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Effects of protein restriction with subsequent realimentation on growth performance of juvenile Chinese shrimp (Fenneropenaeus chinensis)
Aquaculture 210 (2002) 343 – 358 www.elsevier.com/locate/aqua-online
Effects of protein restriction with subsequent realimentation on growth performance of juvenile Chinese shrimp (Fenneropenaeus chinensis) Lixin Wu, Shuanglin Dong * Aquaculture Research Laboratory, Fisheries College, Ocean University of Qingdao, Qingdao, 266003, People’s Republic of China Received 15 June 2001; received in revised form 23 October 2001; accepted 23 October 2001
Abstract The effects of protein restriction in the diet with subsequent realimentation on growth responses of juvenile Chinese shrimp, Fenneropenaeus chinensis (initial mean wet weight 1.347 g), were investigated. The control group (Group C) was fed an adequate diet containing 44.6% crude protein and 18.5 kJ gross energy/g dry matter throughout the experiment. For treatment Groups T15 and T30, in the restriction phase (weeks 1 – 2) dietary crude protein contents were reduced to 15.0% and 29.3%, respectively, with constant energy supply, while in the realimentation phase (weeks 3 – 6) they were supplied with the same diet as the control group. Protein restriction led to significant decrease in specific growth rates and body weight of shrimp. However, when the shrimp were transferred from protein restriction to realimentation, they had significantly increased specific growth rates in terms of dry matter, protein and energy (SGRd, SGRp and SGRe) compared with the control shrimp. At the end of the experiment, the shrimp in Group T30 achieved complete growth compensation, while those in Group T15 were still significantly smaller than the controls. As dietary protein levels reduced, feed conversion efficiencies and apparent protein digestibility decreased, but feed intake and protein efficiency ratio increased. The shrimp responded to a change from protein restriction to realimentation by displaying improved feed conversion efficiencies (FCEd, FCEp and FCEe) compared with the controls, although those in Group T15 delayed in showing the enhanced FCE values. In the initial 2-week realimentation, the shrimp in Group T15 showed significantly higher feed intake, and lower apparent digestibility of dry matter and protein than those of the controls. There was no significant difference in protein efficiency ratio among all groups in the realimentation phase. The above results suggest that compensatory growth in Group T30 is mainly dependent on improved feed conversion efficiencies, while that in Group T15 is attributable to both improved feed conversion efficiencies and increasing feed intake. After 2-week restriction, the shrimp showed lower body crude protein, lipid and energy content, and higher moisture and ash content than the controls. However, during the course of *
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realimentation, the differences between the previously protein restricted shrimp and the controls diminished. This indicates that compensatory growth after a period of protein restriction in juvenile Chinese shrimp was accompanied by a complete recovery in body composition and energy content. D 2002 Elsevier Science B.V. All rights reserved. Keywords: Fenneropenaeus chinensis; Protein restriction; Compensatory growth; Feed consumption; Feed utilization; Body composition
1. Introduction The return to adequate feeding conditions following a period of starvation or undernutrition will often result in animals displaying a rapid growth spurt, known as compensatory or catch-up growth, which is known to occur in a wide range of mammals, including humans and domestic animals, and birds (Wilson and Osbourn, 1960; Ashworth and Millward, 1986; Mersmann et al., 1987; Summers et al., 1990; Marais et al., 1991). Since 1970s, studies on the compensatory growth in aquatic animals have become a highlighted subject, due to the fact that this phenomenon is not only of ecophysiological significant, but also of implications for aquaculture (Quinton and Blake, 1990; Jobling et al., 1994; Hayward et al., 1997). Nutrient composition in diet is one of the factors influencing an animal’s ability to recover from the effects of undernutrition, among which the most attention has been paid to protein restriction (Wilson and Osbourn, 1960). There have been a number of investigations on farm animals showing that a complete recovery in body weight was obtained after a period of protein restriction (Winchester et al., 1957; Zimmerman and Khajarern, 1973; Campbell and Dunkin, 1983). For aquatic animals, a considerable number of studies on the effects of dietary protein levels on growth performances have been conducted, but the possible effects of previous restriction on compensatory growth response are almost unknown, except for the work with common carp indicating some recovery in carcass composition after realimentation (Castell and Budson, 1974; Colvin, 1976; Schwarz et al., 1985; Shiau et al., 1991; Koshio et al., 1993; Mai et al., 1995). The Chinese shrimp (Fenneropenaeus chinensis), widely distributed along the coast of China, is a key species in the natural fishery community, and is the most important commercial shrimp species cultured in China, comprising approximately 80% of total shrimp production per year (Liu, 1990). Previous work with Chinese shrimp has revealed that compensatory growth can be elicited after a period of feed deprivation (Wu et al., 2000, 2001). This study was designed to determine the effect of feeding limited crude protein followed by an adequate diet supply on growth performance of this shrimp, with particular respect to compensatory growth.
2. Materials and methods 2.1. Diets Three test diets were prepared containing 15.0%, 29.3% and 44.6% crude protein (dry weight basis). Cod liver oil and corn starch were adjusted to maintain similar dietary
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energy content. Diets were prepared by mixing dry ingredients and water (2:1, w/w), then pellet type diets were produced through a meat grinder with a 1.6 mm die. The diets were then oven-dried (40 jC for 12 h) to approximately 8% moisture and stored at 20 jC until used. The formulation and proximate composition of the experimental diets are shown in Table 1. 2.2. Experimental design Completely randomized design was used in this growth experiment. The experiment lasted for 6 weeks and was divided into a restriction period (weeks 1 – 2) and a realimentation period (weeks 3– 6). Shrimp in Group C (control) were fed a standardized diet (D45) with 44.6% crude protein in excess ration throughout the trial period. In treatment Group T15 and T30, the crude protein supply was reduced to 15.0% (D15) and 29.3% (D30), respectively, during the restriction period. In the realimentation phase, shrimp previously fed the protein restriction diets were fed the same feed as the controls.
Table 1 Ingredient composition and proximate analysis (dry weight basis) of the experimental diets Ingredients (%)
Experimental diets D15
D30
D45
Casein Fish meal Shrimp meal Wheat flour Corn starch Carboxymethyl-cellulose Peanut oil Cod liver oil Cholesterol Soybean lecithin Vitamin mixa Mineral mixb Chromic oxide
0.0 15.0 5.0 19.5 40.0 5.0 1.0 5.0 1.0 2.0 2.0 4.0 0.5
10.8 22.5 5.0 19.5 23.7 5.0 1.0 3.0 1.0 2.0 2.0 4.0 0.5
21.6 30.0 5.0 19.5 6.9 5.0 1.0 1.5 1.0 2.0 2.0 4.0 0.5
Proximate analysis (means of triplicate) Crude protein (%) Crude lipid (%) Ash (%) Gross energy (kJ g 1)
15.0 10.4 8.4 18.2
29.3 8.7 10.4 18.3
44.6 7.6 12.3 18.5
a Vitamin mix, each 1000 g of diet contained: thiamin – HCl, 60 mg; riboflavin, 100 mg; folic acid, 10 mg; pyridoxine – HCl, 140 mg; niacin, 400 mg; calcium pantothenate, 140 mg; choline chloride, 4000 mg; inositol, 4000 mg; ascorbic acid, 4000 mg; biotin, 2 mg; U-amino benzoic acid, 150 mg; a-tocopherol, 400 mg; menadione, 34 mg; cyanocobalamine, 0.8 mg; retinol acetate, 150,000 IU; cholecalciferol, 60,000 IU. b Mineral mix, each 1000 g of diet contained: Ca(H2PO4)2, 8.800 g; CaCO3, 8.240 g; K2HPO4, 4.000 g; NaH2PO4, 11.200 g; MgSO47H2O, 5.095 g; KCl, 1.600 g; FeSO47H2O, 0.400 g; AlCl6H2O, 0.016 g; ZnSO47H2O, 0.432 g; MnSO4H2O, 0.080 g; CuSO45H2O, 0.008 g; CoCl26H2O, 0.112 g; KI, 0.016 g; Na2SeO3, 0.001 g.
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2.3. Rearing condition A static-water system consisting of 30 aquaria (45 30 30 cm, water volume 35 l) with aeration was used in this experiment. Seawater was filtered by composite sand filters. For each aquarium, two thirds of the seawater was replaced daily. The aquaria were cleaned thoroughly at the end of the fourth week. During the experiment, dissolved oxygen was maintained above 6.0 mg l 1, water temperature at 24.0 F 0.5 jC, salinity ranged from 30x to 33x, pH from 7.8 to 8.2, and photoperiod was 14L:10D. 2.4. Source and acclimation of experimental shrimp The experiment was carried out between 12 August and 23 September 2000 at the Laboratory of Aquaculture Ecology, Ocean University of Qingdao, Qingdao, P. R. China, using Chinese shrimp (F. chinensis) obtained from the Hongdao Shrimp Breeding Farm, Qingdao. The shrimp were initially held in a fiberglass tank (100 100 80 cm) for 3 days, and were then transferred into 30 aquaria (each aquarium held six shrimp) for 1-week acclimation, during which the water temperature was maintain at 24 jC and the shrimp were fed three times a day on the standardized pellet diet (control diet). 2.5. Experimental procedure After 12-h feed deprivation, 150 size-selected shrimp with initial weight range 1.215 – 1.477 g (1.347 F 0.010 g: mean F SE) were pooled into a large fiberglass tank. From the pooled shrimp, three groups of 10 individuals each were randomly sampled for the analysis of initial body composition. The remains (120 shrimp) were randomly selected, individually weighed and stocked into 30 aquaria with each aquarium holding four individuals, and then 10 aquaria were randomly allotted to each experimental group. For the analysis of body composition, three aquaria were randomly sampled at the end of the restriction period and at the end of 2-week realimentation, respectively, and thus four aquaria remained in each treatment during the last 2 weeks of the experiment. The shrimp in each aquarium were individually weighed every 2 weeks, following feed deprivation for 12 h. To remove excess moisture, the shrimp were carefully blotted with paper towel and weighed to the nearest 0.001 g. During the course of the experiment, shrimp were hand-fed at excess ration three times daily (at 06:00, 12:00 and 18:00 h) for each group. Each meal lasted approximately 2 h and any uneaten feed was collected, dried at 70 jC and weighed every 2 weeks. Twice a day, intact faeces were collected from each aquarium by pipetting, freeze-dried immediately and held at 20 jC until analyzed. 2.6. Biochemical analysis The shrimp, faeces and uneaten feed, respectively, from each aquarium were pooled as a sample. Before chemical composition analysis, all the dried samples of shrimp, faeces
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and feed were homogenized and re-stored at 70 jC to constant weight. Crude protein in sample was determined by the micro-Kjeldahl method, lipid by ether extraction using a Soxhlet system, ash by combustion at 550 jC for 12 h (AOAC, 1984), and gross energy content by 1281 Oxygen Bomb Calorimeter (Parr Instrument, USA). The concentration of Cr2O3 added to the diets to estimate the apparent digestibility was determined as described by Furukawa and Tsukahara (1966). 2.7. Calculation of data The following parameters were used to evaluate shrimp growth: Specific growth rate in wet weight ðSGRw : %day1 Þ ¼ 100 ðlnW2 lnW1 Þ=t Feed intake ðFI : % body weight day1 Þ ¼ 100 Df =½t ðW1 þ W2 Þ=2 Feed conversion efficiency in wet weight ðFCEw : %Þ ¼ 100 ðW2 W1 Þ=Df Protein efficiency ratio ðPER : %Þ ¼ 100 ðW2 W1 Þ=Dp where W2 and W1—final and initial wet weight (g) of the shrimp within a measuring interval; t—the measuring interval (days); Df—dry diet intake (g); Dp—dry protein intake (g). Specific growth rates and feed conversion efficiencies in dry matter (SGRd and FCEd), protein (SGRp and FCEp) and energy (SGRe and FCEe) were calculated similarly. Moult increment was defined as MI (g)=(W2 W1)/Nm, where W2 and W1 are the final weight and initial weight (g) of shrimp within a measuring interval, Nm is the number of moults for each shrimp; intermoult period as IP (days) = T/Nm, where T is the measuring interval (days), Nm is the number of moults for each shrimp. Apparent digestibility of dry matter, protein and energy were calculated as follows: % apparent digestibility of dry matter ðADd Þ ¼ ð1 % Cr2 O3 in diet=% Cr2 O3 in faecesÞ 100 % apparent digestibility of protein ðADp Þ or energy ðADe Þ % protein ðor energy contentÞ in faeces=% Cr2 O3 in faeces ¼ 1 100 % protein ðor energy contentÞ in diet=% Cr2 O3 in diet
2.8. Statistical analysis Statistical analysis was performed using SYSTAT statistical software (SYSTAT, 1992). Data from each treatment were subjected to one-way ANOVA. When overall differences were significant at the 0.05 level, Duncan’s multiple range test was used to compare the mean values among treatments.
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3. Results 3.1. Survival and growth All groups showed high survival (more than 90%) and the values among the three groups were not significantly different, indicating that different feeding schedules did not affect survival (Table 2). The mean body weights of Chinese shrimp reared under various feeding schedules during the course of the experiment are shown in Table 2. At the end of the protein restriction period, there were significant differences in body weight among shrimp fed the different experimental diets: the shrimp fed the control diet (44.6% protein) had the highest body weight, while those fed 15.0% protein diet had the lowest body weight. After 2 weeks of realimentation, no significant difference in body weight was observed between the shrimp in Group T30 and C (the control), whereas the body weight of shrimp in Group T15 was still significantly lower than that of the control shrimp, and this situation of body weight maintained till the termination of the experiment. As Fig. 1 illustrates, during the period of protein restriction, specific growth rate in terms of wet weight (SGRw), dry matter (SGRd), protein (SGRp) and energy content (SGRe) markedly increased with dietary protein content. During the first 2 weeks of realimentation, the previously protein-restricted shrimp displayed significantly higher SGRd, SGRp and SGRe than the controls, and there seemed to be a tendency for these values to decrease with increase in severity of protein restriction. During the last 2 weeks of the experiment, SGRd, SGRp and SGRe of the shrimp in Group T15 were significantly higher than those of shrimp in other two groups, while no significant differences in these SGR values were found between the shrimp previously fed 29.3% protein diet and the controls fed 44.6% protein diet continuously. Within each measuring interval (2 weeks) of realimentation, there was no significant difference in SGRw among the shrimp of all groups. 3.2. Moult increment and intermoult period The data on moult increment and intermoult period are presented in Table 3. There was no significant difference in moult increment among the shrimp reared under the three
Table 2 Growth and survival of juvenile Chinese shrimp held on the three feeding schedules during the course of the experiment (mean F SE, n = 4)1 Treatments
T15 T30 C (control) 1
Body weight (g)
Survival (%)
Initial
After restriction
After 2-week realimentation
Final
1.352 F 0.006 1.354 F 0.006 1.336 F 0.009
1.678 F 0.032a 1.840 F 0.025b 1.946 F 0.030c
2.310 F 0.105a 2.578 F 0.023b 2.626 F 0.047b
2.894 F 0.143a 3.205 F 0.046b 3.217 F 0.070b
Values with different superscripts in the same column are significantly different ( P < 0.05).
93.75 F 6.25 100.00 F 0.00 100.00 F 0.00
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Fig. 1. Specific growth rates in terms of wet weight (SGRw), dry matter (SGRd), protein (SGRp) and energy (SGRe) for juvenile Chinese shrimp held on the three feeding schedules during the course of experiment. Means with different letters within each period are significantly different ( P < 0.05), and bars indicate standard errors of the means.
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Table 3 Mean moult increment (MI, g)1, mean intermoult period (IP, days)2 for juvenile Chinese shrimp held on the three feeding schedules during the course of the experiment (mean F SE, n = 4)3 Parameters
MI (g)
IP (days)
Groups
T15 T30 C (control) T15 T30 C (control)
Time (weeks) 0–2
3–4
5–6
0.266 F 0.030 0.268 F 0.019 0.266 F 0.017 11.4 F 1.0a 8.4 F 0.4b 6.1 F 0.3c
0.417 F 0.033 0.430 F 0.022 0.376 F 0.017 8.6 F 1.4 8.2 F 0.2 7.8 F 0.3
0.366 F 0.066 0.316 F 0.029 0.340 F 0.039 7.7 F 0.8 7.1 F 0.4 8.2 F 0.7
1 Mean molt increment (g)=(W2 W1)/Nm, where W2 and W1 are final and initial wet weight (g) of the shrimp within a measuring interval; Nm is the number of moults for each shrimp. 2 Mean intermoult period (days) = T/Nm, where T is the measuring interval (days); Nm is the number of moults for each shrimp. 3 Values with different superscripts in the same column are significantly different ( P < 0.05).
feeding schedules within each measuring interval of the experiment. During the period of protein restriction, intermoult period significantly prolonged with decrease in dietary protein content, but no significant difference in intermoult period was observed among the shrimp of all experimental groups during the realimentation period. 3.3. Apparent digestibility The effects of feeding schedules on the apparent digestibility of juvenile Chinese shrimp are depicted in Fig. 2. Within each measured interval of the experiment, there were no significant differences in apparent energy digestibility (ADe) among all groups, and also no significant differences in apparent digestibility of dry matter (ADd) and protein (ADp) between Group T30 and C. During the protein restriction phase, a marked depression in ADp for shrimp fed the lowest protein content diet was observed, while there was no effect of dietary protein content on ADd. During the first 2 weeks of realimentation, both ADp and ADd were significantly lower in Group T15 than in Group T30 and C. However, during the last 2 weeks of the experiment these digestibility values for Group T15 adjusted to those for the other two groups. 3.4. Feed intake As shown in Fig. 3, in the protein restriction phase, feed intake significantly increased as the protein content decreased. During the first 2 weeks of realimentation, there was no significant difference in feed consumption between the shrimp in Group T30 and C, but the shrimp previously fed 15.0% protein diet still displayed significantly higher feed intake than those in the other two groups. No significant difference in feed intake was found among the shrimp in all groups during the last 2 weeks of the experiment.
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Fig. 2. Apparent digestibility of dry matter (ADd), protein (ADp) and energy (ADe) for juvenile Chinese shrimp held on the three feeding schedules during the course of experiment. Means with different letters within each period are significantly different ( P < 0.05), and bars indicate standard errors of the means.
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Fig. 3. Feed intake (FI) of juvenile Chinese shrimp held on the three feeding schedules during the course of experiment. Means with different letters within each period are significantly different ( P < 0.05), and bars indicate standard errors of the means.
3.5. Protein efficiency ratio During the course of protein restriction, shrimp fed the lowest protein diet (15.0%) had significantly higher protein efficiency ratio (PER) than those fed higher protein diets (29.3% and 44.6%). There were no significant differences in PER among the shrimp in all groups within each growth interval of realimentation (Fig. 4).
Fig. 4. Protein efficiency ratio (PER) for juvenile Chinese shrimp held on the three feeding schedules during the course of experiment. Means with different letters within each period are significantly different ( P < 0.05), and bars indicate standard errors of the means.
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353
Fig. 5. Feed conversion efficiency in terms of wet weight (FCEw), dry matter (FCEd), protein (FCEp) and energy (FCEe) for juvenile Chinese shrimp held on the three feeding schedules during the course of experiment. Means with different letters within each period are significantly different ( P < 0.05), and bars indicate standard errors of the means.
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3.6. Feed conversion efficiency In the protein restriction phase, feed conversion efficiency in terms of wet weight (FCEw), dry matter (FCEd), protein (FCEp) and energy (FCEe) significantly improved with increased dietary protein level. During the first 2 weeks of realimentation, FCEd, FCEp and FCEe were significantly higher in T30-treated shrimp than those in T15-treated shrimp and the controls, whereas within the last 2 weeks of realimentation these FCE values for T15treated shrimp were significantly higher than those for the shrimp in Group T30 and C. No significant difference in FCEw was observed among the shrimp in all groups in the whole realimentation phase (Fig. 5). 3.7. Body composition and energy content The data on proximate body composition and energy content are given in Table 4. At the end of the restriction phase, significantly higher percentages of body moisture and crude ash, and lower percentages of body crude protein, crude lipid and energy content were found in protein restricted shrimp than in those fed the control diet (44.6% protein content), although these body composition values were not significantly different between the T15- and T30-treated shrimp. After 2 weeks of realimentation, the shrimp previously fed 29.3% protein diet restored their body composition and energy content to the levels not significantly different from those of the control shrimp, whereas all these biochemical parameters, except for crude ash, in the shrimp previously fed 15.0% protein diet were still significantly lower than in the control shrimp. At the end of the realimentation, there were no significant differences in body composition and energy content among the shrimp in all experimental groups.
Table 4 Body composition and energy content of juvenile Chinese shrimp held on the three feeding schedules at different times of the experiment (mean F SE, n = 4)1 Time
Treatments
Moisture2
Protein2
Lipid2
Ash2
Energy3
Initial After restriction
– T15 T30 C (control) T15 T30 C (control) T15 T30 C (control)
75.12 F 0.12 78.45 F 0.28b 77.65 F 0.41b 75.40 F 0.38a 77.52 F 0.30b 75.13 F 0.17a 75.76 F 0.28a 75.48 F 0.44 76.14 F 0.20 75.37 F 0.29
16.97 F 0.08 14.42 F 0.18a 15.13 F 0.28a 16.77 F 0.26b 15.30 F 0.20a 16.65 F 0.11b 16.77 F 0.20b 16.56 F 0.30 16.44 F 0.14 16.69 F 0.19
2.55 F 0.10 1.86 F 0.07a 1.82 F 0.12a 2.42 F 0.05b 1.88 F 0.11a 2.45 F 0.13b 2.33 F 0.08b 2.52 F 0.12 2.54 F 0.10 2.39 F 0.07
2.61 F 0.06 2.78 F 0.04b 2.80 F 0.05b 2.61 F 0.04a 2.75 F 0.04 2.73 F 0.06 2.81 F 0.07 2.59 F 0.08 2.50 F 0.08 2.57 F 0.06
4.814 F 0.023 3.887 F 0.050a 4.022 F 0.074a 4.614 F 0.071b 4.028 F 0.053a 4.701 F 0.032b 4.567 F 0.052b 4.640 F 0.083 4.689 F 0.039 4.801 F 0.056
After 2-week realimentation Final
1 2 3
Values with different superscripts in the same column are significantly different ( P < 0.05). Values were expressed as % wet weight. Values were expressed as kJ g 1 wet weight.
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4. Discussion In the present study, the mean specific growth rate in terms of wet weight (SGRw) of the shrimp fed the control diet (44.6% protein content) was approximately 2.10% day 1, which is comparable to those (1.54 –2.46% day 1) reported for similar-sized penaeids (Alava and Lim, 1983; Xu and Li, 1988; Xue et al., 1998). It appears that the control diet prepared for this study was nutritionally adequate to support good growth of juvenile Chinese shrimp. During the protein restriction period, the mean specific growth rate in terms of wet weight (SGRw), dry matter (SGRd), protein (SGRp) and energy (SGRe) of juvenile Chinese shrimp significantly decreased with reduction in the amount of protein in the diet, which is in general agreement with the results of previous studies carried out on a range of shrimp species (Sedgwick, 1979; Smith et al., 1985; Shiau et al., 1991; Koshio et al., 1993). Consequently, at the end of restriction phase, the shrimp fed the lower protein content diets (D15 and D30) were significantly smaller than the controls. Upon realimentation, however, the SGR (SGRd, SGRp and SGRe, except for SGRw) of the previously protein-restricted shrimp were markedly greater than those of the controls, indicating that there was a compensatory growth response. At the end of the realimentation phase, the shrimp in Group T30 achieved complete growth compensation, in that they caught up in body weight to the controls fed 44.6% protein content diet (D45) throughout the experiment. Though the shrimp in Group T15 were still significantly smaller than the controls at the end of the experiment, the possibility that they can also fully regain the body weight lost during the restriction period cannot be excluded from the present study, since in the last 2 weeks of the experiment the SGRd, SGRp and SGRe of the shrimp in Group T15 were still significantly higher than those of the controls (Fig. 1). Thus, an experimental design incorporating a longer realimentation period would be necessary to determine when the SGR values for T15-treated shrimp decline to the levels not significantly different from those of the controls. Due to differences in the quantity of dietary protein, quality of the protein, ratio of dietary protein to energy and species-specific differences, the effects of dietary protein content on carcass composition in crustaceans and fishes seem to be inconsistent (Dabrowski, 1977; Alava and Lim, 1983; Hubbard et al., 1986). In the present study, the average body crude protein, lipid, and energy contents of F. chinensis were positively related to the dietary protein content, whereas body moisture and ash contents significantly decreased as dietary protein content increased (Table 4). Furthermore, the results of this study indicated that during the course of realimentation the differences in body composition and energy content between the previously protein-restricted shrimp and the control shrimp diminished, which is similar to the findings reported for common carp and pig (Wyllie et al., 1969; Zimmerman and Khajarern, 1973; Schwarz et al., 1985). This suggests that compensatory growth following a period of protein restriction in Chinese shrimp was accompanied by a complete recovery in body composition and energy content. Previous investigations on a variety of shrimp and fish have indicated a reduced apparent protein digestibility on diets with very low crude protein content as compared to high amounts (Kitamikado et al., 1964; Smith et al., 1985; Shiau et al., 1991; Koshio et al., 1993). A similar result was obtained in the present study, i.e. the shrimp fed the 15%
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protein content diet (D15) with constant energy supply digested the dietary protein less well than those fed the higher protein content diets (D30 and D45). Furthermore, the shrimp previously fed D15 maintained the lower apparent protein digestibility for 2 weeks in the realimentation phase (Fig. 2), which seems to be consistent with the findings reported for common carp (Schwarz et al., 1985). Nevertheless, in experiments on pigs a rather improved protein digestibility was observed during realimentation (Gadeken et al., 1983; Senckenberg et al., 1984). It is likely that the differences in responses of protein digestibility result from variations in the severity and duration of protein restriction, quality of diet, and interspecific differences. The results of the present study with juvenile Chinese shrimp appear to be in accordance with the general mechanisms for a range of shrimp (Deshimaru and Yone, 1978; Sedgwick, 1979; Alava and Lim, 1983; Shiau et al., 1991), in which feed intake and protein efficiency ratio decreased, and feed conversion efficiencies (FCEs) increased as dietary protein content increased to a certain extent. However, when changed from protein restriction to realimentation, the previously restricted shrimp displayed better feed conversion efficiencies (FCEd, FCEp and FCEe, except for FCEw) than the controls, although those previously fed 15.0% protein content diet (D15) delayed showing improved feed conversion efficiencies (Fig. 5). The data on feed intake indicated that, upon a return to realimentation, feed intake of the shrimp previously fed D15 was still significantly higher than that of the controls, but the shrimp previously fed D30 showed the same feed intake as the controls. There was no significant difference in the protein efficiency ratio among the shrimp of all groups in the realimentation phase. The analysis based on the above results of feed intake, feed conversion efficiencies and protein efficiency ratio, combining the previously noted digestibility data suggests that compensatory growth for T30-treated shrimp is mainly dependent on improved feed conversion efficiencies, while that for T15-treated shrimp is attributable to both the improved feed conversion efficiencies and increasing feed intake. It has been well documented in decapoda crustaceans that poor diets can reduce the moult increment and lengthen the intermoult period (reviewed by Hartnoll, 1982). For example, individual Cherax destructor reared on a low protein diet had significantly smaller moult increments and longer intermoult periods compared with those fed on a high protein diet (Jones et al., 1996). However, the present study with Chinese shrimp demonstrated that during the restriction period there was no effect of dietary protein content on the moult increment, although intermoult period also significantly lengthened as dietary protein level decreased. It is, therefore, needed to further investigate whether or not the effects of diets on the moult increment are related to dietary composition, and/or interspecific differences.
Acknowledgements This study was subsidized by funds from the Chinese National Science Foundation for Talent Youths (Grant no. 39725023) and the Major State Basic Research Projects of China (Grant no. G1999012011). We thank Hongdao Shrimp Breeding Farm, Qingdao, P. R. China, for providing the shrimp used in this experiment.
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References Alava, V.R., Lim, C., 1983. The quantitative dietary protein requirements of Penaeus monodon juveniles in a controlled environment. Aquaculture 30, 53 – 61. AOAC (Association of Official Analytical Chemists), 1984. Official Methods of Analysis, 14th edn. Association of Official Analytical Chemists, Arlington, VA, 1141 pp. Ashworth, A., Millward, D.J., 1986. Catch-up growth in children. Nutr. Rev. 44, 157 – 163. Campbell, R.G., Dunkin, A.C., 1983. The influence of nutrition in early life on growth and development of the pig: 1. Effects of protein nutrition prior and subsequent to 6.5 kg on growth and development to 45 kg. Anim. Prod. 36, 415 – 423. Castell, J.D., Budson, S.D., 1974. Lobster nutrition: the effect on Homarus americanus of dietary protein levels. J. Fish. Res. Board Can. 31, 1363 – 1370. Colvin, P.M., 1976. Nutritional studies on penaeid prawns: protein requirements in compounded diets for juvenile Penaeus indicus (Milne Edwards). Aquaculture 7, 315 – 326. Dabrowski, K., 1977. Protein requirements of grass carp (Ctenopharyngodon idella Val.). Aquaculture 12, 63 – 73. Deshimaru, O., Yone, Y., 1978. Optimum level of dietary protein for prawn. Bull. Jpn. Soc. Sci. Fish. 44, 1395 – 1397. Furukawa, A., Tsukahara, H., 1966. On the acid digestion method for the determination of chromic oxide as an index substance in the study of digestibility of fish feed. Bull. Jpn. Soc. Sci. Fish. 32, 502 – 506. Gadeken, D., Bohme, H., Oslage, H.J., 1983. Protein- und Energieumsatz bei wachsenden Schweinen unter Einfluss des kompensatorischen Wachstums. Arch. Tierernaehr. 33, 125 – 140. Hartnoll, R.G., 1982. Growth. In: Abele, L.G.The Biology of Crustacea. Embryology, Morphology and Genetics, vol. 2. Academic Press, New York, pp. 111 – 196. Hayward, R.S., Noltiem, D.B., Wang, N., 1997. Use of compensatory growth to double hybrid sunfish growth rates. Trans. Am. Fish. Soc. 126, 316 – 322. Hubbard, D.M., Robinson, E.H., Brown, P.B., Daniels, W.H., 1986. Optimum ratio of dietary protein to energy for red crayfish (Procambarus clarkii). Prog. Fish-Cult. 48, 233 – 237. Jobling, M., Moloy, O.H., Dos Santos, J., Christiansen, B., 1994. The compensatory growth response of the Atlantic cod: effects of nutritional history. Aquacult. Int. 2, 75 – 90. Jones, P.L., De Silva, S., Mitchell, B.D., 1996. Effect of dietary protein content on growth performance, feed utilisation and carcass composition in the Australian freshwater crayfish, Cherax albidus Clark and Cherax destructor Clark (Decapoda, Parastacidae). Aquacult. Nutr. 2, 141 – 150. Kitamikado, M., Morishita, T., Tachino, S., 1964. Digestibility of dietary protein in rainbow trout: I. Digestibility of several dietary proteins. Bull. Jpn. Soc. Sci. Fish. 30, 46 – 49. Koshio, S., Teshima, S., Kanazawa, A., Watase, T., 1993. The effect of dietary protein content on growth, digestion efficiency and nitrogen excretion of juvenile kuruma prawns, Penaeus japonicus. Aquaculture 113, 101 – 114. Liu, J.Y., 1990. Present status and future prospects for shrimp mariculture in China. In: Main, K.L., Fulks, W. (Eds.), Proceedings of an Asian – U.S. Workshop on Shrimp Culture. The Oceanic Institute, Hawaii, pp. 16 – 28. Mai, K., Mercer, J.P., Donlon, J., 1995. Comparative studies on the nutrition of two species of abalone, Haliotis tuberculata L. and Haliotis discus hannai Ino: IV. Optimum dietary protein level for growth. Aquaculture 136, 165 – 180. Marais, P.G., Van Der Merwe, H.J., Dutoit, J.E.J., 1991. The effect of compensatory growth on food intake, growth rate, body composition and efficiency of feed utilization in Dorper sheep. S. Afr. J. Anim. Sci. 21, 80 – 88. Mersmann, H.J., MacNeil, M.D., Seideman, S.C., Pond, W.G., 1987. Compensatory growth in finishing pigs after feed restriction. J. Anim. Sci. 64, 752 – 764. Quinton, J.C., Blake, R.W., 1990. The effect of feed cycling and ration level on the compensatory growth response in rainbow trout, Oncorhynchus mykiss. J. Fish Biol. 37, 33 – 41. Schwarz, F.J., Plank, J., Kirchgessner, M., 1985. Effect of protein or energy restriction with subsequent realimentation on performance parameters of carp (Cyprinus carpio L.). Aquaculture 48, 23 – 33.
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Sedgwick, R.W., 1979. Influence of dietary protein and energy on growth, food consumption and food conversion efficiency in Penaeus merguiensis De Man. Aquaculture 16, 7 – 30. Senckenberg, E., Roth, F.X., Kirchgessner, M., 1984. Einfluss einer Proteinrestriktion und -realimentation auf die N-Bilanz von Ferkeln. Arch. Tierernaehr. 34, 457 – 466. Shiau, S., Kwok, C., Chou, B., 1991. Optimal dietary protein level of Penaeus mondon reared in seawater and brackishwater. Nippon Suisan Gakkaishi 57, 711 – 716. Smith, L.L., Lee, P.G., Lawrence, A.L., Strawn, K., 1985. Growth and digestibility by three sizes of Penaeus vannamei Boone: the effects of dietary protein level and protein source. Aquaculture 46, 85 – 96. Summers, J.D., Spratt, D., Atkinson, J.L., 1990. Restricted feeding and compensatory growth for broilers. Poult. Sci. 69, 1855 – 1861. SYSTAT, 1992. SYSTAT for Windows: Statistics Version 5. (SYSTAT Inc. Evanston). Wilson, P.N., Osbourn, D.F., 1960. Compensatory growth after undernutrition in mammals and birds. Biol. Rev. 35, 324 – 363. Winchester, C.F., Hiner, R.L., Scarborough, V.C., 1957. Some effects on beef cattle of protein and energy restriction. J. Anim. Sci. 16, 426 – 436. Wu, L., Dong, S., Wang, F., Tian, X., 2000. Compensatory growth response following period of starvation in Chinese shrimp, Penaeus chinensis Osbeck. J. Shellfish Res. 19, 717 – 722. Wu, L., Dong, S., Wang, F., Tian, X., Ma, S., 2001. The effect of previous feeding regimes on the compensatory growth response in Chinese shrimp, Fenneropenaeus chinensis. J. Crustacean Biol. 21, 559 – 565. Wyllie, D., Speer, V.C., Ewan, R.C., Hays, V.W., 1969. Effects of starter protein level on performance and body composition of pigs. J. Anim. Sci. 29, 433 – 438. Xu, X., Li, A., 1988. Studies on the daily requirements and optimum contents of protein, carbohydrate, fiber and fat in the compound diet of Penaeus orientalis. Mar. Sci. 11, 1 – 6 (in Chinese). Xue, M., Li, A., Dong, S., Zhang, X., 1998. Studies on the optimum DP/DE for different sizes of Penaeus chinensis. J. Oceanogr. Univ. Qingdao 28, 245 – 252. Zimmerman, D.R., Khajarern, S., 1973. Starter protein nutrition and compensatory responses in swine. J. Anim. Sci. 36, 189 – 194.
Effects of protein restriction with subsequent realimentation on growth performance of juvenile Chinese shrimp (Fenneropenaeus chinensis) Lixin Wu, Shuanglin Dong * Aquaculture Research Laboratory, Fisheries College, Ocean University of Qingdao, Qingdao, 266003, People’s Republic of China Received 15 June 2001; received in revised form 23 October 2001; accepted 23 October 2001
Abstract The effects of protein restriction in the diet with subsequent realimentation on growth responses of juvenile Chinese shrimp, Fenneropenaeus chinensis (initial mean wet weight 1.347 g), were investigated. The control group (Group C) was fed an adequate diet containing 44.6% crude protein and 18.5 kJ gross energy/g dry matter throughout the experiment. For treatment Groups T15 and T30, in the restriction phase (weeks 1 – 2) dietary crude protein contents were reduced to 15.0% and 29.3%, respectively, with constant energy supply, while in the realimentation phase (weeks 3 – 6) they were supplied with the same diet as the control group. Protein restriction led to significant decrease in specific growth rates and body weight of shrimp. However, when the shrimp were transferred from protein restriction to realimentation, they had significantly increased specific growth rates in terms of dry matter, protein and energy (SGRd, SGRp and SGRe) compared with the control shrimp. At the end of the experiment, the shrimp in Group T30 achieved complete growth compensation, while those in Group T15 were still significantly smaller than the controls. As dietary protein levels reduced, feed conversion efficiencies and apparent protein digestibility decreased, but feed intake and protein efficiency ratio increased. The shrimp responded to a change from protein restriction to realimentation by displaying improved feed conversion efficiencies (FCEd, FCEp and FCEe) compared with the controls, although those in Group T15 delayed in showing the enhanced FCE values. In the initial 2-week realimentation, the shrimp in Group T15 showed significantly higher feed intake, and lower apparent digestibility of dry matter and protein than those of the controls. There was no significant difference in protein efficiency ratio among all groups in the realimentation phase. The above results suggest that compensatory growth in Group T30 is mainly dependent on improved feed conversion efficiencies, while that in Group T15 is attributable to both improved feed conversion efficiencies and increasing feed intake. After 2-week restriction, the shrimp showed lower body crude protein, lipid and energy content, and higher moisture and ash content than the controls. However, during the course of *
Corresponding author. Tel.: +86-532-2032964; fax: +86-532-2894024. E-mail address: [email protected] (S. Dong).
0044-8486/02/$ - see front matter D 2002 Elsevier Science B.V. All rights reserved. PII: S 0 0 4 4 - 8 4 8 6 ( 0 1 ) 0 0 8 6 0 - 2
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realimentation, the differences between the previously protein restricted shrimp and the controls diminished. This indicates that compensatory growth after a period of protein restriction in juvenile Chinese shrimp was accompanied by a complete recovery in body composition and energy content. D 2002 Elsevier Science B.V. All rights reserved. Keywords: Fenneropenaeus chinensis; Protein restriction; Compensatory growth; Feed consumption; Feed utilization; Body composition
1. Introduction The return to adequate feeding conditions following a period of starvation or undernutrition will often result in animals displaying a rapid growth spurt, known as compensatory or catch-up growth, which is known to occur in a wide range of mammals, including humans and domestic animals, and birds (Wilson and Osbourn, 1960; Ashworth and Millward, 1986; Mersmann et al., 1987; Summers et al., 1990; Marais et al., 1991). Since 1970s, studies on the compensatory growth in aquatic animals have become a highlighted subject, due to the fact that this phenomenon is not only of ecophysiological significant, but also of implications for aquaculture (Quinton and Blake, 1990; Jobling et al., 1994; Hayward et al., 1997). Nutrient composition in diet is one of the factors influencing an animal’s ability to recover from the effects of undernutrition, among which the most attention has been paid to protein restriction (Wilson and Osbourn, 1960). There have been a number of investigations on farm animals showing that a complete recovery in body weight was obtained after a period of protein restriction (Winchester et al., 1957; Zimmerman and Khajarern, 1973; Campbell and Dunkin, 1983). For aquatic animals, a considerable number of studies on the effects of dietary protein levels on growth performances have been conducted, but the possible effects of previous restriction on compensatory growth response are almost unknown, except for the work with common carp indicating some recovery in carcass composition after realimentation (Castell and Budson, 1974; Colvin, 1976; Schwarz et al., 1985; Shiau et al., 1991; Koshio et al., 1993; Mai et al., 1995). The Chinese shrimp (Fenneropenaeus chinensis), widely distributed along the coast of China, is a key species in the natural fishery community, and is the most important commercial shrimp species cultured in China, comprising approximately 80% of total shrimp production per year (Liu, 1990). Previous work with Chinese shrimp has revealed that compensatory growth can be elicited after a period of feed deprivation (Wu et al., 2000, 2001). This study was designed to determine the effect of feeding limited crude protein followed by an adequate diet supply on growth performance of this shrimp, with particular respect to compensatory growth.
2. Materials and methods 2.1. Diets Three test diets were prepared containing 15.0%, 29.3% and 44.6% crude protein (dry weight basis). Cod liver oil and corn starch were adjusted to maintain similar dietary
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energy content. Diets were prepared by mixing dry ingredients and water (2:1, w/w), then pellet type diets were produced through a meat grinder with a 1.6 mm die. The diets were then oven-dried (40 jC for 12 h) to approximately 8% moisture and stored at 20 jC until used. The formulation and proximate composition of the experimental diets are shown in Table 1. 2.2. Experimental design Completely randomized design was used in this growth experiment. The experiment lasted for 6 weeks and was divided into a restriction period (weeks 1 – 2) and a realimentation period (weeks 3– 6). Shrimp in Group C (control) were fed a standardized diet (D45) with 44.6% crude protein in excess ration throughout the trial period. In treatment Group T15 and T30, the crude protein supply was reduced to 15.0% (D15) and 29.3% (D30), respectively, during the restriction period. In the realimentation phase, shrimp previously fed the protein restriction diets were fed the same feed as the controls.
Table 1 Ingredient composition and proximate analysis (dry weight basis) of the experimental diets Ingredients (%)
Experimental diets D15
D30
D45
Casein Fish meal Shrimp meal Wheat flour Corn starch Carboxymethyl-cellulose Peanut oil Cod liver oil Cholesterol Soybean lecithin Vitamin mixa Mineral mixb Chromic oxide
0.0 15.0 5.0 19.5 40.0 5.0 1.0 5.0 1.0 2.0 2.0 4.0 0.5
10.8 22.5 5.0 19.5 23.7 5.0 1.0 3.0 1.0 2.0 2.0 4.0 0.5
21.6 30.0 5.0 19.5 6.9 5.0 1.0 1.5 1.0 2.0 2.0 4.0 0.5
Proximate analysis (means of triplicate) Crude protein (%) Crude lipid (%) Ash (%) Gross energy (kJ g 1)
15.0 10.4 8.4 18.2
29.3 8.7 10.4 18.3
44.6 7.6 12.3 18.5
a Vitamin mix, each 1000 g of diet contained: thiamin – HCl, 60 mg; riboflavin, 100 mg; folic acid, 10 mg; pyridoxine – HCl, 140 mg; niacin, 400 mg; calcium pantothenate, 140 mg; choline chloride, 4000 mg; inositol, 4000 mg; ascorbic acid, 4000 mg; biotin, 2 mg; U-amino benzoic acid, 150 mg; a-tocopherol, 400 mg; menadione, 34 mg; cyanocobalamine, 0.8 mg; retinol acetate, 150,000 IU; cholecalciferol, 60,000 IU. b Mineral mix, each 1000 g of diet contained: Ca(H2PO4)2, 8.800 g; CaCO3, 8.240 g; K2HPO4, 4.000 g; NaH2PO4, 11.200 g; MgSO47H2O, 5.095 g; KCl, 1.600 g; FeSO47H2O, 0.400 g; AlCl6H2O, 0.016 g; ZnSO47H2O, 0.432 g; MnSO4H2O, 0.080 g; CuSO45H2O, 0.008 g; CoCl26H2O, 0.112 g; KI, 0.016 g; Na2SeO3, 0.001 g.
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2.3. Rearing condition A static-water system consisting of 30 aquaria (45 30 30 cm, water volume 35 l) with aeration was used in this experiment. Seawater was filtered by composite sand filters. For each aquarium, two thirds of the seawater was replaced daily. The aquaria were cleaned thoroughly at the end of the fourth week. During the experiment, dissolved oxygen was maintained above 6.0 mg l 1, water temperature at 24.0 F 0.5 jC, salinity ranged from 30x to 33x, pH from 7.8 to 8.2, and photoperiod was 14L:10D. 2.4. Source and acclimation of experimental shrimp The experiment was carried out between 12 August and 23 September 2000 at the Laboratory of Aquaculture Ecology, Ocean University of Qingdao, Qingdao, P. R. China, using Chinese shrimp (F. chinensis) obtained from the Hongdao Shrimp Breeding Farm, Qingdao. The shrimp were initially held in a fiberglass tank (100 100 80 cm) for 3 days, and were then transferred into 30 aquaria (each aquarium held six shrimp) for 1-week acclimation, during which the water temperature was maintain at 24 jC and the shrimp were fed three times a day on the standardized pellet diet (control diet). 2.5. Experimental procedure After 12-h feed deprivation, 150 size-selected shrimp with initial weight range 1.215 – 1.477 g (1.347 F 0.010 g: mean F SE) were pooled into a large fiberglass tank. From the pooled shrimp, three groups of 10 individuals each were randomly sampled for the analysis of initial body composition. The remains (120 shrimp) were randomly selected, individually weighed and stocked into 30 aquaria with each aquarium holding four individuals, and then 10 aquaria were randomly allotted to each experimental group. For the analysis of body composition, three aquaria were randomly sampled at the end of the restriction period and at the end of 2-week realimentation, respectively, and thus four aquaria remained in each treatment during the last 2 weeks of the experiment. The shrimp in each aquarium were individually weighed every 2 weeks, following feed deprivation for 12 h. To remove excess moisture, the shrimp were carefully blotted with paper towel and weighed to the nearest 0.001 g. During the course of the experiment, shrimp were hand-fed at excess ration three times daily (at 06:00, 12:00 and 18:00 h) for each group. Each meal lasted approximately 2 h and any uneaten feed was collected, dried at 70 jC and weighed every 2 weeks. Twice a day, intact faeces were collected from each aquarium by pipetting, freeze-dried immediately and held at 20 jC until analyzed. 2.6. Biochemical analysis The shrimp, faeces and uneaten feed, respectively, from each aquarium were pooled as a sample. Before chemical composition analysis, all the dried samples of shrimp, faeces
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and feed were homogenized and re-stored at 70 jC to constant weight. Crude protein in sample was determined by the micro-Kjeldahl method, lipid by ether extraction using a Soxhlet system, ash by combustion at 550 jC for 12 h (AOAC, 1984), and gross energy content by 1281 Oxygen Bomb Calorimeter (Parr Instrument, USA). The concentration of Cr2O3 added to the diets to estimate the apparent digestibility was determined as described by Furukawa and Tsukahara (1966). 2.7. Calculation of data The following parameters were used to evaluate shrimp growth: Specific growth rate in wet weight ðSGRw : %day1 Þ ¼ 100 ðlnW2 lnW1 Þ=t Feed intake ðFI : % body weight day1 Þ ¼ 100 Df =½t ðW1 þ W2 Þ=2 Feed conversion efficiency in wet weight ðFCEw : %Þ ¼ 100 ðW2 W1 Þ=Df Protein efficiency ratio ðPER : %Þ ¼ 100 ðW2 W1 Þ=Dp where W2 and W1—final and initial wet weight (g) of the shrimp within a measuring interval; t—the measuring interval (days); Df—dry diet intake (g); Dp—dry protein intake (g). Specific growth rates and feed conversion efficiencies in dry matter (SGRd and FCEd), protein (SGRp and FCEp) and energy (SGRe and FCEe) were calculated similarly. Moult increment was defined as MI (g)=(W2 W1)/Nm, where W2 and W1 are the final weight and initial weight (g) of shrimp within a measuring interval, Nm is the number of moults for each shrimp; intermoult period as IP (days) = T/Nm, where T is the measuring interval (days), Nm is the number of moults for each shrimp. Apparent digestibility of dry matter, protein and energy were calculated as follows: % apparent digestibility of dry matter ðADd Þ ¼ ð1 % Cr2 O3 in diet=% Cr2 O3 in faecesÞ 100 % apparent digestibility of protein ðADp Þ or energy ðADe Þ % protein ðor energy contentÞ in faeces=% Cr2 O3 in faeces ¼ 1 100 % protein ðor energy contentÞ in diet=% Cr2 O3 in diet
2.8. Statistical analysis Statistical analysis was performed using SYSTAT statistical software (SYSTAT, 1992). Data from each treatment were subjected to one-way ANOVA. When overall differences were significant at the 0.05 level, Duncan’s multiple range test was used to compare the mean values among treatments.
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3. Results 3.1. Survival and growth All groups showed high survival (more than 90%) and the values among the three groups were not significantly different, indicating that different feeding schedules did not affect survival (Table 2). The mean body weights of Chinese shrimp reared under various feeding schedules during the course of the experiment are shown in Table 2. At the end of the protein restriction period, there were significant differences in body weight among shrimp fed the different experimental diets: the shrimp fed the control diet (44.6% protein) had the highest body weight, while those fed 15.0% protein diet had the lowest body weight. After 2 weeks of realimentation, no significant difference in body weight was observed between the shrimp in Group T30 and C (the control), whereas the body weight of shrimp in Group T15 was still significantly lower than that of the control shrimp, and this situation of body weight maintained till the termination of the experiment. As Fig. 1 illustrates, during the period of protein restriction, specific growth rate in terms of wet weight (SGRw), dry matter (SGRd), protein (SGRp) and energy content (SGRe) markedly increased with dietary protein content. During the first 2 weeks of realimentation, the previously protein-restricted shrimp displayed significantly higher SGRd, SGRp and SGRe than the controls, and there seemed to be a tendency for these values to decrease with increase in severity of protein restriction. During the last 2 weeks of the experiment, SGRd, SGRp and SGRe of the shrimp in Group T15 were significantly higher than those of shrimp in other two groups, while no significant differences in these SGR values were found between the shrimp previously fed 29.3% protein diet and the controls fed 44.6% protein diet continuously. Within each measuring interval (2 weeks) of realimentation, there was no significant difference in SGRw among the shrimp of all groups. 3.2. Moult increment and intermoult period The data on moult increment and intermoult period are presented in Table 3. There was no significant difference in moult increment among the shrimp reared under the three
Table 2 Growth and survival of juvenile Chinese shrimp held on the three feeding schedules during the course of the experiment (mean F SE, n = 4)1 Treatments
T15 T30 C (control) 1
Body weight (g)
Survival (%)
Initial
After restriction
After 2-week realimentation
Final
1.352 F 0.006 1.354 F 0.006 1.336 F 0.009
1.678 F 0.032a 1.840 F 0.025b 1.946 F 0.030c
2.310 F 0.105a 2.578 F 0.023b 2.626 F 0.047b
2.894 F 0.143a 3.205 F 0.046b 3.217 F 0.070b
Values with different superscripts in the same column are significantly different ( P < 0.05).
93.75 F 6.25 100.00 F 0.00 100.00 F 0.00
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Fig. 1. Specific growth rates in terms of wet weight (SGRw), dry matter (SGRd), protein (SGRp) and energy (SGRe) for juvenile Chinese shrimp held on the three feeding schedules during the course of experiment. Means with different letters within each period are significantly different ( P < 0.05), and bars indicate standard errors of the means.
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Table 3 Mean moult increment (MI, g)1, mean intermoult period (IP, days)2 for juvenile Chinese shrimp held on the three feeding schedules during the course of the experiment (mean F SE, n = 4)3 Parameters
MI (g)
IP (days)
Groups
T15 T30 C (control) T15 T30 C (control)
Time (weeks) 0–2
3–4
5–6
0.266 F 0.030 0.268 F 0.019 0.266 F 0.017 11.4 F 1.0a 8.4 F 0.4b 6.1 F 0.3c
0.417 F 0.033 0.430 F 0.022 0.376 F 0.017 8.6 F 1.4 8.2 F 0.2 7.8 F 0.3
0.366 F 0.066 0.316 F 0.029 0.340 F 0.039 7.7 F 0.8 7.1 F 0.4 8.2 F 0.7
1 Mean molt increment (g)=(W2 W1)/Nm, where W2 and W1 are final and initial wet weight (g) of the shrimp within a measuring interval; Nm is the number of moults for each shrimp. 2 Mean intermoult period (days) = T/Nm, where T is the measuring interval (days); Nm is the number of moults for each shrimp. 3 Values with different superscripts in the same column are significantly different ( P < 0.05).
feeding schedules within each measuring interval of the experiment. During the period of protein restriction, intermoult period significantly prolonged with decrease in dietary protein content, but no significant difference in intermoult period was observed among the shrimp of all experimental groups during the realimentation period. 3.3. Apparent digestibility The effects of feeding schedules on the apparent digestibility of juvenile Chinese shrimp are depicted in Fig. 2. Within each measured interval of the experiment, there were no significant differences in apparent energy digestibility (ADe) among all groups, and also no significant differences in apparent digestibility of dry matter (ADd) and protein (ADp) between Group T30 and C. During the protein restriction phase, a marked depression in ADp for shrimp fed the lowest protein content diet was observed, while there was no effect of dietary protein content on ADd. During the first 2 weeks of realimentation, both ADp and ADd were significantly lower in Group T15 than in Group T30 and C. However, during the last 2 weeks of the experiment these digestibility values for Group T15 adjusted to those for the other two groups. 3.4. Feed intake As shown in Fig. 3, in the protein restriction phase, feed intake significantly increased as the protein content decreased. During the first 2 weeks of realimentation, there was no significant difference in feed consumption between the shrimp in Group T30 and C, but the shrimp previously fed 15.0% protein diet still displayed significantly higher feed intake than those in the other two groups. No significant difference in feed intake was found among the shrimp in all groups during the last 2 weeks of the experiment.
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Fig. 2. Apparent digestibility of dry matter (ADd), protein (ADp) and energy (ADe) for juvenile Chinese shrimp held on the three feeding schedules during the course of experiment. Means with different letters within each period are significantly different ( P < 0.05), and bars indicate standard errors of the means.
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Fig. 3. Feed intake (FI) of juvenile Chinese shrimp held on the three feeding schedules during the course of experiment. Means with different letters within each period are significantly different ( P < 0.05), and bars indicate standard errors of the means.
3.5. Protein efficiency ratio During the course of protein restriction, shrimp fed the lowest protein diet (15.0%) had significantly higher protein efficiency ratio (PER) than those fed higher protein diets (29.3% and 44.6%). There were no significant differences in PER among the shrimp in all groups within each growth interval of realimentation (Fig. 4).
Fig. 4. Protein efficiency ratio (PER) for juvenile Chinese shrimp held on the three feeding schedules during the course of experiment. Means with different letters within each period are significantly different ( P < 0.05), and bars indicate standard errors of the means.
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353
Fig. 5. Feed conversion efficiency in terms of wet weight (FCEw), dry matter (FCEd), protein (FCEp) and energy (FCEe) for juvenile Chinese shrimp held on the three feeding schedules during the course of experiment. Means with different letters within each period are significantly different ( P < 0.05), and bars indicate standard errors of the means.
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3.6. Feed conversion efficiency In the protein restriction phase, feed conversion efficiency in terms of wet weight (FCEw), dry matter (FCEd), protein (FCEp) and energy (FCEe) significantly improved with increased dietary protein level. During the first 2 weeks of realimentation, FCEd, FCEp and FCEe were significantly higher in T30-treated shrimp than those in T15-treated shrimp and the controls, whereas within the last 2 weeks of realimentation these FCE values for T15treated shrimp were significantly higher than those for the shrimp in Group T30 and C. No significant difference in FCEw was observed among the shrimp in all groups in the whole realimentation phase (Fig. 5). 3.7. Body composition and energy content The data on proximate body composition and energy content are given in Table 4. At the end of the restriction phase, significantly higher percentages of body moisture and crude ash, and lower percentages of body crude protein, crude lipid and energy content were found in protein restricted shrimp than in those fed the control diet (44.6% protein content), although these body composition values were not significantly different between the T15- and T30-treated shrimp. After 2 weeks of realimentation, the shrimp previously fed 29.3% protein diet restored their body composition and energy content to the levels not significantly different from those of the control shrimp, whereas all these biochemical parameters, except for crude ash, in the shrimp previously fed 15.0% protein diet were still significantly lower than in the control shrimp. At the end of the realimentation, there were no significant differences in body composition and energy content among the shrimp in all experimental groups.
Table 4 Body composition and energy content of juvenile Chinese shrimp held on the three feeding schedules at different times of the experiment (mean F SE, n = 4)1 Time
Treatments
Moisture2
Protein2
Lipid2
Ash2
Energy3
Initial After restriction
– T15 T30 C (control) T15 T30 C (control) T15 T30 C (control)
75.12 F 0.12 78.45 F 0.28b 77.65 F 0.41b 75.40 F 0.38a 77.52 F 0.30b 75.13 F 0.17a 75.76 F 0.28a 75.48 F 0.44 76.14 F 0.20 75.37 F 0.29
16.97 F 0.08 14.42 F 0.18a 15.13 F 0.28a 16.77 F 0.26b 15.30 F 0.20a 16.65 F 0.11b 16.77 F 0.20b 16.56 F 0.30 16.44 F 0.14 16.69 F 0.19
2.55 F 0.10 1.86 F 0.07a 1.82 F 0.12a 2.42 F 0.05b 1.88 F 0.11a 2.45 F 0.13b 2.33 F 0.08b 2.52 F 0.12 2.54 F 0.10 2.39 F 0.07
2.61 F 0.06 2.78 F 0.04b 2.80 F 0.05b 2.61 F 0.04a 2.75 F 0.04 2.73 F 0.06 2.81 F 0.07 2.59 F 0.08 2.50 F 0.08 2.57 F 0.06
4.814 F 0.023 3.887 F 0.050a 4.022 F 0.074a 4.614 F 0.071b 4.028 F 0.053a 4.701 F 0.032b 4.567 F 0.052b 4.640 F 0.083 4.689 F 0.039 4.801 F 0.056
After 2-week realimentation Final
1 2 3
Values with different superscripts in the same column are significantly different ( P < 0.05). Values were expressed as % wet weight. Values were expressed as kJ g 1 wet weight.
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4. Discussion In the present study, the mean specific growth rate in terms of wet weight (SGRw) of the shrimp fed the control diet (44.6% protein content) was approximately 2.10% day 1, which is comparable to those (1.54 –2.46% day 1) reported for similar-sized penaeids (Alava and Lim, 1983; Xu and Li, 1988; Xue et al., 1998). It appears that the control diet prepared for this study was nutritionally adequate to support good growth of juvenile Chinese shrimp. During the protein restriction period, the mean specific growth rate in terms of wet weight (SGRw), dry matter (SGRd), protein (SGRp) and energy (SGRe) of juvenile Chinese shrimp significantly decreased with reduction in the amount of protein in the diet, which is in general agreement with the results of previous studies carried out on a range of shrimp species (Sedgwick, 1979; Smith et al., 1985; Shiau et al., 1991; Koshio et al., 1993). Consequently, at the end of restriction phase, the shrimp fed the lower protein content diets (D15 and D30) were significantly smaller than the controls. Upon realimentation, however, the SGR (SGRd, SGRp and SGRe, except for SGRw) of the previously protein-restricted shrimp were markedly greater than those of the controls, indicating that there was a compensatory growth response. At the end of the realimentation phase, the shrimp in Group T30 achieved complete growth compensation, in that they caught up in body weight to the controls fed 44.6% protein content diet (D45) throughout the experiment. Though the shrimp in Group T15 were still significantly smaller than the controls at the end of the experiment, the possibility that they can also fully regain the body weight lost during the restriction period cannot be excluded from the present study, since in the last 2 weeks of the experiment the SGRd, SGRp and SGRe of the shrimp in Group T15 were still significantly higher than those of the controls (Fig. 1). Thus, an experimental design incorporating a longer realimentation period would be necessary to determine when the SGR values for T15-treated shrimp decline to the levels not significantly different from those of the controls. Due to differences in the quantity of dietary protein, quality of the protein, ratio of dietary protein to energy and species-specific differences, the effects of dietary protein content on carcass composition in crustaceans and fishes seem to be inconsistent (Dabrowski, 1977; Alava and Lim, 1983; Hubbard et al., 1986). In the present study, the average body crude protein, lipid, and energy contents of F. chinensis were positively related to the dietary protein content, whereas body moisture and ash contents significantly decreased as dietary protein content increased (Table 4). Furthermore, the results of this study indicated that during the course of realimentation the differences in body composition and energy content between the previously protein-restricted shrimp and the control shrimp diminished, which is similar to the findings reported for common carp and pig (Wyllie et al., 1969; Zimmerman and Khajarern, 1973; Schwarz et al., 1985). This suggests that compensatory growth following a period of protein restriction in Chinese shrimp was accompanied by a complete recovery in body composition and energy content. Previous investigations on a variety of shrimp and fish have indicated a reduced apparent protein digestibility on diets with very low crude protein content as compared to high amounts (Kitamikado et al., 1964; Smith et al., 1985; Shiau et al., 1991; Koshio et al., 1993). A similar result was obtained in the present study, i.e. the shrimp fed the 15%
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protein content diet (D15) with constant energy supply digested the dietary protein less well than those fed the higher protein content diets (D30 and D45). Furthermore, the shrimp previously fed D15 maintained the lower apparent protein digestibility for 2 weeks in the realimentation phase (Fig. 2), which seems to be consistent with the findings reported for common carp (Schwarz et al., 1985). Nevertheless, in experiments on pigs a rather improved protein digestibility was observed during realimentation (Gadeken et al., 1983; Senckenberg et al., 1984). It is likely that the differences in responses of protein digestibility result from variations in the severity and duration of protein restriction, quality of diet, and interspecific differences. The results of the present study with juvenile Chinese shrimp appear to be in accordance with the general mechanisms for a range of shrimp (Deshimaru and Yone, 1978; Sedgwick, 1979; Alava and Lim, 1983; Shiau et al., 1991), in which feed intake and protein efficiency ratio decreased, and feed conversion efficiencies (FCEs) increased as dietary protein content increased to a certain extent. However, when changed from protein restriction to realimentation, the previously restricted shrimp displayed better feed conversion efficiencies (FCEd, FCEp and FCEe, except for FCEw) than the controls, although those previously fed 15.0% protein content diet (D15) delayed showing improved feed conversion efficiencies (Fig. 5). The data on feed intake indicated that, upon a return to realimentation, feed intake of the shrimp previously fed D15 was still significantly higher than that of the controls, but the shrimp previously fed D30 showed the same feed intake as the controls. There was no significant difference in the protein efficiency ratio among the shrimp of all groups in the realimentation phase. The analysis based on the above results of feed intake, feed conversion efficiencies and protein efficiency ratio, combining the previously noted digestibility data suggests that compensatory growth for T30-treated shrimp is mainly dependent on improved feed conversion efficiencies, while that for T15-treated shrimp is attributable to both the improved feed conversion efficiencies and increasing feed intake. It has been well documented in decapoda crustaceans that poor diets can reduce the moult increment and lengthen the intermoult period (reviewed by Hartnoll, 1982). For example, individual Cherax destructor reared on a low protein diet had significantly smaller moult increments and longer intermoult periods compared with those fed on a high protein diet (Jones et al., 1996). However, the present study with Chinese shrimp demonstrated that during the restriction period there was no effect of dietary protein content on the moult increment, although intermoult period also significantly lengthened as dietary protein level decreased. It is, therefore, needed to further investigate whether or not the effects of diets on the moult increment are related to dietary composition, and/or interspecific differences.
Acknowledgements This study was subsidized by funds from the Chinese National Science Foundation for Talent Youths (Grant no. 39725023) and the Major State Basic Research Projects of China (Grant no. G1999012011). We thank Hongdao Shrimp Breeding Farm, Qingdao, P. R. China, for providing the shrimp used in this experiment.
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