed groups.
Feeding phase Feed deprivation phase Re-feeding phase
2.40ax 0.83axi 2.93a S Line
C
2.08bxi 0.64bx 2.74b
S
2.36ax 0.63xj 3.08a
C
1.99bxj 0.59x 2.65b
S
1.43yi 0.55y 3.49
C
1.37yi 0.54yi 3.22
S
1.58ayj 0.44y 3.12a
C
1.32byj 0.05 b0.0001 b0.0001 0.7550 0.0013 0.0163 0.0220 0.1354 0.39yj 0.05 0.0024 b0.0001 b0.0001 0.0584 0.1602 0.8267 0.0283 2.63b 0.29 0.0190 0.0619 0.1116 0.7855 0.4047 0.0696 0.9534
F*M L*M L*F Statistical analysis ( P)
Line (L) Feeding Mixing level (F) (M) Mixed
Restricted
Single Mixed
Ad libitum
Statistical analyses were based on a completely random experimental design. Variables that were independent of initial body weight (DGC, feed intake, cumulative intake and FE during the feeding phase) were compared using analysis of variance that included the effects of line, feeding level, line-mixing and the interactions between these three factors. To analyze feed intake during the re-feeding phase, the mean weight at the beginning of the re-feeding phase was included in the model as a covariate. The tanks were the experimental unit (three replicates per treatment). Individual body weight and length data did not follow a normal distribution. Individual weights
Single
2.3. Statistical analysis
Feeding level
At the end of each phase (feeding, feed deprivation, and re-feeding phases), individual weights (to nearest g) and fork lengths (to nearest mm) were recorded for 100 fish per tank for S and C reared separately and for 100 fish per line and per tank for the mixed groups. Coefficients of variation for weight and length were calculated for each line within each tank (CV: 100 Standard deviation mean 1). Twenty fish per line and per tank in the S and C groups were killed (large dose of 2-phenoxyethanol) and eviscerated. The weights (g) of the liver and viscera minus the liver were recorded and the hepatosomatic index (HSI: 100 liver weight body weight 1), viscerosomatic index (VSI: 100 weight of the viscera without liver body weight 1) and dressing percentage (100 eviscerated weight body body weight 1) calculated. Feeding demands, recorded for the lines reared separately and fed ad libitum, were summed over 30 min. These were then expressed as percent of the total feeding demands over the day and averaged for successive periods covering days 20–40, 42–60, and 62– 86 for the feeding phase and days 122–141 and 143– 161 for the re-feeding phase.
Rearing conditions
Feed intake (%) = 100 (distributed food feed waste) W i 1 Daily growth coefficient (DGC, % d 1) = 100 ((W fn f 1)1/3 (W in i 1)1/3) days 1 Feed efficiency (FE) = (W f Wi) (distributed food feed waste) 1
L*F*M
M. Mambrini et al. / Aquaculture 252 (2006) 429–440 Table 1 Mean daily growth coefficients (DGC) and root square deviation (RSD) of groups of brown trout selected for growth (S) or control (C) reared single or mixed
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sample, and lnY˜i is the mean logarithm of the ith sample. The scatter of the absolute deviates was equal, indicating that a parametric test may be applied (Sokal and Braumann, 1980). The coefficients of variation were compared by analysis of variance including the effects of line, feeding level, line-mixing, and the interactions between these three factors. The tanks were the experimental unit (three replicates per treatment). The means of the 20 individual measurements of HSI, VSI, and dressing percentage were averaged for each tank, transformed (arcsinus square root), and compared by analysis of variance that included the effects of line, feeding level, and interactions between the two factors. The tanks were the experimental unit (three replicates per treatment). Feeding demands, adjusted to the onset of the feed delivery, were compared with a repeated measures analysis of variance including the effects of time (days) within the experimental phases. Data from the feeding phase were analyzed and included the effects of period, line, the tank nested into the line effect, and the interactions between these three factors. For the re-feeding phase data, the effects of the previous feeding level and the interaction between the line and previous feeding level were also considered. In this case, the tank effect was nested into the interaction. Probabilities of difference between treatments were generated using the General Linear Model procedure of SAS (1996). When the interaction was significant,
S 70
C
Gain (g/fish)
60 50 40 30 20 10 0 0
10
20
30
40
50
60
70
433
80
Cumulative intake (g/fish)
Fig. 2. Mean individual gain (g) versus individual cumulative intake (g) of juvenile brown trout selected for growth (S) or control (C) for the feeding and re-feeding phases.
were log-transformed before being subjected to an analysis of covariance, with the log-transformed length used as a covariate. The model tested the effect of line, feeding level and line-mixing; the tank effect nested into the interaction of the three factors was considered random and was included in the error term (100 individuals per tank, three replicates per treatment). The coefficients of variation of individual body weight and length were transformed to logarithms and the equality of the absolute deviates in each class was controlled. The absolute deviate was calculated (|lnYij lnY˜i |, where Yij is the jth term in the ith
Table 2 Mean individual cumulative intake (g), feed intake (% initial body weight) and root square deviation (RSD) of groups of brown trout selected for growth (S) or control (C) reared single Feeding level
Ad libitum
Line
S
C
Restricted S
C
RSD
Statistical analysis Line (L)
Feeding level (F)
L*F
Cumulative intake Feeding phase Re-feeding phase*
37.15ax 48.03
29.83bx 37.73
15.27y 41.85
14.85y 34.55
1.60 7.06
0.0041 0.1188
b0.0001 0.5315
0.0074 0.5648
Feed intake Feeding phase Re-feeding phase
1.34x 1.46x
1.27x 1.35x
1.09y 1.98y
1.05y 1.78y
0.05 0.20
0.0886 0.2057
b0.0001 0.0043
0.5441 0.7066
During the re-feeding phase all groups were fed ad libitum with self-feeders, the feeding level refers to the feeding phase only. For each phase, means with different superscripts are significantly different ( P b 0.05), when the line-feeding level interaction was significant, differences were tested after separate analyses of variance. a,b indicate significant differences between lines and x,y between feeding levels. *The cumulative intake during the re-feeding phase was analysed with analysis of covariance with the body weight at the start of the re-feeding phase as a covariate.
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Table 3 Repeated time analysis of variance of the pattern of feeding activity (% demand activity half-hour 1 day 1) of brown trout selected for growth or control fed ad libitum by self-feeder during the feeding phase and the re-feeding phase (3 tanks per treatment) Source of variation
df
Type III SS
Mean square
F
P
Growth period Line Time of day Tank (line) Period * time of day Line * time of day Time of day * tank (line) Period * time of day * line
3 1 30 4 90 30 120 90
0.0681 0.0002 4.1915 0.0273 5.5239 0.3067 0.9992 0.4968
0.0227 0.0002 0.1397 0.0068 0.0614 0.0102 0.0083 0.0055
7.25 0.05 21.54 2.18 9.46 1.58 1.28 0.85
0.0072 0.8239 b0.0001 0.1445 b0.0001 0.0317 0.0462 0.8166
Each feeding phase is divided into two growth periods.
separate analyses of variance were performed to test the effects of the line, the feeding method or the mixing. The means were subsequently compared using Newman and Keul’s test (significance level P b 0.05).
2.4. Ethical note The experiment was conducted in compliance with national legislation on animal care, following procedures stipulated by the French Ministry of Research.
15.0 S C
Demand feeding activity (% . half-hours-1)
12.5
10.0
7.5
5.0
2.5
0.0 genotype effect period effect 0
2
4 6 8 10 Time (hours after onset of food delivery)
12
14
16
18
Fig. 3. Pattern of demand feeding activity profile in brown trout selected for growth (S) or control (C) and fed using self-feeders during the feeding and the re-feeding phases. Horizontal bars below the histogram indicate when line or period effects are significant ( P b 0.05). Vertical bars indicate one S.D.
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3.2. Feed intake and feeding activity Feed efficiency was on average 1.41 during the feeding phase and 1.39 during the re-feeding phase, and was neither affected by line (Two-way ANOVA, n = 24, P = 0.9214) nor by feeding level (Two-way ANOVA on data from the feeding phase, n = 12,
Fig. 4. Daily cumulative feeding activity in brown trout selected for growth (S) or control (C) and fed using self-feeders. (a) feeding phase, (b) beginning of the re-feeding phase (days 125–138), (c) end of the re-feeding phase (days 148–161). During the re-feeding phase (b, c), the feeding level refers to the feeding conditions during the feeding phase (a). Vertical bars indicate one S.D.
Cumulative feeding activity (% half-hours-1)
At the end of the experiment, the survival rate ranged from 96% to 99% depending on tank, with no line or treatment effects. In fish fed ad libitum individual body weight was affected by line in both single and mixed groups, whereas in the restricted groups, a line influence was only seen when the fish were held in mixed groups (Fig. 1). During the feeding phase, the daily growth coefficient (Table 1) of S and C held singly differed, being higher in S than in C when fish were fed ad libitum. Mixing the lines had a detrimental effect on the growth of C. During the food deprivation phase, the loss of weight, indicated by a negative DGC, was related to growth during the feeding period: the higher the growth rate during the feeding phase, the higher the loss of weight during the feed deprivation phase (n = 22, r = 0.64, P b 0.0001). The relative loss of weight was higher in S than in C. During the refeeding phase, DGC increased by 20–30% in comparison to the feeding phase when fish had previously been fed ad libitum, and by 100–135% when fish had previously been restricted. The growth of S was higher than that of C, irrespective of mixing status or previous feeding regime. There was no relationship between growth during the re-feeding phase and the relative loss of weight during the feed deprivation phase, or between growth during the re-feeding phase and DGC in the feeding phase.
100
Cumulative feeding activity (% half-hours-1)
3.1. Growth performance
100
Cumulative feeding activity (% half-hours-1)
3. Results
100
a
90 80 70 60 50 40 30 20
S C
10 0
0
4
8
12
16
20
24
b
90 80 70 60 50 40 30
S - previously ad libitum S - previously restricted C - previously ad libitum C - previously restricted
20 10 0
0
4
8
12
16
20
24
c
90 80 70 60 50 40 30
S - previously ad libitum S - previously restricted C - previously ad libitum C - previously restricted
20 10 0
0
4
8
12 Time (hours)
16
20
24
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apparent difference seemed to occur at the beginning of the re-feeding phase, where S fish that had previously been restricted tended to eat more in the early morning than did both the S fish that had previously been fed ad libitum or the C fish. However, a two-way ANOVA to compare cumulative intake after 4 h of feeding at the beginning and at the end of the refeeding phase (Fig. 4b, c) isolated a period effect (n = 24, P = 0.0066) but not any line or previous feeding level effect (n = 24, P = 0.5508).
P = 0.9364). Growth differences between lines were fully explained by differences in feed intake, as illustrated by the relationship between gain and cumulative intake that is not affected by the line (Fig. 2). In the groups where lines were held singly, cumulative intake (g) was higher for S fed ad libitum during the feeding phase than for C (Table 2). In both lines, feed intake during the re-feeding phase was higher for fish that had previously been restricted. Period and time of day had a significant effect on feeding activity, with a strong interaction between these two variables, but no effect of line was observed (Table 3). Because of the lack of interaction between lines, period and time of the day (Table 3), the daily feeding activity is illustrated by plotting the mean daily demands of both lines over the experiment (Fig. 3). There were few nocturnal demands and a peak of feeding activity was seen during the first 2 h of light. This peak represented ca. 30% of total daily demands. During the rest of the day, the hourly feed demand was ca. 5% of the daily total. Feeding was similar for the two lines, the only significant difference being that, in the early afternoon, relative activity was higher for C than S. Cumulative feeding activity profiles were compared for the feeding phase, and at the beginning and end of the re-feeding phase (Fig. 4): profiles were similar for the two lines. The only
3.3. Fish features The HSI, VSI, and dressing % were affected by line (Table 4). The HSI was lower for S than C at the end of the feeding and re-feeding phases, but did not differ between lines at the end of the feed deprivation phase. The VSI was lower for S than C at every experimental phase, and the dressing % was always higher for S than C. During the feeding phase, restricted fish had a lower HSI but VSI did not differ between treatments. Feed deprivation induced a reduction in HSI and VSI in both lines, and gave a higher dressing %, which was higher for S than C. During the re-feeding phase, HSI, VSI and dressing % returned to values similar to those observed before the feed deprivation phase, but the previous feeding level
Table 4 Mean individual hepatosomatic index (%), viscerosomatic index (%), dressing (%) and root square deviation (RSD) of groups of brown trout selected for growth (S) or control (C) reared single Feeding level
Ad libitum
Line
S
Restricted C
S
Statistical analysis C
RSD
Line (L)
Feeding level (F)
L*F
Hepatosomatic index Feeding phase Feed deprivation phase Re-feeding phase
1.52bx 1.03 1.26b
1.65ax 0.93 1.47a
1.36by 0.99 1.40b
1.47ay 1.05 1.61a
0.06 0.14 0.12
0.0014 0.8871 0.0173
0.0018 0.5917 0.0790
0.2563 0.3810 0.9963
Viscerosomatic index Feeding phase Feed deprivation phase Re-feeding phase
9.51b 5.33bx 8.74by
10.59a 6.37ax 9.51a
8.93b 5.00by 9.83bx
10.38a 5.89ay 10.76a
0.45 0.22 0.37
0.0061 0.0001 0.0112
0.1431 0.0073 0.0015
0.6393 0.9811 0.7452
89.95b 91.31b 89.42y
0.45 0.29 0.48
0.0061 0.0006 0.0879
0.1431 0.6097 0.0094
0.6393 0.1680 0.1239
Dressing Feeding phase Feed deprivation phase Re-feeding phase
90.49a 92.30a 90.89x
89.41b 91.63b 89.90x
90.78a 92.47a 89.48y
During the re-feeding phase all groups were fed ad libitum with self-feeders, the feeding level refers to the feeding phase only. For each phase, means with different superscripts are significantly different ( P b 0.05), when the line-feeding level interaction was significant, differences were tested after separate analyses of variance. a,b indicate significant differences between lines and x,y between feeding levels.
0.3942 0.2411 0.7260 0.7160 0.8240 0.0001 0.0530 2.5 27.4b 22.4a 28.5b 20.0a 24.1b 20.2a 25.2b 19.4a
During the re-feeding phase all groups were fed ad libitum with self-feeders, the feeding level refers to the feeding phase only. For each phase, means with different superscripts are significantly different ( P b 0.05), when an interaction was significant, differences were tested after separate analyses of variance. a,b indicate significant differences between lines, x,y between feeding levels and i,j between single and mixed groups.
0.5022 0.3369 0.9657 0.3643 0.7589 0.4751 0.2598 0.0844 0.5655 0.4025 0.0008 0.0017 0.0015 0.1530 2.6 2.7 29.1by 29.4b 21.3ay 21.4a 27.5by 26.0b 24.1ay 24.0a 22.8bx 23.7b 18.7ax 20.7a 23.5bx 27.4b 19.5ax 21.8a
CV of weight Feeding phase Feed deprivation phase Re-feeding phase
0.2439 0.0063 0.9215
0.3396 0.9385 0.0330 0.6687
0.3662 0.8534
Weight / length Feeding phase 57.4ax / 16.2 48.1bx / 15.1 55.2a / 16.1 44.2b / 14.5 26.3y / 12.8 26.5y / 12.6 30.3a / 13.4 25.5b / 12.3 2.0 Feed deprivation 45.3ax / 16.2 41.2bx / 15.3 46.8ax / 16.3 38.0bx / 15.0 22.9y / 13.0 22.9y / 12.8 26.1ay / 13.5 20.7by / 12.3 1.8 phase Re-feeding phase 113.8 / 20.8 96.1 / 19.3 115.8a / 20.7 89.0b / 18.6 79.0 / 18.2 71.0 / 17.3 77.0a / 18.1 57.9b / 16.3 1.3
RSD C S C S C S S Line
C Single Rearing conditions
b0.0001 0.0050 b0.0001 0.0224
0.3069 0.0053 0.8979 0.9837 0.0956 0.6821 0.4329 0.4408
L*F*M F*M L*M Feeding Mixing L * F level (F) (M)
Statistical analysis
Line (L) Mixed Single Mixed
Restricted Ad libitum Feeding level
Table 5 Mean individual weight (g) / length (cm), CV of weight and root square deviation (RSD) of groups of brown trout selected for growth (S) or control (C) reared single or mixed and results of the analysis of variance with length as a covariate
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was found to significantly affect both the VSI and the dressing %. Individual weights were analyzed with the length as covariate so that we characterize the treatments effects on body shape (Table 5). At the end of the feeding phase, S fish were more slender than C fish, and restricting the amount of food rendered both lines slender. Fish features and the specific effect of the line and previous feeding level were conserved during the feed deprivation phase. At the end of the re-feeding phase, S fish were still more slender than C in all the groups; previous feeding level did not have any impact nor did mixing of lines. The CV for weight was lower in S than C throughout the experiment (Table 5). There was an effect of feeding level, which was highly significant during the feeding phase, with higher CVs in feed restricted groups, regardless of line. Mixing had no effect on CV for either line.
4. Discussion The body weight of S was nearly 25% higher than that of C when fed ad libitum, and the daily growth coefficient was 12% to 17% higher for S than C. Although the genetic gain was lower than that reported for another line of brown trout selected with the same procedure (Mambrini et al., 2004a,b), the results conform to the 6% genetic gain per generation usually measured on the line used in the present experiment (M. Vandeputte, pers. com.). Thus, significant gains can be achieved using the selection procedure employed, but the extent of the gain may vary with the characteristics of the basal population and rearing conditions during the selection process. Better growth of S was only seen when the fish were fed ad libitum, feed efficiency being neither affected by line nor feeding regime. The better growth of the selected fish was therefore explained by their higher feed intake. A lack of difference in feed efficiency between S and C, was also seen in another line of brown trout selected according to the same procedure (Mambrini et al., 2004a,b), and one might wonder if this correlated response is specific to the selection procedure used or if the genetic correlation between feed efficiency and growth is poor in fish. In salmonids, feed
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intake capacity has higher heritability (0.15 F 0.30, Gjoen et al., 1991; 0.41 F 0.13, Kinghorn, 1983b) than feed efficiency (not different from 0, Rab and Kalal, 1984; Kinghorn, 1983a; low to moderate, Henryon et al., 2002), and in higher vertebrates, direct selection for the trait has been largely unsuccessful (Webb and King, 1983). This does not mean that genetic variations in feed efficiency do not exist; family differences have been observed in salmonid (Thodesen et al., 2001; Kolstad et al., 2004), but the high phenotypic correlation between growth and feed intake (0.98, Kolstad et al., 2004) makes it difficult to select for better feed efficiency when selecting for growth. Selecting for growth on a fixed ration may improve feed efficiency, as demonstrated in pigs (Nguyen and McPhee, 2005). However, because fish are reared in groups, such an approach might be ineffective. Feed restriction favour competition for food and increases feeding hierarchy (McCarthy et al., 1992, Kadri et al., 1996), and the selected fish could be those that are superior competitors and monopolize a higher proportion of the food delivered. Indeed, indirect selection of agonistic behaviour in selection procedures for growth has been reported in medaka (Oryzias latipes) (Ruzzante and Doyle, 1991). This competition situation seems to have been reflected by the higher growth of S compared to C when the S and C lines were held together under feed restriction conditions. Feeding activity profiles reflect the sum of individual feed demands, and there was a peak of feeding activity during the morning. This is probably due to lack of food delivery at night, but could also reflect an endogenous feeding rhythm (Boujard, 2001; Madrid et al., 2001). It is noticeable that the morning peak is exacerbated in both lines after the period of food deprivation. There were no significant differences in the feeding activity profiles between S and C. This differs from findings reported by Mambrini et al. (2004a), on another selected line of brown trout. In that study, selected fish had a more pronounced morning peak of feeding activity than the controls. A difference in feeding activity profile was also observed between fast and slow growing strains of rainbow trout (Valente et al., 2001), the fast-growing strain having a more pronounced peak of feeding at dawn than the slow growing strain. Because the differences in growth and feed intake between S and C were lower than those
reported by Mambrini and co-workers (2004a,b), the differences in the feeding activity profiles of S and C may have been too low to be evidenced in the present study. Alternatively, the increase in feed intake of S may have been equally distributed throughout the day, then the impact of selection on feeding behavior may vary with the strain and rearing conditions applied during the selection process. In the present study, body weight heterogeneity was higher in feed restricted groups than in ad libitum groups, which is in line with the expectations from other work with salmonids (McCarthy et al., 1992; Jobling and Koskela, 1996; Ge´lineau et al., 1998; Kristiansen, 1999). The observed weight heterogeneity is likely a result of individual intake heterogeneity, which is higher when fish are feed restricted because of increased competition for food (Davis and Olla, 1987). An increase in CV is generally interpreted as indicating inter-individual competition and aggressive behavior (Jobling, 1983, 1995, McCarthy et al., 1992; Koskela et al., 1997). When S and C lines were held together and feed restricted, the competition for food between the lines was evident, but was not accompanied by higher CV, suggesting that the level of aggressiveness may have been unaffected. Body weight heterogeneity was lower in S than in C in all treatments, and this appears to be a constant feature of the selection procedure employed (Sanchez et al., 2001; Mambrini et al., 2004a,b). Decrease in CV of the selected trait may be due to loss of genetic variability after many generations of selection (Kawahara et al., 1974; Metodiev and Drbohlav, 1998), but this is not the case for the selection procedure employed here (Chevassus et al., 2004). The lower CV of selected lines may then reflect less competition for food in S than in C. In all treatments, S was more slender than C, but in other studies using same selection procedure, either fish conformation has been found not to differ among the lines (Mambrini et al., 2004b), or S has been stouter than C (Sanchez et al., 2001; Mambrini et al., 2004a). In the present study, the difference in fish conformation was accompanied by lower HSI and VSI, and a higher dressing % in S than in C. This implies that selection may modify the respective proportion of tissues. Genetic differences in liver weight exist in mice (Jones et al., 1992), and pigs selected for improved growth have heavier livers than
M. Mambrini et al. / Aquaculture 252 (2006) 429–440
their control counterparts (Fabian et al., 2003). Differences in liver weight may be a reflection of differences in metabolic rates and maintenance energy requirements (Webster, 1989). Our selection procedure may have affected the metabolic rate, directly or indirectly via the increase in food intake. Indeed in mice, selection that results in greater food intake is associated with higher resting metabolic rates (Selman et al., 2001). On the counterpart, selection to reduce maintenance requirements may not produce animals with higher intake, better growth or altered body composition (Kgwatalala and Nielsen, 2004). In the present study, the loss of weight during deprivation was higher in S than in C. Mobilization of reserves occurred from the viscera and liver, as already shown for brown trout (Regost et al., 2001), but mobilization from the liver seemed to be higher for C than S. This suggests that S and C differ in maintenance requirement, unlike in the selected line characterized by Mambrini and co-workers (2004b). We conclude that the individual selection program for enhanced growth using fork length as the criterion results in improved growth and lowers body weight heterogeneity. Rearing a line selected with this procedure implies revisiting feeding charts because improved growth is achieved by increased feed intake with no modification of feed efficiency. This may have positive effects via reduction in the length of the production cycle and resorting operations. However some correlated responses of this selection program may vary with the strain and the rearing conditions applied during the process, such as maintenance requirements, body composition, and feeding behavior.
Acknowledgements The authors wish to thank L. Lebrun for the daily care of the fish and the team of the SEMII fish farm for his spontaneous help. Constructive comments from the referees were greatly appreciated.
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selected for high and low growth rate on a fixed ration over a set time. Gen. Sel. Evol. 37, 199 – 213. Rab, P., Kalal, L., 1984. Genetic aspects of breeding salmonidae. Agric. Lit. Czechoslov. 1, 35 – 37. Regost, C., Arzel, J., Cardinal, M., Laroche, M., Kaushik, S.J., 2001. Fat deposition and flesh quality in seawater reared, triploid brown trout (Salmo trutta) as affected by dietary fat levels and starvation. Aquaculture 193, 325 – 345. Robinson, B.W., Doyle, R.W., 1990. Phenotypic correlations among behavior and growth variables in tilapia: implications for domestication selection. Aquaculture 85, 177 – 186. Ruzzante, D.E., Doyle, R.W., 1991. Rapid behavioral-changes in medaka (Oryzias latipes) caused by selection for competitive and non-competitive growth. Evolution 45, 1936 – 1946. Sanchez, M.P., Chevassus, B., Labbe, L., Quillet, E., Mambrini, M., 2001. Selection for growth of brown trout (Salmo trutta) affects feed intake but not feed efficiency. Aquat. Living Resour. 14, 41 – 48. SAS, 1996. Statistical Analysis Software copyright 1989–1996. Cary, NC, USA. Selman, C., Korhonen, T.K., Bunger, L., Hill, W.G., Speakman, J.R., 2001. Thermoregulatory responses of two mouse Mus musculus strains selectively bred for high and low food intake. J. Comp. Physiol., B 171, 661 – 668. Smith, R.R., Kincaid, H.L., Regenstein, J.M., Rumsey, G.L., 1988. Growth, carcass composition, and taste of rainbow trout of different strains fed diets containing primarily plant or animal protein. Aquaculture 70, 309 – 321. Sokal, R.R., Braumann, C.A., 1980. Significance tests for coefficients of variation and variability profiles. Syst. Zool. 29, 50 – 62. Thodesen, J., Grisdale-Helland, B., Helland, S.J., Gjerde, B., 1999. Feed intake, growth and feed utilization of offspring from wild and selected Atlantic salmon (Salmo salar). Aquaculture 180, 237 – 246. Thodesen, J., Gjerde, B., Grisdale-Helland, B., Storebakken, T., 2001. Genetic variation in feed intake, growth and feed utilization in Atlantic salmon (Salmo salar). Aquaculture 194, 273 – 281. Valente, L.M.P., Fauconneau, B., Gomes, E.F.S., Boujard, T., 2001. Feed intake and growth of fast and slow growing strains of rainbow trout (Oncorhynchus mykiss) fed by automatic feeders or by self-feeders. Aquaculture 195, 121 – 131. Webb, A.J., King, J.W.B., 1983. Selection for improved food conversion ratio on ad libitum group feeding in pigs. Anim. Prod. 37, 375 – 385. Webster, A.J.F., 1989. Bioenergetics, bioengineering and growth. Anim. Prod. 48, 249 – 269.
Response of growth-selected brown trout (Salmo trutta) to challenging feeding conditions Muriel Mambrini a,*, Laurent Labbe´ b, Faramalala Randriamanantsoa a, Thierry Boujard a a
INRA, Laboratoire de ge´ne´tique des Poissons, 78352 Jouy en Josas Cedex, France b Station expe´rimentale mixte Inra-Ifremer, BP17, 29450 Sizun, France
Received 18 May 2005; received in revised form 6 July 2005; accepted 7 July 2005
Abstract Correlated responses for feed intake, feed utilization and growth were measured in brown trout from lines after five generations of selection on fork length (S) and in control (C). Groups of fish with the same initial weight (5 g) were constituted (500 S, 500 C, 250 S + 250 C) and were either fed ad libitum using self-feeders or were food restricted (75% ad libitum) for 87 days (2 feeding levels 3 replicates for S, C, and mixed groups). After 34 days of food deprivation, all groups were re-fed ad libitum using self-feeders for 41 days. Greater growth of S compared to C was related to higher feed intake (line effect on cumulative intake, P = 0.0041), but feed efficiency was similar (1.4 on average), irrespective of feeding level. During the food deprivation phase, S lost more weight than C ( P = 0.0024). When fish from the two lines were mixed they exhibited the same growth when fed ad libitum; when food was restricted, S grew faster than C ( P = 0.0190), suggesting that S may consume a higher proportion of the available food than C. The daily profile of feeding activity was comparable among the lines. Within groups, weight variation (assessed as CV) was lower in S than in C at all the experimental phases, suggesting that food sharing may be more homogeneous in S than in C. S fish were more slender than C, had lower hepatosomatic and viscerosomatic indices and a higher dressing %. The robustness of the response correlated to our selection procedure is discussed. D 2005 Elsevier B.V. All rights reserved. Keywords: Fish; Selection; Growth; Feed intake; Feed efficiency; Correlated response
1. Introduction
* Corresponding author. Tel.: +33 1 3465 2705; fax: +33 1 3465 2390. E-mail address: [email protected] (M. Mambrini). 0044-8486/$ - see front matter D 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.aquaculture.2005.07.001
Genetic selection for growth improvement of farmed fish has led to high genetic gains (10–20% per generation, Gjedrem, 1998), without affecting genetic variability (Hershberger et al., 1990; Chevassus et al., 2004). Correlated response that accompa-
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nies this selection is generally increased feed intake (Smith et al., 1988; Gjedrem, 1992; Thodesen et al., 1999) and sometimes, improved feed efficiency (Kinghorn, 1983a). This is comparable to what is described in higher vertebrates, even if in fish, one should pay great attention to the influence of environmental factors and dominance effects (Kestemont and Baras, 2001), as well as to the domestication status (Gjedrem, 1979), on growth performance. A genetic individual selection program for brown trout has been underway in France since 1987 (Chevassus et al., 1992), taking into account the environmental and dominance effects. The protocol has been applied to two base populations, held in two experimental fish farms. For each population, a control line has been maintained under the same rearing conditions, and thus submitted to the same domestication influences. The correlated responses to growth enhancement have been measured on one of the two selected lines using a protocol to assess feed intake and feed efficiency (Sanchez et al., 2001). The better growth of the selected population was achieved by higher feed intake; feed efficiency did not differ from that of the control (Sanchez et al., 2001). The selected fish demonstrated a more pronounced feeding rhythm and less individual growth variations than controls (Mambrini et al., 2004a). This may be driven by differences in social interactions (Robinson and Doyle, 1990; Jobling et al., 2001) and by differences in appetite. Further, the requirements for maintenance appeared comparable among the selected and control lines (Mambrini et al., 2004b), as also suggested by the lack of difference in weight loss during feed deprivation (Mambrini et al., 2004a). The objective of the present study is to measure the response to selection of the second selected population of brown trout to assess the robustness of the selection procedure. We used an improved protocol, where we measured feed intake, feeding rhythm and growth simultaneously. We added the challenging condition of rearing selected and control lines together to determine for possible differences related to a situation involving social interaction. In addition we analyzed the variations in liver mass because in higher vertebrates they indicate differences in maintenance and energy requirements (Webster, 1989; Kgwatalala and Nielsen, 2004).
2. Material and methods 2.1. Animals The base population of brown trout (Salmo trutta) was a mixture of five strains from different regions of France, chosen for good growth (Chevassus et al., 1992). Genetic selection involved an improved individual selection process (Chevassus et al., 2004), and a control line (C) was maintained under the same rearing conditions at the experimental fish farm (Gournay, France). The selection criterion was fork length (Chevassus et al., 1992). With a selection pressure of about 5% (proportion of fish selected), the improvement in weight gain for one year olds was about 6% per generation for the selected line (S) compared to C (M. Vandeputte, pers. com). The S and C fish used in the present study were offspring from the fifth generation, and they were produced by in vitro fertilization at the Gournay experimental fish farm. Fifteen females were crossed with 15 males for both lines. To obtain selected and control offspring of similar weight (approximately 5 g) at the beginning of the experiment, we fertilized C 12 days before S. The eggs were incubated at the Gournay fish farm until the eyed stage (temperature 11 F 2 8C; mean F SD). Eggs were then transferred to the SEMII fish farm (Britanny, France), where they were incubated at the same temperature. After hatching, the fish were reared in two tanks per line supplied with flow through 11 8C water. Fish were fed commercial dry feed (Biomar Ecolife 18, 51% protein and 18% lipid according to the manufacturer) provided in excess by automatic feeders, delivering food 12 h a day until the beginning of the experiment. The day before starting the experiment, body weights (BW) and lengths (fork length: L) were measured for representative samples of the C and S populations (500 individuals per tank): 5.1 F 0.9 g and 7.5 F 0.5 cm for C and 4.7 F 0.9 g and 7.4 F 0.5 cm for S. At the start of the experiment, six groups of 500 individuals per line and six mixed groups of 250 C and 250 S fish were established. During handling, the fish were lightly anaesthetized (2-phenoxy-ethanol, 0.2 ml l 1). In the mixed group, the adipose fin of S was cut to aid in recognition. The fish were reared in 2 m3 tanks with flow-through water from Lake Drennec
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(temperature 9–18 8C, water flow 4 m3 h 1, O2 saturated, NH4 b 0.01 mg l 1, pH = 6.7). The first experimental phase, referred to as the feeding phase, lasted for 87 days. During this phase, the fish in the S, C and mixed groups were fed either ad libitum or restricted to 75% of the expected ad libitum level for C (calculated using bEcureuilQ software developed on the SEMII fish farm). The two feeding levels were randomly assigned to 3 tanks of fish for each group. Feed was made available during the light phase (between 0430–2200 hours at the beginning of the experiment and 0530–2200 hours at the end) from computercontrolled self-feeders (Imetronic Sarl, France). Trigger activations were recorded for the S and C groups that were reared separately and fed ad libitum. Fish were rewarded with 2 g of food (Biomar Bioptimal, 1.5 mm, 53% protein and 16% lipid) for each demand. In the restricted feeding tanks, demands were rewarded until the prescribed ration was dispensed. Feed waste was collected in a sediment trap at the outlet of each tank and weighed for calculation of feed intake. Over the first week, uneaten feed and feces were separated by hand, and the respective proportions of each were assessed for each tank. The moisture content of the uneaten feed was also measured and taken into account when making calculations.
2.2. Measurements and calculations At the end of each phase (days 87, 121, and 162), all fish were counted (n i and n f for the initial and final number of fish, respectively) and weighed by tank (W i and W f, for initial and final weights per tank, respectively) after 1 day of fasting to ensure empty gut. In addition, fish were weighed by tank at 21 days intervals during the feeding and re-feeding phases (days 20, 41, and 61 for the feeding phase and day 142 for the re-feeding phase) and the total numbers of fish estimated, taking into account mortality which was recorded daily. For each phase, food consumption, growth and food utilization were assessed using the following: Cumulative intake (g fish feed waste) n f 1
a a
S
C mixed 75
S 100
S mixed C mixed
a a ab
75 aa b b
25
b 50 a 25
bbb Food deprivation
Food deprivation 0 0
) = (distributed food
C b b
S mixed
50
1
Restricted groups
125
C
100
IBW (g)
After the feeding phase, a 34 days feed deprivation was imposed. In the last phase, referred to as the re-feeding phase, all fish were fed ad libitum with self-feeders for 41 days. The reward level was set at 4 g (Biomar Aqua 17, 3 mm, 42% protein and 22% lipid). Feed demands were recorded for the S and C groups reared separately. Feed waste was assessed as during the feeding phase.
Unrestricted groups
125
431
20 40 60 80 100 120 140 160 180 Time (days)
0
0
20 40 60 80 100 120 140 160 180 Time (days)
Fig. 1. Evolution of the mean individual body weight (IBW, g) of brown trout selected for growth (S) or control (C) and held separated or mixed. Groups were fed unrestricted by self-feeder (left) or restricted by automatic feeders (right) until day 87 and feed-deprived until day 121. All groups were fed by self-feeders during the re-feeding phase (until day 161) that followed the phase of food deprivation. Vertical bars indicate one S.D. (a, b) represent significantly different ( P b 0.05) mean body weights on a given day.
RSD
During the re-feeding phase all groups were fed ad libitum with self-feeders, the feeding level refers to the feeding phase only. For each phase, means with different superscripts are significantly different ( P b 0.05), when an interaction was significant, DGC differences were tested after separate analyses of variance. a,b indicate significant differences between lines, x,y between feeding levels and i,j between single and mixed groups.
Feeding phase Feed deprivation phase Re-feeding phase
2.40ax 0.83axi 2.93a S Line
C
2.08bxi 0.64bx 2.74b
S
2.36ax 0.63xj 3.08a
C
1.99bxj 0.59x 2.65b
S
1.43yi 0.55y 3.49
C
1.37yi 0.54yi 3.22
S
1.58ayj 0.44y 3.12a
C
1.32byj 0.05 b0.0001 b0.0001 0.7550 0.0013 0.0163 0.0220 0.1354 0.39yj 0.05 0.0024 b0.0001 b0.0001 0.0584 0.1602 0.8267 0.0283 2.63b 0.29 0.0190 0.0619 0.1116 0.7855 0.4047 0.0696 0.9534
F*M L*M L*F Statistical analysis ( P)
Line (L) Feeding Mixing level (F) (M) Mixed
Restricted
Single Mixed
Ad libitum
Statistical analyses were based on a completely random experimental design. Variables that were independent of initial body weight (DGC, feed intake, cumulative intake and FE during the feeding phase) were compared using analysis of variance that included the effects of line, feeding level, line-mixing and the interactions between these three factors. To analyze feed intake during the re-feeding phase, the mean weight at the beginning of the re-feeding phase was included in the model as a covariate. The tanks were the experimental unit (three replicates per treatment). Individual body weight and length data did not follow a normal distribution. Individual weights
Single
2.3. Statistical analysis
Feeding level
At the end of each phase (feeding, feed deprivation, and re-feeding phases), individual weights (to nearest g) and fork lengths (to nearest mm) were recorded for 100 fish per tank for S and C reared separately and for 100 fish per line and per tank for the mixed groups. Coefficients of variation for weight and length were calculated for each line within each tank (CV: 100 Standard deviation mean 1). Twenty fish per line and per tank in the S and C groups were killed (large dose of 2-phenoxyethanol) and eviscerated. The weights (g) of the liver and viscera minus the liver were recorded and the hepatosomatic index (HSI: 100 liver weight body weight 1), viscerosomatic index (VSI: 100 weight of the viscera without liver body weight 1) and dressing percentage (100 eviscerated weight body body weight 1) calculated. Feeding demands, recorded for the lines reared separately and fed ad libitum, were summed over 30 min. These were then expressed as percent of the total feeding demands over the day and averaged for successive periods covering days 20–40, 42–60, and 62– 86 for the feeding phase and days 122–141 and 143– 161 for the re-feeding phase.
Rearing conditions
Feed intake (%) = 100 (distributed food feed waste) W i 1 Daily growth coefficient (DGC, % d 1) = 100 ((W fn f 1)1/3 (W in i 1)1/3) days 1 Feed efficiency (FE) = (W f Wi) (distributed food feed waste) 1
L*F*M
M. Mambrini et al. / Aquaculture 252 (2006) 429–440 Table 1 Mean daily growth coefficients (DGC) and root square deviation (RSD) of groups of brown trout selected for growth (S) or control (C) reared single or mixed
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M. Mambrini et al. / Aquaculture 252 (2006) 429–440 80
sample, and lnY˜i is the mean logarithm of the ith sample. The scatter of the absolute deviates was equal, indicating that a parametric test may be applied (Sokal and Braumann, 1980). The coefficients of variation were compared by analysis of variance including the effects of line, feeding level, line-mixing, and the interactions between these three factors. The tanks were the experimental unit (three replicates per treatment). The means of the 20 individual measurements of HSI, VSI, and dressing percentage were averaged for each tank, transformed (arcsinus square root), and compared by analysis of variance that included the effects of line, feeding level, and interactions between the two factors. The tanks were the experimental unit (three replicates per treatment). Feeding demands, adjusted to the onset of the feed delivery, were compared with a repeated measures analysis of variance including the effects of time (days) within the experimental phases. Data from the feeding phase were analyzed and included the effects of period, line, the tank nested into the line effect, and the interactions between these three factors. For the re-feeding phase data, the effects of the previous feeding level and the interaction between the line and previous feeding level were also considered. In this case, the tank effect was nested into the interaction. Probabilities of difference between treatments were generated using the General Linear Model procedure of SAS (1996). When the interaction was significant,
S 70
C
Gain (g/fish)
60 50 40 30 20 10 0 0
10
20
30
40
50
60
70
433
80
Cumulative intake (g/fish)
Fig. 2. Mean individual gain (g) versus individual cumulative intake (g) of juvenile brown trout selected for growth (S) or control (C) for the feeding and re-feeding phases.
were log-transformed before being subjected to an analysis of covariance, with the log-transformed length used as a covariate. The model tested the effect of line, feeding level and line-mixing; the tank effect nested into the interaction of the three factors was considered random and was included in the error term (100 individuals per tank, three replicates per treatment). The coefficients of variation of individual body weight and length were transformed to logarithms and the equality of the absolute deviates in each class was controlled. The absolute deviate was calculated (|lnYij lnY˜i |, where Yij is the jth term in the ith
Table 2 Mean individual cumulative intake (g), feed intake (% initial body weight) and root square deviation (RSD) of groups of brown trout selected for growth (S) or control (C) reared single Feeding level
Ad libitum
Line
S
C
Restricted S
C
RSD
Statistical analysis Line (L)
Feeding level (F)
L*F
Cumulative intake Feeding phase Re-feeding phase*
37.15ax 48.03
29.83bx 37.73
15.27y 41.85
14.85y 34.55
1.60 7.06
0.0041 0.1188
b0.0001 0.5315
0.0074 0.5648
Feed intake Feeding phase Re-feeding phase
1.34x 1.46x
1.27x 1.35x
1.09y 1.98y
1.05y 1.78y
0.05 0.20
0.0886 0.2057
b0.0001 0.0043
0.5441 0.7066
During the re-feeding phase all groups were fed ad libitum with self-feeders, the feeding level refers to the feeding phase only. For each phase, means with different superscripts are significantly different ( P b 0.05), when the line-feeding level interaction was significant, differences were tested after separate analyses of variance. a,b indicate significant differences between lines and x,y between feeding levels. *The cumulative intake during the re-feeding phase was analysed with analysis of covariance with the body weight at the start of the re-feeding phase as a covariate.
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Table 3 Repeated time analysis of variance of the pattern of feeding activity (% demand activity half-hour 1 day 1) of brown trout selected for growth or control fed ad libitum by self-feeder during the feeding phase and the re-feeding phase (3 tanks per treatment) Source of variation
df
Type III SS
Mean square
F
P
Growth period Line Time of day Tank (line) Period * time of day Line * time of day Time of day * tank (line) Period * time of day * line
3 1 30 4 90 30 120 90
0.0681 0.0002 4.1915 0.0273 5.5239 0.3067 0.9992 0.4968
0.0227 0.0002 0.1397 0.0068 0.0614 0.0102 0.0083 0.0055
7.25 0.05 21.54 2.18 9.46 1.58 1.28 0.85
0.0072 0.8239 b0.0001 0.1445 b0.0001 0.0317 0.0462 0.8166
Each feeding phase is divided into two growth periods.
separate analyses of variance were performed to test the effects of the line, the feeding method or the mixing. The means were subsequently compared using Newman and Keul’s test (significance level P b 0.05).
2.4. Ethical note The experiment was conducted in compliance with national legislation on animal care, following procedures stipulated by the French Ministry of Research.
15.0 S C
Demand feeding activity (% . half-hours-1)
12.5
10.0
7.5
5.0
2.5
0.0 genotype effect period effect 0
2
4 6 8 10 Time (hours after onset of food delivery)
12
14
16
18
Fig. 3. Pattern of demand feeding activity profile in brown trout selected for growth (S) or control (C) and fed using self-feeders during the feeding and the re-feeding phases. Horizontal bars below the histogram indicate when line or period effects are significant ( P b 0.05). Vertical bars indicate one S.D.
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3.2. Feed intake and feeding activity Feed efficiency was on average 1.41 during the feeding phase and 1.39 during the re-feeding phase, and was neither affected by line (Two-way ANOVA, n = 24, P = 0.9214) nor by feeding level (Two-way ANOVA on data from the feeding phase, n = 12,
Fig. 4. Daily cumulative feeding activity in brown trout selected for growth (S) or control (C) and fed using self-feeders. (a) feeding phase, (b) beginning of the re-feeding phase (days 125–138), (c) end of the re-feeding phase (days 148–161). During the re-feeding phase (b, c), the feeding level refers to the feeding conditions during the feeding phase (a). Vertical bars indicate one S.D.
Cumulative feeding activity (% half-hours-1)
At the end of the experiment, the survival rate ranged from 96% to 99% depending on tank, with no line or treatment effects. In fish fed ad libitum individual body weight was affected by line in both single and mixed groups, whereas in the restricted groups, a line influence was only seen when the fish were held in mixed groups (Fig. 1). During the feeding phase, the daily growth coefficient (Table 1) of S and C held singly differed, being higher in S than in C when fish were fed ad libitum. Mixing the lines had a detrimental effect on the growth of C. During the food deprivation phase, the loss of weight, indicated by a negative DGC, was related to growth during the feeding period: the higher the growth rate during the feeding phase, the higher the loss of weight during the feed deprivation phase (n = 22, r = 0.64, P b 0.0001). The relative loss of weight was higher in S than in C. During the refeeding phase, DGC increased by 20–30% in comparison to the feeding phase when fish had previously been fed ad libitum, and by 100–135% when fish had previously been restricted. The growth of S was higher than that of C, irrespective of mixing status or previous feeding regime. There was no relationship between growth during the re-feeding phase and the relative loss of weight during the feed deprivation phase, or between growth during the re-feeding phase and DGC in the feeding phase.
100
Cumulative feeding activity (% half-hours-1)
3.1. Growth performance
100
Cumulative feeding activity (% half-hours-1)
3. Results
100
a
90 80 70 60 50 40 30 20
S C
10 0
0
4
8
12
16
20
24
b
90 80 70 60 50 40 30
S - previously ad libitum S - previously restricted C - previously ad libitum C - previously restricted
20 10 0
0
4
8
12
16
20
24
c
90 80 70 60 50 40 30
S - previously ad libitum S - previously restricted C - previously ad libitum C - previously restricted
20 10 0
0
4
8
12 Time (hours)
16
20
24
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apparent difference seemed to occur at the beginning of the re-feeding phase, where S fish that had previously been restricted tended to eat more in the early morning than did both the S fish that had previously been fed ad libitum or the C fish. However, a two-way ANOVA to compare cumulative intake after 4 h of feeding at the beginning and at the end of the refeeding phase (Fig. 4b, c) isolated a period effect (n = 24, P = 0.0066) but not any line or previous feeding level effect (n = 24, P = 0.5508).
P = 0.9364). Growth differences between lines were fully explained by differences in feed intake, as illustrated by the relationship between gain and cumulative intake that is not affected by the line (Fig. 2). In the groups where lines were held singly, cumulative intake (g) was higher for S fed ad libitum during the feeding phase than for C (Table 2). In both lines, feed intake during the re-feeding phase was higher for fish that had previously been restricted. Period and time of day had a significant effect on feeding activity, with a strong interaction between these two variables, but no effect of line was observed (Table 3). Because of the lack of interaction between lines, period and time of the day (Table 3), the daily feeding activity is illustrated by plotting the mean daily demands of both lines over the experiment (Fig. 3). There were few nocturnal demands and a peak of feeding activity was seen during the first 2 h of light. This peak represented ca. 30% of total daily demands. During the rest of the day, the hourly feed demand was ca. 5% of the daily total. Feeding was similar for the two lines, the only significant difference being that, in the early afternoon, relative activity was higher for C than S. Cumulative feeding activity profiles were compared for the feeding phase, and at the beginning and end of the re-feeding phase (Fig. 4): profiles were similar for the two lines. The only
3.3. Fish features The HSI, VSI, and dressing % were affected by line (Table 4). The HSI was lower for S than C at the end of the feeding and re-feeding phases, but did not differ between lines at the end of the feed deprivation phase. The VSI was lower for S than C at every experimental phase, and the dressing % was always higher for S than C. During the feeding phase, restricted fish had a lower HSI but VSI did not differ between treatments. Feed deprivation induced a reduction in HSI and VSI in both lines, and gave a higher dressing %, which was higher for S than C. During the re-feeding phase, HSI, VSI and dressing % returned to values similar to those observed before the feed deprivation phase, but the previous feeding level
Table 4 Mean individual hepatosomatic index (%), viscerosomatic index (%), dressing (%) and root square deviation (RSD) of groups of brown trout selected for growth (S) or control (C) reared single Feeding level
Ad libitum
Line
S
Restricted C
S
Statistical analysis C
RSD
Line (L)
Feeding level (F)
L*F
Hepatosomatic index Feeding phase Feed deprivation phase Re-feeding phase
1.52bx 1.03 1.26b
1.65ax 0.93 1.47a
1.36by 0.99 1.40b
1.47ay 1.05 1.61a
0.06 0.14 0.12
0.0014 0.8871 0.0173
0.0018 0.5917 0.0790
0.2563 0.3810 0.9963
Viscerosomatic index Feeding phase Feed deprivation phase Re-feeding phase
9.51b 5.33bx 8.74by
10.59a 6.37ax 9.51a
8.93b 5.00by 9.83bx
10.38a 5.89ay 10.76a
0.45 0.22 0.37
0.0061 0.0001 0.0112
0.1431 0.0073 0.0015
0.6393 0.9811 0.7452
89.95b 91.31b 89.42y
0.45 0.29 0.48
0.0061 0.0006 0.0879
0.1431 0.6097 0.0094
0.6393 0.1680 0.1239
Dressing Feeding phase Feed deprivation phase Re-feeding phase
90.49a 92.30a 90.89x
89.41b 91.63b 89.90x
90.78a 92.47a 89.48y
During the re-feeding phase all groups were fed ad libitum with self-feeders, the feeding level refers to the feeding phase only. For each phase, means with different superscripts are significantly different ( P b 0.05), when the line-feeding level interaction was significant, differences were tested after separate analyses of variance. a,b indicate significant differences between lines and x,y between feeding levels.
0.3942 0.2411 0.7260 0.7160 0.8240 0.0001 0.0530 2.5 27.4b 22.4a 28.5b 20.0a 24.1b 20.2a 25.2b 19.4a
During the re-feeding phase all groups were fed ad libitum with self-feeders, the feeding level refers to the feeding phase only. For each phase, means with different superscripts are significantly different ( P b 0.05), when an interaction was significant, differences were tested after separate analyses of variance. a,b indicate significant differences between lines, x,y between feeding levels and i,j between single and mixed groups.
0.5022 0.3369 0.9657 0.3643 0.7589 0.4751 0.2598 0.0844 0.5655 0.4025 0.0008 0.0017 0.0015 0.1530 2.6 2.7 29.1by 29.4b 21.3ay 21.4a 27.5by 26.0b 24.1ay 24.0a 22.8bx 23.7b 18.7ax 20.7a 23.5bx 27.4b 19.5ax 21.8a
CV of weight Feeding phase Feed deprivation phase Re-feeding phase
0.2439 0.0063 0.9215
0.3396 0.9385 0.0330 0.6687
0.3662 0.8534
Weight / length Feeding phase 57.4ax / 16.2 48.1bx / 15.1 55.2a / 16.1 44.2b / 14.5 26.3y / 12.8 26.5y / 12.6 30.3a / 13.4 25.5b / 12.3 2.0 Feed deprivation 45.3ax / 16.2 41.2bx / 15.3 46.8ax / 16.3 38.0bx / 15.0 22.9y / 13.0 22.9y / 12.8 26.1ay / 13.5 20.7by / 12.3 1.8 phase Re-feeding phase 113.8 / 20.8 96.1 / 19.3 115.8a / 20.7 89.0b / 18.6 79.0 / 18.2 71.0 / 17.3 77.0a / 18.1 57.9b / 16.3 1.3
RSD C S C S C S S Line
C Single Rearing conditions
b0.0001 0.0050 b0.0001 0.0224
0.3069 0.0053 0.8979 0.9837 0.0956 0.6821 0.4329 0.4408
L*F*M F*M L*M Feeding Mixing L * F level (F) (M)
Statistical analysis
Line (L) Mixed Single Mixed
Restricted Ad libitum Feeding level
Table 5 Mean individual weight (g) / length (cm), CV of weight and root square deviation (RSD) of groups of brown trout selected for growth (S) or control (C) reared single or mixed and results of the analysis of variance with length as a covariate
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was found to significantly affect both the VSI and the dressing %. Individual weights were analyzed with the length as covariate so that we characterize the treatments effects on body shape (Table 5). At the end of the feeding phase, S fish were more slender than C fish, and restricting the amount of food rendered both lines slender. Fish features and the specific effect of the line and previous feeding level were conserved during the feed deprivation phase. At the end of the re-feeding phase, S fish were still more slender than C in all the groups; previous feeding level did not have any impact nor did mixing of lines. The CV for weight was lower in S than C throughout the experiment (Table 5). There was an effect of feeding level, which was highly significant during the feeding phase, with higher CVs in feed restricted groups, regardless of line. Mixing had no effect on CV for either line.
4. Discussion The body weight of S was nearly 25% higher than that of C when fed ad libitum, and the daily growth coefficient was 12% to 17% higher for S than C. Although the genetic gain was lower than that reported for another line of brown trout selected with the same procedure (Mambrini et al., 2004a,b), the results conform to the 6% genetic gain per generation usually measured on the line used in the present experiment (M. Vandeputte, pers. com.). Thus, significant gains can be achieved using the selection procedure employed, but the extent of the gain may vary with the characteristics of the basal population and rearing conditions during the selection process. Better growth of S was only seen when the fish were fed ad libitum, feed efficiency being neither affected by line nor feeding regime. The better growth of the selected fish was therefore explained by their higher feed intake. A lack of difference in feed efficiency between S and C, was also seen in another line of brown trout selected according to the same procedure (Mambrini et al., 2004a,b), and one might wonder if this correlated response is specific to the selection procedure used or if the genetic correlation between feed efficiency and growth is poor in fish. In salmonids, feed
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intake capacity has higher heritability (0.15 F 0.30, Gjoen et al., 1991; 0.41 F 0.13, Kinghorn, 1983b) than feed efficiency (not different from 0, Rab and Kalal, 1984; Kinghorn, 1983a; low to moderate, Henryon et al., 2002), and in higher vertebrates, direct selection for the trait has been largely unsuccessful (Webb and King, 1983). This does not mean that genetic variations in feed efficiency do not exist; family differences have been observed in salmonid (Thodesen et al., 2001; Kolstad et al., 2004), but the high phenotypic correlation between growth and feed intake (0.98, Kolstad et al., 2004) makes it difficult to select for better feed efficiency when selecting for growth. Selecting for growth on a fixed ration may improve feed efficiency, as demonstrated in pigs (Nguyen and McPhee, 2005). However, because fish are reared in groups, such an approach might be ineffective. Feed restriction favour competition for food and increases feeding hierarchy (McCarthy et al., 1992, Kadri et al., 1996), and the selected fish could be those that are superior competitors and monopolize a higher proportion of the food delivered. Indeed, indirect selection of agonistic behaviour in selection procedures for growth has been reported in medaka (Oryzias latipes) (Ruzzante and Doyle, 1991). This competition situation seems to have been reflected by the higher growth of S compared to C when the S and C lines were held together under feed restriction conditions. Feeding activity profiles reflect the sum of individual feed demands, and there was a peak of feeding activity during the morning. This is probably due to lack of food delivery at night, but could also reflect an endogenous feeding rhythm (Boujard, 2001; Madrid et al., 2001). It is noticeable that the morning peak is exacerbated in both lines after the period of food deprivation. There were no significant differences in the feeding activity profiles between S and C. This differs from findings reported by Mambrini et al. (2004a), on another selected line of brown trout. In that study, selected fish had a more pronounced morning peak of feeding activity than the controls. A difference in feeding activity profile was also observed between fast and slow growing strains of rainbow trout (Valente et al., 2001), the fast-growing strain having a more pronounced peak of feeding at dawn than the slow growing strain. Because the differences in growth and feed intake between S and C were lower than those
reported by Mambrini and co-workers (2004a,b), the differences in the feeding activity profiles of S and C may have been too low to be evidenced in the present study. Alternatively, the increase in feed intake of S may have been equally distributed throughout the day, then the impact of selection on feeding behavior may vary with the strain and rearing conditions applied during the selection process. In the present study, body weight heterogeneity was higher in feed restricted groups than in ad libitum groups, which is in line with the expectations from other work with salmonids (McCarthy et al., 1992; Jobling and Koskela, 1996; Ge´lineau et al., 1998; Kristiansen, 1999). The observed weight heterogeneity is likely a result of individual intake heterogeneity, which is higher when fish are feed restricted because of increased competition for food (Davis and Olla, 1987). An increase in CV is generally interpreted as indicating inter-individual competition and aggressive behavior (Jobling, 1983, 1995, McCarthy et al., 1992; Koskela et al., 1997). When S and C lines were held together and feed restricted, the competition for food between the lines was evident, but was not accompanied by higher CV, suggesting that the level of aggressiveness may have been unaffected. Body weight heterogeneity was lower in S than in C in all treatments, and this appears to be a constant feature of the selection procedure employed (Sanchez et al., 2001; Mambrini et al., 2004a,b). Decrease in CV of the selected trait may be due to loss of genetic variability after many generations of selection (Kawahara et al., 1974; Metodiev and Drbohlav, 1998), but this is not the case for the selection procedure employed here (Chevassus et al., 2004). The lower CV of selected lines may then reflect less competition for food in S than in C. In all treatments, S was more slender than C, but in other studies using same selection procedure, either fish conformation has been found not to differ among the lines (Mambrini et al., 2004b), or S has been stouter than C (Sanchez et al., 2001; Mambrini et al., 2004a). In the present study, the difference in fish conformation was accompanied by lower HSI and VSI, and a higher dressing % in S than in C. This implies that selection may modify the respective proportion of tissues. Genetic differences in liver weight exist in mice (Jones et al., 1992), and pigs selected for improved growth have heavier livers than
M. Mambrini et al. / Aquaculture 252 (2006) 429–440
their control counterparts (Fabian et al., 2003). Differences in liver weight may be a reflection of differences in metabolic rates and maintenance energy requirements (Webster, 1989). Our selection procedure may have affected the metabolic rate, directly or indirectly via the increase in food intake. Indeed in mice, selection that results in greater food intake is associated with higher resting metabolic rates (Selman et al., 2001). On the counterpart, selection to reduce maintenance requirements may not produce animals with higher intake, better growth or altered body composition (Kgwatalala and Nielsen, 2004). In the present study, the loss of weight during deprivation was higher in S than in C. Mobilization of reserves occurred from the viscera and liver, as already shown for brown trout (Regost et al., 2001), but mobilization from the liver seemed to be higher for C than S. This suggests that S and C differ in maintenance requirement, unlike in the selected line characterized by Mambrini and co-workers (2004b). We conclude that the individual selection program for enhanced growth using fork length as the criterion results in improved growth and lowers body weight heterogeneity. Rearing a line selected with this procedure implies revisiting feeding charts because improved growth is achieved by increased feed intake with no modification of feed efficiency. This may have positive effects via reduction in the length of the production cycle and resorting operations. However some correlated responses of this selection program may vary with the strain and the rearing conditions applied during the process, such as maintenance requirements, body composition, and feeding behavior.
Acknowledgements The authors wish to thank L. Lebrun for the daily care of the fish and the team of the SEMII fish farm for his spontaneous help. Constructive comments from the referees were greatly appreciated.
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