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The effects of dietary crude protein on growth of the Eurasian perch Perca fluviatilis
Aquaculture Aquaculture 144( 1996) 239-249
ELSEVIER
The effects of dietary crude protein on growth of the Eurasian perch Perca jhviatilis E.D. FiogbC a, P. Kestemont ay*, C. M&t-d b, J.C. Micha a a Unirt? d’Ecologie des Eaux Deuces, Faculte’s Universitaires N.D. de la Poix, 61 rue de Bruxelles, B-5000 Namur, Belgium b Laboratoire de Dkmographie des Poissons et d’Aquaculrure, Unioersite’ de Li?ge, IO. Chemin de ia Justice, B-4500 Tihange, Belgium
Accepted 26 February 1996
Abstract A 73-day feeding experiment was conducted to evaluate the effects of dietary crude protein level on growth of Eurasian perch juveniles. Determination of the protein requirement of 2.9 g perch was performed with six semi-purified diets containing crude protein levels ranging from 0 to 60%. Fish were held in three recirculated systems, each diet being tested in triplicate. Significant differences in growth and survival appeared among fish fed diets containing up to 30% crude protein and fish fed diets from 40% crude protein and above. Three mathematical models (the four parameter saturation kinetics, broken line and second order polynomial Brett model) were used to analyse the relationships between dietary crude protein and specific growth rate. According to the saturation kinetics and polynomial models, the optimum dietary crude protein levels were 36.8 and 43.6%. respectively. Based on broken line and polynomial models, maximum growth occured at 43.1 and 56.5%, respectively. Endogenous protein losses of 2.9 g juvenile perch reached 1.11 mg fish-’ day-’ at 23°C. Keywords:
Perch; Perca jluviatilis;
Crude protein; Diet; Growth
1. Introduction Dietary protein is used by fish for energy, growth and maintenance (Marshall, 1994, Kaushik and Medale, 1994). As is the case with a number of nutrients, the economic
l
Corresponding author.
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E.D. Fiogbe’ et al./Aquaculture
240
144 (1996) 239-249
influence of protein is probably much greater than its amount since it is generally believed that the provision of amino acids, either free or in form of proteins, accounts with energy for approximately 95% of the cost of practical diets formulated for fish (Bai and Gatlin, 1992). Thus, any reduction in dietary crude protein without negatively affecting fish growth can substantially reduce the cost of feed. This study was designed to examine the effect of dietary crude protein on growth and feed utilization in juvenile Eurasian perch. Since perch are carnivorous, we expected to observe a high requirement for dietary crude protein. However, a previous study using purified diets in which the pattern of essential amino acids matched whole body patterns estimated the optimal crude protein of juvenile yellow perch Percu j7uuescens M. (a percid fish very close to the Eurasian perch) (Thorpe, 1977) to be 26-28% (Garling, unpublished data, in Brown et al., 1995). Considering these contradictory statements, experimental diets containing different levels of crude protein (ranging from 0 to 60%) were tested in the present study to determine the dietary crude protein requirement of this species.
2. Material and methods 2.1. Facilities
and fish
The experiments were carried out in three recirculating systems similar to those described by Kestemont and Stalmans (1992). The water flow through each rearing tank unit (vol = 25 1) was maintained constant at 0.5 1 min- ’ . Temperature was 23 + 0.5”C and dissolved oxygen ranged from 7 to 8.5 mg l- ’ . Each rearing tank was equipped with an automatic feeder that distributed feed 15 min h- ’ during the daylight period (from 06:OO to 22:00 h). Perch (Percufluviarilis) used in the experiment were obtained from a semi-intensive system of larval production, consisting of green water tanks in which perch grew for 44 days, from eyed eggs to 0.5 g (Kestemont et al., 1995, Melard et al., 1995a). During this period, the fry were trained to accept formulated feed by progressively replacing Artemia nauplii with dry diet. The fry were then reared as described above until the onset of the experiment (at 2.88 + 0.13 g body weight). Before the start of the experiment, fish were randomly distributed in the 18 rearing tanks (corresponding to 3 X 6 protein levels) at a density of 35 fish tank-’ (mean initial density = 4032 g mW3) and fed a mixture of the different experimental diets (Table 1) for 2 weeks. Survival was determined daily by removing dead fish from each rearing tank and weight gain was recorded every week to adjust daily feed ration (5% tank biomass day-’ ) according to the total biomass in each tank. The level 5% of biomass was the maximum quantitative feed requirement for juvenile perch (Melard et al., 1995b). At the end of the feeding period, all fish were individually weighed in order to calculate growth performances and survival. Experimental duration was 73 days, except in the group fed the protein-free diet in which the experimental period was limited to 60 days to assure some live fish for biochemical analysis. Crude protein (Nitrogen X 6.25) in fish whole
E.D. F&be’ et al./Aquacubure Table 1 Composition Ingredients
of experimental
241
144 (1996) 239-249
diets Diets (% protein)
(o/o)
Predicted levels Actual levels Casein a Yeast b Cod meal ’ Dextrin a Glucose a Cod liver oil d Soya oil e Vitamin premix (NRC, 1978) d Mineral premix (NRC. 1978) d Carboxymetbylcellulose a Gross energy (kcal 100 gMa- ’ ) (MI 100 g-i) Protein/energy (g M- ‘)
0.0 2.7
20.0 20.8
30.0 32.1
40.0 40.1
50.0 51.5
60.0 58.4
0.0 0.0 0.0 48.0 19.0 10.0 12.0 5.0 5.0 1.0
0.0 14.0 14.0 20.0 21.0 10.0 10.0 5.0 5.0 1.0
10.8 14.0 14.0 20.0 14.0 10.0 6.2 5.0 5.0 1.0
21.6 14.0 14.0 20.0 6.4 10.0 3.0 5.0 5.0 1.0
32.4 14.0 14.0 10.0 8.6 10.0 0.0 5.0 5.0 1.0
43.1 14.0 14.0 2.9 5.0 10.0 0.0 5.0 5.0 1.0
481 2 1
487 2 IO
a SIGMA product; b Protibel (yeast Saccharomyces) Be1 industries, Son, N.5002 Bergen, Norway; d Drugstore; ’ Market.
484 2 16
485 2 20
487 2 25
503 2 28
4 rue d’Anjou Paris Se, France; ’ Rieber &
body and diets was measured with a Nitrogen/Carbon analyzer (Carlo Erba NA 1500). Fish were freeze-dried, ground and stored at -20°C before protein determination. Growth parameters and nutrient utilization were calculated as follows: SGR = lOO( LnW, - LnW,) At-’ FCR = TFS( FB - IB) - ’ PER = (FB - IB) Wprot; PPV = lOO(Wprot,
’
- Wprot,)Wprot;i
where SGR is specific growth rate (% day-‘), W, 2 are initial and final FCR is feed conversion ratio, IB and FB are initial and final biomass feed supply (g), PER is protein efficiency ratio, Wprot,,, are initial weight in fish (g), PPV is protein productive value (%I and WprotF is crude protein supply per fish (8). 2.2. Composition
of experimental
body weight (g>, (g>, TFS is total and final protein weight of dietary
diets
Six semi-purified diets, including one protein free diet, were prepared (Table 1) by thoroughly mixing the dry pulverized ingredients with the oil and then adding cold water until a stiff dough resulted. The diets were then freeze-dried, ground, and particle sizes of l-2 mm and 500 pm-1 mm were separated with three sieves (500 km, lmm, 2mm). Diets were maintained isocaloric by replacing casein with dextrin, glucose or lipid. Since digestible energy values for the ingredients have not been determined for the
242
E.D. FiogbC et al./Aquaculture
144 (1996) 239-249
Eurasian perch, gross energy values were used. The protein-free diet was prepared estimate endogenous losses and the protein requirement for maintenance. 2.3. Analysis
to
of data
Three mathematical models were used to assess the effect of dietary crude protein level on specific growth rate of perch juveniles. The saturation kinetics model (Morgan et al., 1975, Mercer, 1982) is based on the determination of the following parameters: the protein level of maximum efficiency (Pme), the protein level at maximum slope (Pms) and the protein level of zero response (PrO). The two former levels represent the point at which the organism is operating most efficiently in terms of production of response and the point at which the organism is most sensitive to changes in nutrient intake.
This
model
uses the following
equation:
y=
CbK+
yhx”)
where
y
is
(K+X”) velocity of saturation fraction (SGR), b is ordinate intercept, Y,i, is asymptotic velocity (SGR max), X is concentration of substrate (protein level), n is apparent kinetic order of the velocity, K is characteristic constant of the system, having the property that for X=X’/“,
y=
+_
The general
equation
of the broken
line model (Robbins
et al.,
1979) is y = L + CJ(R - X,,) where L is the ordinate and R is the abscissa of the breakpoint, R is taken as the estimated requirement, X,, means X less than R, and U is the slope of the line for X,,. By definition R - X,, is zero when X > R. The model of Brett et al. (1969) was applied to the second order polynomial regression between protein level and SGR. This model allows determination of the maximum protein level (corresponding to the maximum SGR and calculated by taking the first derivative of the 2nd order polynomial equation), of the optimum protein level (obtained graphically and corresponding to the best feed conversion ratio) and the maintenance level for which no growth may be expected ( y = 0). Values of the different models were calculated by using the SAS procedure (Statistical Analysis Systems Institute Inc., 1985). All data were subjected to factorial analysis of variance using one way ANOVA (Dagnelie, 1975). Treatment effects were considered significantly at P < 0.05. If interactions were significant, orthogonal contrasts were performed to detect mean separation.
3. Results Dietary crude protein level had a significant effect on the survival of perch juveniles (Table 2). Survival was significantly higher in fish fed diets ranging from 40 to 60% crude protein (between 79.1 and 82.9%) than in fish fed diets containing 20 and 30% crude protein (45.7 and 42.9%, respectively). However, no significant difference (P > 0.05) exists within these two groups. Similar results were observed for weight gain. Maximum mean body weight reached 7.28 f 0.64 g in fish fed the 60% crude protein diet whereas mean body weight of fish fed the 20% crude protein diet attained only 3.01 f 0.63 g. Regardless of dietary crude protein level, dominance hierarchy was
‘1
8.60 3.00
0.60 0.60 0.00 0.09 1.20
3.01 a 2.40 -0.01 -0.39 18.27
.._
_
42.86 = 1.00 b 7.58 b 2.70 a 4.18 b 0.02 b 0.60 b 23.49 a 0.23 b 21.42 a 79.05 3.00 4.62 2.71 5.95 0.04 1.08 24.03 0.38 31.11
Mean
40.14
__.._
< 0.05) different.
11.40 1.oo I .70 0.40 0.60 0.00 0.11 2.05 0.08 4.82
*SD
(P
8.60 3.00 10.10 0.50 0.60 0.01 0.42 1.38 0.42
*SD
Mean
32.09
different levels of protein.
superscripts are significantly
45.71 B 4.00 B 22.76 a 2.97 a 3.01 p 0.00 a 0.01 p 21.82 a 0.001 a
Mean
17.14 2.00
20.81
Mean
&-SD
2.66
Dietary protein
of juvenile perch fed diets containing
rb’c*d Means on the same line followed by different
Survival rate (o/o) Cannibalism (%I FCR Initial weight(g) Final weight (g) Weight gain (g daySGR(% day-‘) Dry matter (“lo) PER p.p.v. (%I
Growth parameters
Table 2 Growth performances
b c ’ a c c ’ a ’ b
8.70 4.00 0.70 0.43 1.00 0.01 0.15 1.18 0.09 5.19
*SD 82.86 4.00 3.91 2.95 6.96 0.05 1.18 24.08 0.42 31.11
Mean
51.49
b
b a d a ’ c ’ a ’
4.90 2.00 1.00 0.20 0.60 0.0 1 0.16 1.24 0.13 8.28
*SD
81.90 2.00 3.81 2.91 7.28 0.06 I .26 21.95 0.43 28.13’
Mean
58.38
b d d a d ’ ’ a c
0.06 3.91
1.80
8.20 2.00 0.60 0.40 0.60 0.01 0.20
*SD
e
N
244
E.D. Fiogbi et al./Aquuculture
I44 (1996) 239-249
1.5 y = -0.001x2+0.113x-
k-l 4 # z w l
1.913 l
0.5 ,’ ,** cI
c-*
I*’ c1-L
-0.5
0
I
I
10
20
I 20.6
I
30
1
40 &
50 56.5’
(
Dietary protein (% D.M.) Fig. 1. Relationship between specific growth rate (SGR (% day-‘) DM) in juvenile perch, according to the Brett model.
and dietary crude protein (% dry matter,
Pme
2%0.4
24.9
30
]J
36.8
40
.
I
50
6
Dietary protein (% D.M.) Fig. 2. Relationship between specific growth rate (SGR) and dietary crude protein (% dry matter, DM) in juvenile perch, according to the Mercer model.
E.D. Fiogbk et al./Aqwculture
7-
0
P
144 (1996) 239-249
‘y=1.17-0.05(43.08-xLR)
245
0
0
0
_-_--------
*
0
I
_o,lj., ““Xi”“;/ , 30
20
40
43.08 50 Dietary protein (% D.M.)
Fig. 3. Relationship between specific growth rate (SGR) and dietary juvenile perch, according to the broken line model
t
crude protein (% dry matter,
DM) in
10
0
s 2 2
5
0.5 0
-5 0
,I0 0
-0.5
(
I
20
30
40
50
60
20
I
30
I
40
I
50
I
,I5
60
Dietary protein (% D.M.) Fig. 4. Protein efficiency ratio (PER) and protein productive different levels of protein
value (PPV) in juvenile perch fed diets containing
246
E.D. Fiogbe’ et al./Aquaculture
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present in all tanks, dominant fish being territorial and having a privileged access to the feed. This hierarchy induced a marked size heterogeneity into each group, but particularly in the low protein diet groups. Indeed, the coefficient of variation ranged from 21% for fish fed 20% dietary crude protein to 8.8% for fish fed 60% dietary crude protein. Feed conversion ratio decreased with increasing dietary crude protein levels (Table 2). Specific growth rate increased with dietary crude protein level (Fig. 1) with significant differences from 0 to 60% dietary crude protein (P < 0.05). However, orthogonal contrasts indicated no significant difference between the groups fed diets containing from 40 to 60% crude protein (P > 0.05). The model of Brett et al. (1969) applied to the second order polynomial regression curve showed that maximum, optimum and maintenance dietary crude protein levels were 56.5, 43.6 and 20.6%, respectively (Fig. 1). According to the model of Mercer (19821, used to characterize the relationships between dietary crude protein and specific growth rate (Fig. 2), the protein level to produce maximum efficiency was 36.8%, the protein level for maintenance was 20.4% and the minimum level at which the fish organism is most sensitive to protein intake was 24.9%. By applying the broken line model on the SGR data (Fig. 3c), the maximum dietary crude protein requirement was 43.1%. These results were confirmed by the variation in protein efficiency ratio and the protein productive values which were maximum for dietary crude protein levels between 40 and 50% (Fig. 4). Based on the protein-free diet, the endogenous protein losses of 2.9 g juvenile perch reached 1.l 1 mg fish-’ day- ’ at 23°C.
4. Discussion This work constitutes the first controlled nutritional study in Eurasian perch although nutritional studies of yellow perch have started recently (Brown et al., 1995). However, little information is available to guide formulation of practical diets. As reported by Brown et al. (19951, current diets fed to perch are generally modifications of diets formulated for trout and salmon. A preliminary study estimated the optimal crude protein of juvenile yellow perch at 26-28% (Garling, unpublished data, in Brown et al., 1995). According to the present results, protein requirements of Eurasian perch appear higher, and relatively close to the requirements reported for other carnivorous fish. Although growth increased with increasing dietary crude protein, no significant difference (based on ANOVA) was recorded between diets containing 40-60% dietary crude protein. Despite a non-limiting feeding rate and a high feeding frequency, territorial and dominant behavior induced a strong fish size heterogeneity into each group, regardless of dietary crude protein content. This territorial behavior is probably due to the relatively low rearing density (Melard et al., 1995b), as observed in other species like Sduelinus fontinalis M. (Vijayan and Leatherland, 1988). The semi-purified diets used in this study were based on graded levels of casein. However, nutritional studies have demonstrated that, in yellow perch, casein alone was an inferior source of protein to casein supplemented with crystalline arginine or diets containing mostly crystalline amino acids, probably reflective of insufficient arginine concentration (Brown et al., 1995).
E.D. Fiogbi et al./Aqunculture
144 (1996) 239-249
247
According to the three mathematical models used to determine the protein requirement of juvenile perch, the optimal dietary crude protein content allowing maximal nutrient efficiency is between 36.8 and 43.6% (with a P:E ratio of 2.9-3.5 mg N KJ-‘1. These results are slightly lower than those reported in other carnivorous fish such as juvenile Atlantic salmon (44%, Austreng, 1977), juvenile rainbow trout (40-45%, Zeitoun et al., 1976; Wilson, 1989) or brown trout fry (48-53%, Arzel et al., 1995) but very close to that of hybrid striped bass (36-40%, Brown et al., 1992). The merit of a mathematical treament of experimental data is appreciated through accuracies of statistical and predictive analysis and its ability to suggest new experimental approaches(Mercer, 1982). From a biological point of view, this study has established that the models of saturation kinetics and of Brett et al. (1969) appear the most appropriate. Nevertheless, the saturation kinetic model provides additional interesting information corresponding to the protein level at which the organism is most sensitive to changes in nutrient intake (protein level for maximum slope). In order to maintain the diets isoenergetic, the concentration of lipid was increased in the low protein diets, reaching between 16.2 and 22% of added lipid in the diets containing between 0 and 30% crude protein, respectively. However, recently developed nutritional information for hybrid striped bass indicated that dietary lipid greater than 8% depressed weight gain (Nematipour et al., 1992). This potentially depressive effect of lipid requires further investigation in perch since it is known that excess lipid may reduce feed consumption or may reduce optimal utilization of other dietary components (Lovell, 1979; Watanabe, 1988). The two diets containing 20 and 30% crude protein caused a significant decrease in weight gain, probably also due to the fact that most of the protein was used for maintenance, making it unavailable for growth. The recommended value of dietary crude protein to dietary crude energy ratio (P:E = 2.9-3.5 mg N KJ- ‘1 in perch is similar to the requirement for salmon (3.4 mg N KJ- ‘, Austreng, 1976; Austreng and Storebakken, 1984) or trout (2.4-5.1 mg N KJ-‘, Lee and Putnam, 1973; Takeuchi et al., 19781, slightly higher than the one of carp (2.8-3.2 mg N KJ-‘, Watanabe et al., 1987, Takeuchi et al., 1989) but lower than those recommended for African catfish (3.7-5.8 mg N KJ-‘, Machiels and Henken, 1985, Degani et al., 1989), blue catfish (5.3 mg N KJ-‘, Webster et al., 1995) and channel catfish (3.2-3.7 mg N KJ-‘, Garling and Wilson, 1976). Protein efficiency ratio (PER) and protein productive value (PPV) were very low (Fig. 4) and feed conversion ratio too high (Table 21, probably due to excess feed supply, since the maximum feeding level (based on commercial diets) was maintained throughout the whole experiment. Although PER and PPV values were in agreement with the protein requirements calculated from specific growth rate curve, reduced feeding level would probably improved protein utilization.
Acknowledgements We wish to thank V. Frank and L. Pirmez for their assistance in the feeding experiments. This research was supported by the Ministry of Walloon Region (General Directorate of Natural Resources and Environment) and the Belgian Administration for Development Cooperation (providing a PhD grant to E. FiogbC).
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References Arzel, J., M&her, R., Kerleguer, Ch., Le, Delliou, H. and Guillaume, J., 1995. The protein requirement of brown trout (Salvo trutta) fry. Aquaculture, 130: 67-78. Austreng, E., 1976. Fat and protein in diets for salmonid fishes. I. Fat content in dry diets for salmon parr, (Salmon salar, L.). Meld. Norg. Landbr. Hogsk., 55: 1. Austreng, E., 1977. Fat and protein in diets for salmonoid fishes. IV. Protein content in dry diets for salmon parr (Saltno salar, L.). Meld. Norg. Landbr. Hogsk., 56: l- 10. Austreng, E. and Storebakken, T., 1984. Practical formulation of salmonid diets with emphasis on fat and protein. Acts of the Norwegian-French Workshop on Aquaculture, Brest, 5-8 December 1984. Bai, SC. and Gatlin, D.M., 1992. Present and future use of computer linear programming for fish feed formulations in the United States. Korean J. Anim. Nutr. Feed., 16: 93-104. Brett, J.R., Shelboum, J.E. and Shoop, C.T., 1969. Growth rate and body composition of fingerling sockeye salmon, Oncorhynchus nerka, in relation to temperature and ration size. Fish. Res. Board Can., 26: 2363-2393. Brown, M.L., Nematipour, G.R. and Gatlin, D.M. III., 1992. Dietary crude protein requirement of hybrid striped bass at different salinities. Prog. Fish-Cult., 54: 148-156. Brown, P., Dabrowski, K. and Garling, D., 1995. Nutritional requirements and commercial diets for yellow perch. In: P. Kestemont and K. Dabrowski (Editors), Workshop on Aquaculture of Percids, Presses Universitaires de Namur, Namur, pp. 42-43. Dagnelie, R., 1975. Theorie et M&odes Statistiques, Vol. 2. Presses Agronomiques de Gembloux, Gembloux, 463 PP. Degani, G., Ben-Zvi, Y. and Levanon, D., 1989. The effect of different protein levels and temperatures on feed utilization, growth and body composition of Clarias gariepinus (Burchell, 1822). Aquaculture, 76: 293-30 1. Garling, D.L. and Wilson, R.P., 1976. The optimum dietary protein to energy ratio for channel catfish fingerlings. J. Nutr., 106: 1368-1375. Kaushik, S.J. and MCdale, F., 1994. Energy requirements, utilization and dietary supply to salmonids. Aquaculture, 124: 81-97. Kestemont, P. and Stalmans, J.M., 1992. Initial feeding of European minnow larvae, Phoxinus phoxinus L. 1. Influence of diet and feeding level. Aquaculture, 104: 327-340. Kestemont, P., MBlard, C., FiogbC, E.D., Vlavonou R. and Masson G., 1995. Larval and post-larval rearing of European perch Percafluuiatilis: ontogeny of digestive system, growth and nutritional requirements. In: P. Kestemont and K. Dabrowski (Editors), Workshop on Aquaculture of Percids, Presses Universitaires de Namur, Namur, pp. 20-24. Lee, D.J. and Putnam, G.B., 1973. The response of rainbow trout to varying protein/energy ratios in a test diet. J. Nutr., 103: 916-922. Lovell, R.T., 1979. Factors affecting voluntary feed consumption by channel catfish. Proc. World Symp. Fintish Nutr. Fishfced Technol., 1, Hamburg, pp. 555-564. Machiels, M.A.M. and Henken, M., 1985. Growth rate, feed utilization and energy metabolism of the African cattish, C/arias gariepinus (Burchell, 1822). as affected by dietary protein and energy content. Aquaculture, 44: 271-284. Marshall, W.E., 1994. Ammo acids, peptides, and proteins. In: J.P.F. D’Mello (Editor), Amino Acids in Farm Animal Nutrition. Scottish Agricultural College, Edinburgh, pp. 242-260. Mtlard, C., Baras, E., Mary, L. and Kestemont, P., 1995a. Relationships between growth, cannibalism and survival rate in intensively cultured larvae and alevins of Perch (Perca jluuiatilis). Abstract Percis 11, Second International Percid fish Symposium. Vaasa, Finland, 21-25 August 1995: pp. 53-54. Melard, C., Kestemont, P. and Grignard, J.C., 1995b. Intensive ongrowing of European perch juveniles (Perca fluoiatilis): zootcchnical parameters and growth. In: P. Kestemont and K. Dabrowski (Editors), Workshop on Aquaculture of Percids, Presses Universitaires de Namur, Namur, pp. 34-37. Mercer, L.P., 1982. The quantitative nutrient-response relationship. J. Nutr., 112: 560-566. Morgan, P.H., Mercer, L.P. and Flodin, N.W., 1975. General model for nutritional responses of higher organisms (bioassay/saturation kinetic/growth responses). hoc. Nat. Acad. Sci., USA, 72(11): 43274331.
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Nematipour, G.R., Brown, M.L. and Gatlin, D.M., III, 1992. Effects of dietary carbohydrate: lipid ratio on growth and body composition of hybrid striped bass. J. World Aquacult. Sot., 3: 128-132. Robbins, K.R., Norton, H.W. and Baker, D.H., 1979.. Estimation of nutrient requirements from growth data. J. Nutr., 109: 1710-1714. Statistical Analysis Systems Institute Inc., 1985. SAS/Graph User’s Guide: Statistics, Version 5 edn., Gary, NC, 5% pp. Takeuchi, T., Yokoyama, M., Watanabe, T. and Ogino, C., 1978. Optimum ratio of dietary energy to protein for rainbow trout. Bull. Jpn. Sot. Fish., 44: 729-732. Takeuchi, T., Watanabe, T.. Satoh, S., Martino, R.C., Ida, T. and Yaguchi, M., 1989. Suitable levels of protein and digestible energy in practical carp diets. Nippon Suisan Gakkaishi, 56: 1839- 1845. Thorpe, J.E., 1977. Morphology, physiology, behavior, and ecology of Perca fluviatilis L. and P. flavescens Mitchell. I. Fish. Res. Board Can., 4: 1504-1514. Vijayan, M.M. and Leatherland, J.F., 1988. Effect of stocking density on the growth and stress-respond in brook charr, Salvelinus fontinalis. Aquaculture, 75: 159-170. Watanabe T., 1988. Fish Nutrition and MaricuIture. JICA Texbook, General Aquaculture Course, Kanagawa International Fisheries Training Centre, Japan International Cooperation Agency, 233 pp. Watanabe, T., Takeuchi, T., Satoh. S., Wang, K.W., Ida, T., Yaguchi, M., Nakada, M., Amano, T., Yoshijima, S. and Ace, H., 1987. Development of practical carp diets for reduction of total nitrogen loading on water environment. Nippon Suisan Gakkaishi, 53: 2217-2225. Webster, CD., Tidwell, J.H., Tiu, L.S. and Yancey, D.H., 1995. Use of soybean meal as partial or total substitute of fish meal in diet for blue cattish (lctalurusfurcatus). Aquat. Living Resour., 8: 379-384. Wilson, R.P., 1989. Amino acids and proteins. In: J.E. Halver (Editor), Fish Nutrition. Academic Press, San Diego, CA, pp. 111-151. Zeitoun, I.H., Ullrey, D.E. and Magee, W.T., 1976. Quantifying nutrient requirements of tish. J. Fish. Res. Board Can.. 3: 167-172.
ELSEVIER
The effects of dietary crude protein on growth of the Eurasian perch Perca jhviatilis E.D. FiogbC a, P. Kestemont ay*, C. M&t-d b, J.C. Micha a a Unirt? d’Ecologie des Eaux Deuces, Faculte’s Universitaires N.D. de la Poix, 61 rue de Bruxelles, B-5000 Namur, Belgium b Laboratoire de Dkmographie des Poissons et d’Aquaculrure, Unioersite’ de Li?ge, IO. Chemin de ia Justice, B-4500 Tihange, Belgium
Accepted 26 February 1996
Abstract A 73-day feeding experiment was conducted to evaluate the effects of dietary crude protein level on growth of Eurasian perch juveniles. Determination of the protein requirement of 2.9 g perch was performed with six semi-purified diets containing crude protein levels ranging from 0 to 60%. Fish were held in three recirculated systems, each diet being tested in triplicate. Significant differences in growth and survival appeared among fish fed diets containing up to 30% crude protein and fish fed diets from 40% crude protein and above. Three mathematical models (the four parameter saturation kinetics, broken line and second order polynomial Brett model) were used to analyse the relationships between dietary crude protein and specific growth rate. According to the saturation kinetics and polynomial models, the optimum dietary crude protein levels were 36.8 and 43.6%. respectively. Based on broken line and polynomial models, maximum growth occured at 43.1 and 56.5%, respectively. Endogenous protein losses of 2.9 g juvenile perch reached 1.11 mg fish-’ day-’ at 23°C. Keywords:
Perch; Perca jluviatilis;
Crude protein; Diet; Growth
1. Introduction Dietary protein is used by fish for energy, growth and maintenance (Marshall, 1994, Kaushik and Medale, 1994). As is the case with a number of nutrients, the economic
l
Corresponding author.
00448486/96/$15.00 PII SOO44-8486(96)0
Copyright 0 1996 Elsevier Science B.V. All rights reserved. 1293-S
E.D. Fiogbe’ et al./Aquaculture
240
144 (1996) 239-249
influence of protein is probably much greater than its amount since it is generally believed that the provision of amino acids, either free or in form of proteins, accounts with energy for approximately 95% of the cost of practical diets formulated for fish (Bai and Gatlin, 1992). Thus, any reduction in dietary crude protein without negatively affecting fish growth can substantially reduce the cost of feed. This study was designed to examine the effect of dietary crude protein on growth and feed utilization in juvenile Eurasian perch. Since perch are carnivorous, we expected to observe a high requirement for dietary crude protein. However, a previous study using purified diets in which the pattern of essential amino acids matched whole body patterns estimated the optimal crude protein of juvenile yellow perch Percu j7uuescens M. (a percid fish very close to the Eurasian perch) (Thorpe, 1977) to be 26-28% (Garling, unpublished data, in Brown et al., 1995). Considering these contradictory statements, experimental diets containing different levels of crude protein (ranging from 0 to 60%) were tested in the present study to determine the dietary crude protein requirement of this species.
2. Material and methods 2.1. Facilities
and fish
The experiments were carried out in three recirculating systems similar to those described by Kestemont and Stalmans (1992). The water flow through each rearing tank unit (vol = 25 1) was maintained constant at 0.5 1 min- ’ . Temperature was 23 + 0.5”C and dissolved oxygen ranged from 7 to 8.5 mg l- ’ . Each rearing tank was equipped with an automatic feeder that distributed feed 15 min h- ’ during the daylight period (from 06:OO to 22:00 h). Perch (Percufluviarilis) used in the experiment were obtained from a semi-intensive system of larval production, consisting of green water tanks in which perch grew for 44 days, from eyed eggs to 0.5 g (Kestemont et al., 1995, Melard et al., 1995a). During this period, the fry were trained to accept formulated feed by progressively replacing Artemia nauplii with dry diet. The fry were then reared as described above until the onset of the experiment (at 2.88 + 0.13 g body weight). Before the start of the experiment, fish were randomly distributed in the 18 rearing tanks (corresponding to 3 X 6 protein levels) at a density of 35 fish tank-’ (mean initial density = 4032 g mW3) and fed a mixture of the different experimental diets (Table 1) for 2 weeks. Survival was determined daily by removing dead fish from each rearing tank and weight gain was recorded every week to adjust daily feed ration (5% tank biomass day-’ ) according to the total biomass in each tank. The level 5% of biomass was the maximum quantitative feed requirement for juvenile perch (Melard et al., 1995b). At the end of the feeding period, all fish were individually weighed in order to calculate growth performances and survival. Experimental duration was 73 days, except in the group fed the protein-free diet in which the experimental period was limited to 60 days to assure some live fish for biochemical analysis. Crude protein (Nitrogen X 6.25) in fish whole
E.D. F&be’ et al./Aquacubure Table 1 Composition Ingredients
of experimental
241
144 (1996) 239-249
diets Diets (% protein)
(o/o)
Predicted levels Actual levels Casein a Yeast b Cod meal ’ Dextrin a Glucose a Cod liver oil d Soya oil e Vitamin premix (NRC, 1978) d Mineral premix (NRC. 1978) d Carboxymetbylcellulose a Gross energy (kcal 100 gMa- ’ ) (MI 100 g-i) Protein/energy (g M- ‘)
0.0 2.7
20.0 20.8
30.0 32.1
40.0 40.1
50.0 51.5
60.0 58.4
0.0 0.0 0.0 48.0 19.0 10.0 12.0 5.0 5.0 1.0
0.0 14.0 14.0 20.0 21.0 10.0 10.0 5.0 5.0 1.0
10.8 14.0 14.0 20.0 14.0 10.0 6.2 5.0 5.0 1.0
21.6 14.0 14.0 20.0 6.4 10.0 3.0 5.0 5.0 1.0
32.4 14.0 14.0 10.0 8.6 10.0 0.0 5.0 5.0 1.0
43.1 14.0 14.0 2.9 5.0 10.0 0.0 5.0 5.0 1.0
481 2 1
487 2 IO
a SIGMA product; b Protibel (yeast Saccharomyces) Be1 industries, Son, N.5002 Bergen, Norway; d Drugstore; ’ Market.
484 2 16
485 2 20
487 2 25
503 2 28
4 rue d’Anjou Paris Se, France; ’ Rieber &
body and diets was measured with a Nitrogen/Carbon analyzer (Carlo Erba NA 1500). Fish were freeze-dried, ground and stored at -20°C before protein determination. Growth parameters and nutrient utilization were calculated as follows: SGR = lOO( LnW, - LnW,) At-’ FCR = TFS( FB - IB) - ’ PER = (FB - IB) Wprot; PPV = lOO(Wprot,
’
- Wprot,)Wprot;i
where SGR is specific growth rate (% day-‘), W, 2 are initial and final FCR is feed conversion ratio, IB and FB are initial and final biomass feed supply (g), PER is protein efficiency ratio, Wprot,,, are initial weight in fish (g), PPV is protein productive value (%I and WprotF is crude protein supply per fish (8). 2.2. Composition
of experimental
body weight (g>, (g>, TFS is total and final protein weight of dietary
diets
Six semi-purified diets, including one protein free diet, were prepared (Table 1) by thoroughly mixing the dry pulverized ingredients with the oil and then adding cold water until a stiff dough resulted. The diets were then freeze-dried, ground, and particle sizes of l-2 mm and 500 pm-1 mm were separated with three sieves (500 km, lmm, 2mm). Diets were maintained isocaloric by replacing casein with dextrin, glucose or lipid. Since digestible energy values for the ingredients have not been determined for the
242
E.D. FiogbC et al./Aquaculture
144 (1996) 239-249
Eurasian perch, gross energy values were used. The protein-free diet was prepared estimate endogenous losses and the protein requirement for maintenance. 2.3. Analysis
to
of data
Three mathematical models were used to assess the effect of dietary crude protein level on specific growth rate of perch juveniles. The saturation kinetics model (Morgan et al., 1975, Mercer, 1982) is based on the determination of the following parameters: the protein level of maximum efficiency (Pme), the protein level at maximum slope (Pms) and the protein level of zero response (PrO). The two former levels represent the point at which the organism is operating most efficiently in terms of production of response and the point at which the organism is most sensitive to changes in nutrient intake.
This
model
uses the following
equation:
y=
CbK+
yhx”)
where
y
is
(K+X”) velocity of saturation fraction (SGR), b is ordinate intercept, Y,i, is asymptotic velocity (SGR max), X is concentration of substrate (protein level), n is apparent kinetic order of the velocity, K is characteristic constant of the system, having the property that for X=X’/“,
y=
+_
The general
equation
of the broken
line model (Robbins
et al.,
1979) is y = L + CJ(R - X,,) where L is the ordinate and R is the abscissa of the breakpoint, R is taken as the estimated requirement, X,, means X less than R, and U is the slope of the line for X,,. By definition R - X,, is zero when X > R. The model of Brett et al. (1969) was applied to the second order polynomial regression between protein level and SGR. This model allows determination of the maximum protein level (corresponding to the maximum SGR and calculated by taking the first derivative of the 2nd order polynomial equation), of the optimum protein level (obtained graphically and corresponding to the best feed conversion ratio) and the maintenance level for which no growth may be expected ( y = 0). Values of the different models were calculated by using the SAS procedure (Statistical Analysis Systems Institute Inc., 1985). All data were subjected to factorial analysis of variance using one way ANOVA (Dagnelie, 1975). Treatment effects were considered significantly at P < 0.05. If interactions were significant, orthogonal contrasts were performed to detect mean separation.
3. Results Dietary crude protein level had a significant effect on the survival of perch juveniles (Table 2). Survival was significantly higher in fish fed diets ranging from 40 to 60% crude protein (between 79.1 and 82.9%) than in fish fed diets containing 20 and 30% crude protein (45.7 and 42.9%, respectively). However, no significant difference (P > 0.05) exists within these two groups. Similar results were observed for weight gain. Maximum mean body weight reached 7.28 f 0.64 g in fish fed the 60% crude protein diet whereas mean body weight of fish fed the 20% crude protein diet attained only 3.01 f 0.63 g. Regardless of dietary crude protein level, dominance hierarchy was
‘1
8.60 3.00
0.60 0.60 0.00 0.09 1.20
3.01 a 2.40 -0.01 -0.39 18.27
.._
_
42.86 = 1.00 b 7.58 b 2.70 a 4.18 b 0.02 b 0.60 b 23.49 a 0.23 b 21.42 a 79.05 3.00 4.62 2.71 5.95 0.04 1.08 24.03 0.38 31.11
Mean
40.14
__.._
< 0.05) different.
11.40 1.oo I .70 0.40 0.60 0.00 0.11 2.05 0.08 4.82
*SD
(P
8.60 3.00 10.10 0.50 0.60 0.01 0.42 1.38 0.42
*SD
Mean
32.09
different levels of protein.
superscripts are significantly
45.71 B 4.00 B 22.76 a 2.97 a 3.01 p 0.00 a 0.01 p 21.82 a 0.001 a
Mean
17.14 2.00
20.81
Mean
&-SD
2.66
Dietary protein
of juvenile perch fed diets containing
rb’c*d Means on the same line followed by different
Survival rate (o/o) Cannibalism (%I FCR Initial weight(g) Final weight (g) Weight gain (g daySGR(% day-‘) Dry matter (“lo) PER p.p.v. (%I
Growth parameters
Table 2 Growth performances
b c ’ a c c ’ a ’ b
8.70 4.00 0.70 0.43 1.00 0.01 0.15 1.18 0.09 5.19
*SD 82.86 4.00 3.91 2.95 6.96 0.05 1.18 24.08 0.42 31.11
Mean
51.49
b
b a d a ’ c ’ a ’
4.90 2.00 1.00 0.20 0.60 0.0 1 0.16 1.24 0.13 8.28
*SD
81.90 2.00 3.81 2.91 7.28 0.06 I .26 21.95 0.43 28.13’
Mean
58.38
b d d a d ’ ’ a c
0.06 3.91
1.80
8.20 2.00 0.60 0.40 0.60 0.01 0.20
*SD
e
N
244
E.D. Fiogbi et al./Aquuculture
I44 (1996) 239-249
1.5 y = -0.001x2+0.113x-
k-l 4 # z w l
1.913 l
0.5 ,’ ,** cI
c-*
I*’ c1-L
-0.5
0
I
I
10
20
I 20.6
I
30
1
40 &
50 56.5’
(
Dietary protein (% D.M.) Fig. 1. Relationship between specific growth rate (SGR (% day-‘) DM) in juvenile perch, according to the Brett model.
and dietary crude protein (% dry matter,
Pme
2%0.4
24.9
30
]J
36.8
40
.
I
50
6
Dietary protein (% D.M.) Fig. 2. Relationship between specific growth rate (SGR) and dietary crude protein (% dry matter, DM) in juvenile perch, according to the Mercer model.
E.D. Fiogbk et al./Aqwculture
7-
0
P
144 (1996) 239-249
‘y=1.17-0.05(43.08-xLR)
245
0
0
0
_-_--------
*
0
I
_o,lj., ““Xi”“;/ , 30
20
40
43.08 50 Dietary protein (% D.M.)
Fig. 3. Relationship between specific growth rate (SGR) and dietary juvenile perch, according to the broken line model
t
crude protein (% dry matter,
DM) in
10
0
s 2 2
5
0.5 0
-5 0
,I0 0
-0.5
(
I
20
30
40
50
60
20
I
30
I
40
I
50
I
,I5
60
Dietary protein (% D.M.) Fig. 4. Protein efficiency ratio (PER) and protein productive different levels of protein
value (PPV) in juvenile perch fed diets containing
246
E.D. Fiogbe’ et al./Aquaculture
I44 (1996) 239-249
present in all tanks, dominant fish being territorial and having a privileged access to the feed. This hierarchy induced a marked size heterogeneity into each group, but particularly in the low protein diet groups. Indeed, the coefficient of variation ranged from 21% for fish fed 20% dietary crude protein to 8.8% for fish fed 60% dietary crude protein. Feed conversion ratio decreased with increasing dietary crude protein levels (Table 2). Specific growth rate increased with dietary crude protein level (Fig. 1) with significant differences from 0 to 60% dietary crude protein (P < 0.05). However, orthogonal contrasts indicated no significant difference between the groups fed diets containing from 40 to 60% crude protein (P > 0.05). The model of Brett et al. (1969) applied to the second order polynomial regression curve showed that maximum, optimum and maintenance dietary crude protein levels were 56.5, 43.6 and 20.6%, respectively (Fig. 1). According to the model of Mercer (19821, used to characterize the relationships between dietary crude protein and specific growth rate (Fig. 2), the protein level to produce maximum efficiency was 36.8%, the protein level for maintenance was 20.4% and the minimum level at which the fish organism is most sensitive to protein intake was 24.9%. By applying the broken line model on the SGR data (Fig. 3c), the maximum dietary crude protein requirement was 43.1%. These results were confirmed by the variation in protein efficiency ratio and the protein productive values which were maximum for dietary crude protein levels between 40 and 50% (Fig. 4). Based on the protein-free diet, the endogenous protein losses of 2.9 g juvenile perch reached 1.l 1 mg fish-’ day- ’ at 23°C.
4. Discussion This work constitutes the first controlled nutritional study in Eurasian perch although nutritional studies of yellow perch have started recently (Brown et al., 1995). However, little information is available to guide formulation of practical diets. As reported by Brown et al. (19951, current diets fed to perch are generally modifications of diets formulated for trout and salmon. A preliminary study estimated the optimal crude protein of juvenile yellow perch at 26-28% (Garling, unpublished data, in Brown et al., 1995). According to the present results, protein requirements of Eurasian perch appear higher, and relatively close to the requirements reported for other carnivorous fish. Although growth increased with increasing dietary crude protein, no significant difference (based on ANOVA) was recorded between diets containing 40-60% dietary crude protein. Despite a non-limiting feeding rate and a high feeding frequency, territorial and dominant behavior induced a strong fish size heterogeneity into each group, regardless of dietary crude protein content. This territorial behavior is probably due to the relatively low rearing density (Melard et al., 1995b), as observed in other species like Sduelinus fontinalis M. (Vijayan and Leatherland, 1988). The semi-purified diets used in this study were based on graded levels of casein. However, nutritional studies have demonstrated that, in yellow perch, casein alone was an inferior source of protein to casein supplemented with crystalline arginine or diets containing mostly crystalline amino acids, probably reflective of insufficient arginine concentration (Brown et al., 1995).
E.D. Fiogbi et al./Aqunculture
144 (1996) 239-249
247
According to the three mathematical models used to determine the protein requirement of juvenile perch, the optimal dietary crude protein content allowing maximal nutrient efficiency is between 36.8 and 43.6% (with a P:E ratio of 2.9-3.5 mg N KJ-‘1. These results are slightly lower than those reported in other carnivorous fish such as juvenile Atlantic salmon (44%, Austreng, 1977), juvenile rainbow trout (40-45%, Zeitoun et al., 1976; Wilson, 1989) or brown trout fry (48-53%, Arzel et al., 1995) but very close to that of hybrid striped bass (36-40%, Brown et al., 1992). The merit of a mathematical treament of experimental data is appreciated through accuracies of statistical and predictive analysis and its ability to suggest new experimental approaches(Mercer, 1982). From a biological point of view, this study has established that the models of saturation kinetics and of Brett et al. (1969) appear the most appropriate. Nevertheless, the saturation kinetic model provides additional interesting information corresponding to the protein level at which the organism is most sensitive to changes in nutrient intake (protein level for maximum slope). In order to maintain the diets isoenergetic, the concentration of lipid was increased in the low protein diets, reaching between 16.2 and 22% of added lipid in the diets containing between 0 and 30% crude protein, respectively. However, recently developed nutritional information for hybrid striped bass indicated that dietary lipid greater than 8% depressed weight gain (Nematipour et al., 1992). This potentially depressive effect of lipid requires further investigation in perch since it is known that excess lipid may reduce feed consumption or may reduce optimal utilization of other dietary components (Lovell, 1979; Watanabe, 1988). The two diets containing 20 and 30% crude protein caused a significant decrease in weight gain, probably also due to the fact that most of the protein was used for maintenance, making it unavailable for growth. The recommended value of dietary crude protein to dietary crude energy ratio (P:E = 2.9-3.5 mg N KJ- ‘1 in perch is similar to the requirement for salmon (3.4 mg N KJ- ‘, Austreng, 1976; Austreng and Storebakken, 1984) or trout (2.4-5.1 mg N KJ-‘, Lee and Putnam, 1973; Takeuchi et al., 19781, slightly higher than the one of carp (2.8-3.2 mg N KJ-‘, Watanabe et al., 1987, Takeuchi et al., 1989) but lower than those recommended for African catfish (3.7-5.8 mg N KJ-‘, Machiels and Henken, 1985, Degani et al., 1989), blue catfish (5.3 mg N KJ-‘, Webster et al., 1995) and channel catfish (3.2-3.7 mg N KJ-‘, Garling and Wilson, 1976). Protein efficiency ratio (PER) and protein productive value (PPV) were very low (Fig. 4) and feed conversion ratio too high (Table 21, probably due to excess feed supply, since the maximum feeding level (based on commercial diets) was maintained throughout the whole experiment. Although PER and PPV values were in agreement with the protein requirements calculated from specific growth rate curve, reduced feeding level would probably improved protein utilization.
Acknowledgements We wish to thank V. Frank and L. Pirmez for their assistance in the feeding experiments. This research was supported by the Ministry of Walloon Region (General Directorate of Natural Resources and Environment) and the Belgian Administration for Development Cooperation (providing a PhD grant to E. FiogbC).
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Nematipour, G.R., Brown, M.L. and Gatlin, D.M., III, 1992. Effects of dietary carbohydrate: lipid ratio on growth and body composition of hybrid striped bass. J. World Aquacult. Sot., 3: 128-132. Robbins, K.R., Norton, H.W. and Baker, D.H., 1979.. Estimation of nutrient requirements from growth data. J. Nutr., 109: 1710-1714. Statistical Analysis Systems Institute Inc., 1985. SAS/Graph User’s Guide: Statistics, Version 5 edn., Gary, NC, 5% pp. Takeuchi, T., Yokoyama, M., Watanabe, T. and Ogino, C., 1978. Optimum ratio of dietary energy to protein for rainbow trout. Bull. Jpn. Sot. Fish., 44: 729-732. Takeuchi, T., Watanabe, T.. Satoh, S., Martino, R.C., Ida, T. and Yaguchi, M., 1989. Suitable levels of protein and digestible energy in practical carp diets. Nippon Suisan Gakkaishi, 56: 1839- 1845. Thorpe, J.E., 1977. Morphology, physiology, behavior, and ecology of Perca fluviatilis L. and P. flavescens Mitchell. I. Fish. Res. Board Can., 4: 1504-1514. Vijayan, M.M. and Leatherland, J.F., 1988. Effect of stocking density on the growth and stress-respond in brook charr, Salvelinus fontinalis. Aquaculture, 75: 159-170. Watanabe T., 1988. Fish Nutrition and MaricuIture. JICA Texbook, General Aquaculture Course, Kanagawa International Fisheries Training Centre, Japan International Cooperation Agency, 233 pp. Watanabe, T., Takeuchi, T., Satoh. S., Wang, K.W., Ida, T., Yaguchi, M., Nakada, M., Amano, T., Yoshijima, S. and Ace, H., 1987. Development of practical carp diets for reduction of total nitrogen loading on water environment. Nippon Suisan Gakkaishi, 53: 2217-2225. Webster, CD., Tidwell, J.H., Tiu, L.S. and Yancey, D.H., 1995. Use of soybean meal as partial or total substitute of fish meal in diet for blue cattish (lctalurusfurcatus). Aquat. Living Resour., 8: 379-384. Wilson, R.P., 1989. Amino acids and proteins. In: J.E. Halver (Editor), Fish Nutrition. Academic Press, San Diego, CA, pp. 111-151. Zeitoun, I.H., Ullrey, D.E. and Magee, W.T., 1976. Quantifying nutrient requirements of tish. J. Fish. Res. Board Can.. 3: 167-172.