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Growth, faecal production, nitrogenous excretion and energy budget of juvenile yellow grouper (Epinephelus awoara) relative to ration level
Aquaculture 264 (2007) 228 – 235 www.elsevier.com/locate/aqua-online
Growth, faecal production, nitrogenous excretion and energy budget of juvenile yellow grouper (Epinephelus awoara) relative to ration level Lihua Sun ⁎, Haoru Chen, Liangmin Huang South China Sea Institute of Oceanology, Chinese Academy of Sciences, 164 Xingang west Road, Guangzhou 510301, PR China Marine Biology Research Station at Daya Bay, Chinese Academy of Sciences, Dongshan village Nan'ao town, Shenzhen 518120, PR China Received 24 August 2006; received in revised form 6 November 2006; accepted 20 December 2006
Abstract Growth, faecal production, nitrogenous excretion and energy budget of juvenile yellow grouper (initial body weight 5.5 g or so) at various ration levels (starvation, 0.5%, 1% and 2% of initial body weight per day, and satiation) were investigated in this study. Faecal production (f, mg g− 1 d− 1) and nitrogenous excretion (u, mg g− 1 d− 1) increased markedly with increased ration level (RL, % per day), described as f = 0.483RL + 0.112 for faecal production and u = 0.218RL + 0.219 for nitrogenous excretion, respectively. Feed absorption efficiency (FAE, %) increased as ration increased with ranges of 91.4–94.0%, 95.6–97.3% and 96.5–97.6% for FAEd, FAEp and FAEe, respectively, but all of the variations were small. Relationships between specific growth rate in wet weight (SGRw, % per day), dry weight (SGRd, % per day), protein (SGRp, % per day), energy (SGRe, % per day) and ration level (RL, % per day) were linear and described as simple equations SGRw = 0.738RL–0.764, SGRd = 0.871RL–0.928, SGRp = 0.904RL–0.966 and SGRe = 1.038RL–1.060. Feed conversion efficiency in wet weight (FCEw, %), dry weight (FCEd, %), protein (FCEp, %) and energy (FCEe, %) all increased as ration increased and maximized at ad libitum ration level. Energy budgets of juvenile Epinephelus awoara at satiation ration level was: 100C = 2F + 4U + 75R + 19G or 100A = 80R + 20G, where C is food energy, A is assimilated energy, F is faeces energy, U is excretion energy, R is metabolism energy and G is growth energy. © 2007 Elsevier B.V. All rights reserved. Keywords: Juvenile yellow grouper (Epinephelus awoara); Ration level; Growth; Faecal production; Nitrogenous excretion; Energy budget
1. Introduction Yellow grouper, Epinephelus awoara, is a rare, but economically important marine species distributed in south eastern China Sea, where there are island reefs. The products from yellow grouper are salable in home and overseas markets because of the palatability and ⁎ Corresponding author. Tel./fax: +86 755 8442 2460. E-mail address: [email protected] (L. Sun). 0044-8486/$ - see front matter © 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.aquaculture.2006.12.036
nutritional quality of its flesh and its high economic value. Yellow grouper does not migrate long distances. So it is regarded as having a great potential for offshore cage culture. In recent years, yellow grouper has become an important cultured species in the coastal waters of southern China. Most seed for large-scale aquaculture is obtained by artificial breeding. In the artificial breeding of yellow grouper, especially during the period of using artificial formulated feed, one of the key issues is how to optimize ration to support fast
L. Sun et al. / Aquaculture 264 (2007) 228–235 Table 1 Chemical composition and energy content of the commercial eel formulated feed used during yellow grouper growth experiments (percentage by weight) Composition
Percentage of wet matter (%)
Percentage of dry matter (%)
Moisture Crude protein Crude lipid Ash Gross energy (kJ g− 1)
8.48 44.63 10.42 12.24 16.71
– 48.77 11.39 13.37 18.26
growth and feed conversion, and to reduce feed waste and water pollution. Thus, it is necessary to investigate the effects of ration level on yellow grouper growth, faecal production, nitrogenous excretion and energy budget. There are only a few publications on the biology of yellow grouper. Bo et al. (1993) studied the ageing, morphology and growth of larvae, fry and juvenile of yellow grouper. Zhou et al. (1994) investigated feeding conditions of larvae, fry and juvenile of yellow grouper in artificial culture. Dai and Zhao (1994) determined O2 consumption of yellow grouper. Qin et al. (2004) reported the pathogeny of ulcer disease in yellow grouper. Little, however, is known about the bioenergetics of this species, so growth, faecal production, nitrogenous excretion and energy budget of juvenile yellow grouper relative to ration were investigated in this paper. The study aimed to characterize the bioenergetics of juvenile yellow grouper, but also to provide a scientific basis for feeding management in the large-scale artificial breeding of yellow grouper. 2. Materials and methods 2.1. Experimental fish and diet Juvenile yellow grouper for the experiment were from the artificial breeding by the research group at the Marine Biology Research Station at Daya Bay, Chinese Academy of Sciences (MBRS). The experimental diet for juvenile yellow grouper was a commercial eel formulated feed (Grobest brand, Quanxing aquatic feed L.T.D.). The main components of this feed include fish meal from Peru, α-starch, yeast powder, FeSO4, ZnSO4·7H2O, CuSO4·5H2O, MnSO4, Na2SeO3, Vitamin A, Vitamin D3, Vitamin E, Vitamin K3, Vitamin C, Vitamin B1, Vitamin B2, Vitamin B6, Vitamin B12, niacin, folic acid, inositol, etc. The chemical composition of this diet is listed in Table 1. Before the start of feeding the diet was added with a fixed proportion of water (water: eel feed = 1:2) and made into pellets (diameter 2–3mm) suitable for fish feeding.
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2.2. Fish acclimation Juvenile yellow grouper belonging to the same batch and in good health were collected from outside breeding ponds at MBRS. About one hundred and eighty fish were transferred into four indoor concrete ponds with about forty-five fish per pond (2 m × 1 m × 1 m, water volume 1.6 M3) and acclimated for 2 weeks. Then fish of similar body size and showing normal feeding behavior were captured randomly from the indoor ponds, marked as described by Russell et al. (1996), and then placed randomly into rectangular transparent plastic tanks (60 cm × 45 cm × 40 cm, water volume 90 L) for further acclimation 1 week. A pilot trial was conducted to estimate the maximal ration during this period, which would provide experimental evidence for designing the ration levels used in the growth experiment. During the whole acclimation period, no fish died. Enough feed was provided to satiation as judged by visual inspection once a day (about 09:00). All seawater in each tank was replaced by fresh, filtered and wellaerated seawater every 3–4 days. Aeration was provided continuously except for the feeding time and dissolved oxygen was maintained above 6 mg l− 1. Temperature and salinity were monitored daily. During this period water temperature was 25.7–29.1 °C, salinity was 29.4– 33.2, and fish were subjected to a natural photoperiod regime with similar light conditions for all tanks. 2.3. Growth experiment Five ration levels were tested in the growth experiment: starvation, 0.5, 1, 2% of initial body weight per day, and ad libitum, with five replicates for each level and five fish for each replicate. In addition, another twenty fish were sampled for measurement of initial body composition and energy content. One hundred and fifty fish, which had been starved for 2 days, were captured, blotted of excess water weighed and then placed into individual experimental tanks at the start of the growth experiment. During the experiment fish (mean weight about 5.5 g) in each tank were subjected to the five prescribed ration levels ranging from starvation to an ad libitum ration equal to feeding the fish to satiation once a day (about 09:00). An excess of feed was fed to the satiation (ad libitum) ration group, the daily feed supplied was recorded, and the uneaten feed was collected 30 min after feeding by pipetting and then ovendried at 70 °C. Potential loss of uneaten feed was determined by placing feed in water for 30 min and then collecting, drying and weighing. The proportion of the
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Table 2 Body chemical composition (g g− 1 W.W.) and energy content (kJ g− 1 W.W.) of juvenile yellow grouper at different ration levels (RL, % per day) Ration level
Starvation
0.5
1
2
Ad libitum
Moisture content Protein content Lipid content Ash content Energy content
76.29 ± 0.85 c 14.69 ± 0.59 a 2.66 ± 0.10 a 6.33 ± 0.44 c 4.14 ± 0.13 a
76.13 ± 0.54 c 15.18 ± 0.27 bc 2.57 ± 0.17 a 5.92 ± 0.35 c 4.16 ± 0.06 a
75.94 ± 0.62 c 15.39 ± 0.38 bc 2.82 ± 0.12 ab 5.50 ± 0.34 b 4.37 ± 0.09 b
75.62 ± 0.63 ab 15.43 ± 0.32 ab 3.20 ± 0.14 ab 4.90 ± 0.20 a 4.51 ± 0.13 b
74.85 ± 0.69 a 16.02 ± 0.22 c 3.34 ± 0.17 b 4.84 ± 0.18 a 4.76 ± 0.08 c
Values (mean ± SD) in the same row with different letters are significantly different (P b 0.05).
food remaining was calculated and this value was used to adjust the amount of the feed intake. Faeces were collected twice a day by pipetting, ovendried at 70 °C, weighed, homogenized and stored at − 20 °C for later chemical and calorific analyses. All seawater in each plastic tank was replaced by fresh, filtered and well-aerated seawater every 4 days except that one water-replacement lasted 7 days, at the beginning and end of which period, water was sampled, and ammonia and urea contents in each tank were determined by the method of Chaney and Marbach (1962) and converted into energy by multiplying by 24.83 kJ g− 1 for ammonia and 23.03 kJ g− 1 for urea (Elliot, 1976a). Potential loss of nitrogenous compounds through bacterial action or diffusion was quantified by setting controls without fish and the value was used to adjust determined nitrogenous excretion. Aeration was provided continuously except during feeding and following faeces collecting, and dissolved oxygen was maintained above 6 mg l− 1. Temperature and salinity were monitored daily. During this period, water temperature was 25.2–28.4 °C, salinity was 30.2–33.6 and the experiment was conducted at the natural photoperiod conditions with similar light intensity for all tanks. The growth experiment lasted 21 days. After starvation for 2 days fish from the same tank were weighed, pooled, chopped, dried, reweighed, homogenized and then stored at − 20°C for later chemical and caloric analyses.
2.4. Chemical analysis Moisture contents of fish and feed were determined after oven-drying to constant weight at 105 °C for diet and 70 °C for fish. Protein contents of fish, faeces and feed were measured by the Kjeldahl method using an auto Kjeldahl system (BÜCHI K-370/K-437, Switzerland). Lipid contents of fish and feed were measured by ether extraction. Ash contents of fish and feed were determined by a muffle furnace at 550 °C for 8–10 h. Gross energy contents of fish, faeces and feed were measured by oxygen calorimetric bomb (model 1341EE, USA, calibrated by benzoic acid). For each variable, at least duplicate samples were determined and the mean of duplicate determination was taken as the result when the relative deviation was less than 2%. 2.5. Statistical analysis A one-way Analysis of Variance (ANOVA) followed by a multiple range test (Newman–Keuls) was used after previous determination of the normality and homescedasticity of the data. There are significant differences among various treatments when P b 0.05. Least squares regression was performed to evaluate the relationships between nitrogenous excretion, faecal production, specific growth rate and ration, and judged by coefficient of determination (R2) and residual analysis. Analysis of Covariance (ANCOVA) was made to investigate
Table 3 Nitrogenous excretion (u, mg g− 1 d− 1), faecal production (f, mg g− 1 d− 1) and feed absorption efficiency in dry weight (FAEd, %), protein (FAEp, %), energy (FAEe, %) of juvenile yellow grouper at different ration levels (RL, % per day) RL
Starvation
0.5
1
2
Ad libitum
u f FAEd a FAEp b FAEe c
0.18 ± 0.02 a 0.00 ± 0.00 a – – –
0.26 ± 0.03 b 0.42 ± 0.09 b 91.4 ± 1.8 a 95.6 ± 0.8 a 96.5 ± 0.7 a
0.43 ± 0.02 c 0.70 ± 0.10 c 92.2 ± 1.1 a 96.2 ± 0.4 a 96.9 ± 0.3 a
0.69 ± 0.08 d 1.01 ± 0.10 d 94.0 ± 0.5 b 97.2 ± 0.3 b 97.6 ± 0.3 b
0.77 ± 0.10 e 1.28 ± 0.23 e 93.6 ± 0.6 b 97.3 ± 0.3 b 97.6 ± 0.2 b
Values (mean ± SD) in the same row with different letters are significantly different (P b 0.05). a FAEd = 100 × (feed intake × dry matter content − faecal production) / feed intake × dry matter content. b FAEp = 100 × (feed intake × protein content − faecal production × protein content) / feed intake × protein content. c FAEe = 100 × (feed intake × energy content − faecal production × energy content) / feed intake × energy content.
L. Sun et al. / Aquaculture 264 (2007) 228–235 Table 4 Coefficients of the regression equation (Y = a + bRL) relating to specific growth rate in wet weight (SGRw, % per day), dry weight (SGRd, % per day), protein (SGRp, % per day) and energy (SGRe, % per day) as well as nitrogenous excretion (u, mg g− 1 d− 1) and faecal production (f, mg g− 1 d− 1) to ration level (RL, % per day) for juvenile yellow grouper Y
a
b
n
R2
P
u f SGRw SGRd SGRp SGRe
0.173 0.112 − 0.764 − 0.928 − 0.966 − 1.060
0.250 0.483 0.738 0.871 0.904 1.038
25 25 25 25 25 25
0.942 0.938 0.919 0.901 0.897 0.936
b0.01 b0.01 b0.01 b0.01 b0.01 b0.01
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lipid and energy contents, and a negative correlation for moisture and ash contents. 3.2. Nitrogenous excretion, faecal production and feed absorption efficiency Nitrogenous excretion, faecal production and feed absorption efficiency in dry weight, protein and energy of juvenile yellow grouper all increased as ration increased (Table 3). The relationship between nitrogenous excretion as well as faecal production and ration level could be described with a simple linear relationship as well as a power function (Table 4). 3.3. Specific growth rate and feed conversion efficiency
the effect of fish weight on growth across ration treatments. Data were expressed as mean ± SD of five replicate ration levels. The statistical analyses, using SPSS 11.0 for windows, were performed on tank means, with five replicate means per treatment. 3. Results 3.1. Body chemical composition and energy content The contents of moisture, protein, lipid, ash and energy in the body of juvenile yellow grouper at different ration levels are listed in Table 2. A positive correlation to ration level was observed for the protein,
Specific growth rate in wet weight (SGRw), dry weight (SGRd), protein (SGRp) and energy (SGRe) of juvenile yellow grouper increased with increased ration (Table 5). There was a positive, linear relationship between specific growth rate and ration (Table 4). ANCOVA showed that across ration treatments fish weight had no significant effect on SGRw (F = 0.237, P N 0.05), SGRd (F = 0.571, P N 0.05), SGRp (F = 0.515, P N 0.05) and SGRe (F = 0.484, P N 0.05). Feed conversion efficiency in wet weight, dry weight, protein and energy of juvenile yellow grouper also increased with increased ration and were highest at satiation ration (Table 5).
Table 5 Specific growth rate in wet weight (SGRw, % day− 1), dry weight (SGRd, % day− 1), protein (SGRp, % day− 1) and energy (SGRe, % day− 1) and feed conversation efficiency in wet weight (FCEw, %), dry weight (FCEd, %), protein (FCEp, %) and energy (FCEe, %) of juvenile yellow grouper at different ration levels (% per day) Ration level IBW (g per fish) SGRw b SGRd c SGRp d SGRe e FCEw f FCEd g FCEp h FCEe i
a
Starvation
0.5
1
2
Ad libitum
5.69 ± 0.75 a − 0.82 ± 0.14 a − 1.03 ± 0.26 a − 1.13 ± 0.22 a − 1.13 ± 0.19 a − − − −
6.36 ± 0.99 a − 0.35 ± 0.16 b − 0.40 ± 0.18 b − 0.38 ± 0.21 b − 0.51 ± 0.15 b − 66.58 ± 29.79 a − 20.20 ± 8.64 a − 24.71 ± 13.24 a − 24.99 ± 7.06 a
5.01 ± 0.78 a 0.07 ± 0.03 c 0.05 ± 0.14 c 0.10 ± 0.13 c 0.13 ± 0.11 c 6.93 ± 2.87 b 1.43 ± 3.84 b 3.60 ± 4.64 b 3.51 ± 2.80 b
5.04 ± 0.63 a 0.41 ± 0.12 d 0.46 ± 0.17 d 0.46 ± 0.12 d 0.63 ± 0.14 d 21.51 ± 6.56 b 6.34 ± 2.48 b 8.24 ± 2.29 b 8.75 ± 2.10 b
5.26 ± 0.86 a 1.24 ± 0.24 e 1.43 ± 0.26 e 1.46 ± 0.27 e 1.71 ± 0.30 e 49.89 ± 8.50 c 15.59 ± 2.64 c 20.78 ± 3.88 c 18.80 ± 2.49 c
Values (mean ± SD) in the same row with different letters are significantly different (P b 0.05). a IBW = initial body weight. b SGRw = 100 × [ln(final body weight) − ln(initial body weight)] / days of the experiment. c SGRd = 100 × [ln(final body weight × final dry matter content) − ln(initial body weight × initial dry matter content)] / days of the experiment. d SGRp = 100 × [ln(final body weight × final protein content) − ln(initial body weight × initial protein content)] / days of the experiment. e SGRe = 100 × [ln(final body weight × final energy content) − ln(initial body weight × initial energy content)] / days of the experiment. f FCEw = 100 × (final body weight − initial body weight) / feed intake. g FCEd = 100 × [(final body weight × final dry matter content) − (initial body weight × initial dry matter content)] / (feed intake × dry matter content). h FCEp = 100 × [(final body weight × final protein content) − (initial body weight × initial protein content)] / (feed intake × protein content). i FCEe = 100 × [(final body weight × final energy content) − (initial body weight × initial energy content)] / (feed intake × energy content).
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Table 6 Energy budgets a at different ration levels (RL, % per day) for juvenile yellow grouper Starvation b
RL −1
C (kJ g
−1
day )
0.000 ± 0.000
0.5
1
2
Ad libitum
0.087 ± 0.002
0.166 ± 0.002
0.320 ± 0.004
0.416 ± 0.072
As a percentage of C (%) F U R G
– 0.004 ± 0.001 0.044 ± 0.008 −0.048 ± 0.008
3.51 ± 0.68 b 6.80 ± 0.83 c 114.68 ± 7.75 c −24.99 ± 7.06 a
3.12 ± 0.33 b 5.79 ± 0.30 b 87.58 ± 2.85 b 3.51 ± 2.80 b
2.35 ± 0.25 a 4.81 ± 0.61 b 84.09 ± 2.20 b 8.75 ± 2.10 c
2.38 ± 0.21 a 4.19 ± 0.49 a 74.63 ± 2.43 a 18.80 ± 2.49 d
As a percentage of A (%) R G
– –
127.82 ± 7.69 c −27.82 ± 7.69 a
96.14 ± 3.08 b 3.86 ± 3.08 b
90.58 ± 2.27 b 9.42 ± 2.27 b
79.88 ± 2.65 a 20.12 ± 2.65 c
Values (mean ± SD) in the same row with different letters are significantly different (P b 0.05). a C = F + U + R + G or A = R + G (Brett and Groves, 1979), where C is food energy, A is assimilated energy, F is faeces energy, U is excretion energy, R is metabolism energy, calculated by difference R = C − F − U − G (Elliot, 1976b), and G is growth energy. b Values for the starving fish were expressed as kJ g− 1 day− 1.
3.4. Energy budget Energy budgets at each ration level for juvenile yellow grouper are shown in Table 6. The proportions of energy intake lost in faecal production and excretion were 2.38– 3.51% and 4.19–6.80%, respectively, and both proportions tended to decrease with an increase in ration size. As ration increased, the proportion of energy intake (or absorption) stored in body (growth) increased and was highest at satiation ration, whereas the proportions of energy intake (or absorption) spent in metabolism decreased and were lowest at satiation ration. 4. Discussion Faecal production of juvenile yellow grouper increased linearly with increased ration, which was consistent with the studies on bluegill sunfish Lepomis macrochirus (Gerking, 1955), bastard halibut Paralichthys olivaceus (Xian and Zhu, 2001a) and mullet Liza haematocheila (Xian and Zhu, 2001b) but different from the studies on south catfish Silurus meridionalis Chen (Xie and Sun, 1993) and cobia Rachycentron canadum (Sun et al., 2006), whose faecal production showed a curvilinear increase. Feed absorption efficiency in dry weight, protein and energy also tended to increase with ration level, though the variation was small, which agreed with a study of the cyprinid Phoxinus phoxinus (Cui and Wootton, 1988). However, the effect of ration on feed absorption efficiency will rarely be large as ration increases from low levels to ad libitum (Jobling, 1994). In some papers faecal production was also reported as a simple or exponential function of ration (Gerking, 1955; Allen and Wootton, 1982; Cui and Wootton, 1988).
Usually nitrogenous excretion increases with increased ration and a simple linear, power or exponential function has been used to describe the relationship (Savitz et al., 1977; Mortensen, 1985; Cui and Liu, 1990). Nitrogenous excretion for juvenile yellow grouper increased linearly as ration increased, which was similar to the results for largemouth bass Micropterus salmoides (Savitz et al., 1977), rainbow trout Oncorhynchus mykiss (Beamish and Thomas, 1984) and cyprinid P. phoxinus (Cui and Wootton, 1988). The relationship between growth and ration has usually been described by one of two patterns: one is a decelerating curve, which has been described by a variety of functions (Wayne et al., 1983; Zhu et al., 2001; Allen and Wootton, 1982; Tang et al., 2002; Cortes and Gruber, 1994; Xie et al., 1997; Rafail, 1968), and the other is a simple linear relationship (Niimi and Beamish, 1974; Paul et al., 1992, 1994; Cui et al., 1996). Cui et al. (1996) speculated that the curvilinear growth– ration relationship was caused by the inability of fish to convert food materials into body tissues at high rations efficiently and the relationship would be linear if: (1) the food intake or absorption (C–F) at the maximum ration was low, so that the decline in conversion efficiency did not occur; or (2) the fish could maintain a high foodconversion efficiency even at maximum ration. In this study the growth–ration relationship for juvenile yellow grouper produced a significant linear relationship and feed conversion efficiency also increased with increased ration. Low consumption but a high feed conversion efficiency at ad libitum ration might be the reasons for the linear growth-relationship of juvenile yellow grouper, which was in agreement with the studies on flathead sole Hippoglossoides elassodon (Paul et al., 1992), juvenile Pacific halibut Hippoglossus stenolepis
L. Sun et al. / Aquaculture 264 (2007) 228–235
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Table 7 Comparison of maximal ration level (RLmax) or maximal energy intake (Cmax), specific growth rate (SGRw) and energy budget among several fish species at satiation ration Fish species a
Yellow grouper (Epinephelus awoara)
Cobia (Rachycentron canadum)
Bastard habibut (Paralichthys olivaceus)
Rainbow trout (Oncorhynchus mykiss)
Initial average body weight (g) Temperature (°C) RLmax (% d− 1) / Cmax (kJ g− 1 d− 1) SGRw (% per day) As a percentage of C (%) F U R G As a percentage of A (%) R G Reference
5.47 25.2–28.4 2.49/0.42
9.91 27.2–30.4 12.84/1.50
2.27 24.0 6.39/1.55
3.62 11.4 3.04/0.37
1.24 2.38 4.19 74.63 18.80 79.88 20.12 Present study
5.08 7.07 75.91
6.62 0.95 5.52 44.31 49.21 47.38 52.62 Xian and Zhu (2000)
2.23 23.45
a
17.12
Sun et al. (2006)
35.68 40.87 46.61 53.39 Staples and Nomura (1976)
Fed on artificial formulated feed.
(Paul et al., 1994) and rainbow trout O. mykiss (Staples and Nomura, 1976). It is important for aquaculture to determine that whether the growth–ration relationship is linear or curvilinear. If it is curvilinear, feed conversion efficiency with increased ration usually shows a domed curve, in which case the ration that maximizes growth efficiency is an intermediate not a satiation ration, but if it is linear, feed conversion efficiency increases as ration increases, in which case the optimum feeding strategy would be that fish are fed to satiation to obtain both rapid growth and high feed conversion efficiency (Xie et al., 1997). The data on growth and feed conversion efficiency in the present study indicated that a satiation ration would maximize both growth rate and growth efficiency in juvenile yellow grouper at this ontogentic stage and given the artificial feed. Tang et al. (2003) calculated an average energy budget based on the published budgets of seven marine fish species fed satiation ration: 100A ¼ 71:5R þ 28:5G On the basis of this average energy budget, Tang et al. (2003) divided the mode of energy allocation into three styles: (1) Lower metabolism and higher growth, such as Schlegel's black rockfish Sebastes schlegeli and finespot goby Chaeturichthys stigmatias; (2) Higher metabolism and lower growth, such as black porgy Acanthopagrus schegeli and fat greenling Hexagrammos otakii; (3) Moderate metabolism and moderate growth, such as red seabream Pagrus major, tiger puffer Takifugu rubripes and chub mackerel Scomber japonicus.
Energy budget of juvenile yellow grouper at satiation ration in this paper was: 100A ¼ 80R þ 20G The proportion of assimilated energy spent in metabolism for juvenile yellow grouper was obviously higher than the average value. Referring to the energy budget modes of other marine fish the energy allocation mode of juvenile yellow grouper is a pattern of moderate metabolism and moderate growth with a tendency to higher metabolism and lower growth. Yellow grouper, whose natural habitat is areas with island reefs, were observed to consume little and hold still at the bottom of the tanks for a large part of time during the experiment. The large differences between the experimental conditions and the natural habitat may lead to stress in the experimental fish, with a consequent increase in metabolic rate and a decrease in food consumption. A study on the fat greenling H. otakii, whose natural habitat is also island reefs (Tang et al., 2003), showed a comparable phenomenon. However, for a given fish species, the growth–ration relationship and energy budget may be dependent on many factors such as experimental method (Tang et al., 2003), feed type or composition (Huisman and Valentijn, 1981; Cui et al., 1992, 1994; Jobling, 1994; Yang et al., 2003), body size (Niimi and Beamish, 1974; Staples and Nomura, 1976), water temperature (Elliot, 1976b; Malloy and Targett, 1994), etc. Further research is required to quantify these effects in juvenile yellow grouper. Table 7 lists the growth and energy budget of several fish species fed at maximum rations. A provisional explanation of bio-energetic mechanisms of the growth
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of different species can be based on their energy allocation patterns. Juvenile yellow grouper showed a low rate of food consumption combined with a small allocation of energy to growth. Consequently, their growth at maximum rations was low. Juvenile rainbow trout, O. mykiss, had a low rate of food consumption but allocated a higher proportion of energy to growth and consequently had a higher growth rate than juvenile yellow grouper (Staples and Nomura, 1976). Juvenile cobia, R. canadum, allocated a low proportion to growth but had high rates of food consumption and consequently showed a higher growth rate than rainbow trout (Sun et al., 2006). Juvenile bastard halibut, Paralichthys olivaceus, combined high rates of food consumption with a high proportion allocated to growth and so had high growth rates (Xian and Zhu, 2000). The ecological factors that select for particular patterns of food consumption and energy partitioning are still poorly understood. A better understanding of these factors may follow for the design of more effective holding and feeding regimes for species used in aquaculture. Acknowledgements The authors are grateful for the financial support by grant No. 2001A305020201 from the key project of Science and Technology of Guangdong Province, China. Thanks are given to three referees for their critical comments on the manuscript. References Allen, J.R.M., Wootton, R.J., 1982. The effect of ration and temperature on the growth of the three-spined stickleback, Gasterosteus aculeatus L. Journal of Fish Biology 20, 409–422. Beamish, F.W.H., Thomas, E., 1984. Effects of dietary protein and lipid on nitrogen losses in rainbow trout, Salmo gairdneri. Aquaculture 41, 359–371. Brett, J.R., Groves, T.D.D., 1979. Physiological energetics. In: Hoar, W.S., et al. (Ed.), Fish Physiology, vol. 8. Academic Press, New York, pp. 279–352. Bo, Z.L., Zhou, W.X., Xin, J., et al., 1993. Study on daily age, morphology and growth of larva, fry juvenile of Epinephelus awoara. Journal of Zhejiang College of Fisheries 12 (3), 165–173. Chaney, A.L., Marbach, E.P., 1962. Modified reagents for determination of urea and ammonia. Clinical Chemistry 8, 130–132. Cortes, E., Gruber, S.H., 1994. Effect of ration size on growth and gross conversion efficiency of young lemon sharks, Negaprion brevirostris. Journal of Fish Biology 44, 331–341. Cui, Y.B., Liu, J.K., 1990. Comparison of energy budget among six teleosts-I. food consumption, faecal production and nitrogenous excretion. Comparative Biochemistry and Physiology 96A (1), 163–171. Cui, Y., Wootton, R.J., 1988. Bioenergetics of growth of a cyprinid, Phoximus phoxinus (L.): the effect of ration, temperature and body size on food consumption, fecal production and nitrogenous excretion. Journal of Fish Biology 33, 431–443.
Cui, Y.B., Liu, X.F., Wang, S.M., et al., 1992. Growth and energy budget in young grass carp, Ctenopharyngodon idella Val., fed plant and animal diets. Journal of Fish Biology 41, 231–238. Cui, Y., Chen, S., Wang, S., 1994. Effect of ration size on the grown and energy budget of the grass carp, Ctenopharyngodon idella Val. Aquaculture 123, 95–107. Cui, Y., Hung, S.S.O., Zhu, X., 1996. Effect of ration and body size in the energy budget of juvenile white sturgeon[J]. Journal of Fish Biology 49, 863–876. Dai, Q.N., Zhao, L.L., 1994. Study on O2 consumption for Epinephelus awoara. Fisheries science (China) 13 (3), 6–9. Elliot, J.M., 1976a. Energy losses in the waste products of brown trout (Salmo truttaL.). Journal of Animal Ecology 45, 561–580. Elliot, J.M., 1976b. The energetics of feeding, metabolism and growth of brown trout (Salmo truttaL.). Journal of Animal Ecology 45, 923–948. Jobling, M., 1994. Fish Bioenergetics. Chapman and Hall, London. Gerking, S.D., 1955. Influence of rate of feeding on body composition metabolism of bluegill fish. Physiological Zoology 28, 267–282. Huisman, E.A., Valentijn, P., 1981. Conversation efficiencies in grass carp (Ctenopharyngodon idella Val.) using a feed for commercial production. Aquaculture 22, 279–288. Malloy, K.D., Targett, T.E., 1994. Effect of ration limitation and low temperature on growth, biochemical condition, and survival of juvenile summer flounder from two Atlantic coat nurseries. Transactions of the American Fisheries Society 123, 182–193. Mortensen, E., 1985. Population and energy dynamics of trout Salmo trutta in a small Danish stream. Journal of Animal Ecology 54, 869–882. Niimi, A.J., Beamish, F.W.H., 1974. Bioenergetics and growth of largemouth bass (Micropterus salmoides) in relation to body weight and temperature. Canadian Journal of Zoology 52, 447–456. Paul, A.J., Paul, J.M., Smith, R.L., 1992. Energy and ration requirements of flathead sole (Hippoglossoides elassodon Jordan and Gilbert, 1880) based on energy consumption and growth. ICES Journal of Marine Science 49, 413–416. Paul, A.J., Paul, J.M., Smith, R.L., 1994. Energy and ration requirements of juvenile Pacific halibut (Hippoglossus stenolepis) based on energy consumption and growth rates. Journal of Fish Biology 44, 1023–1031. Qin, Y.X., Chi, X.C., Su, Y.Q., et al., 2004. The pathogeny of ulcer disease in Epinephelus awoara. Journal of Fisheries of China 28 (3), 287–302. Rafail, S.Z., 1968. A statistical analysis of ration and growth relationship of plaice (Pleuronectes platessa). Journal of the Fisheries Research Board of Canada 25, 717–732. Russell, N.R., Fish, J.D., Wootton, R.J., 1996. Feeding and growth of juvenile sea bass: the effect of ration and temperature on growth rate and efficiency. Journal of Fish Biology 49, 206–220. Savitz, J., Albanese, E., Evinge, M.J., 1977. Effect of ration level on nitrogen excretion, nitrogen retention and efficiency of nitrogen utilization for growth in largemouth bass (Micropterus salmoides). Journal of Fish Biology 11 (2), 185–192. Staples, D.J., Nomura, M., 1976. Influence of body size and food ration on the energy budget of rainbow trout Salmo gairdneri Richardson. Journal of Fish Biology 9, 29–43. Sun, L.H., Chen, H.R., Huang, L.M., et al., 2006. Growth and energy budget of juvenile cobia (Rachycentron canadum) relative to ration. Aquaculture 257, 214–220. Tang, Q.S., Sun, Y., Guo, X.W., et al., 2002. Ecological conversion efficiencies of 8 fish species in Yellow Sea and Bohai Sea and main influence factor. Journal of Fisheries of China 26 (3), 219–225.
L. Sun et al. / Aquaculture 264 (2007) 228–235 Tang, Q.S., Sun, Y., Zhang, B., 2003. Bioenergetics models for seven species of marine fish. Journal of Fisheries of China 27 (5), 443–449. Wayne, A., Wurtsbaugh and Joseph, Cech Jr., J., 1983. Growth and activity of juvenile mosquito fish: temperature and ration effects. Transactions of the American Fisheries Society 112, 653–660. Xian, W.W., Zhu, X.H., 2000. Preliminary study on the effect of ration on growth of bastard halibut Paralichthys olivaceus (T. et S.). Journal of Ocean University of Qingdao 30 (3), 453–458. Xian, W.W., Zhu, X.H., 2001a. Effect of ration on energy budget of bastard halibut Paralichthys olivaceus (T. et S.). Journal of Ocean University of Qingdao 31 (5), 695–700. Xian, W.W., Zhu, X.H., 2001b. Effect of ration size on the growth and energy budget of the mullet Liza haematocheila (T. et S.). Journal of Ocean University of Qingdao 32 (6), 612–620. Xie, X.J., Sun, R.Y., 1993. The faecal production and digestibility of the southern catfish (Silurus meridionalis Chen), in relation to ration level, body weight and temperature. Oceanologia and Limnologia Sinica 24 (6), 627–633.
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Xie, S.Q., Cui, Y.B., Yang, Y.X., et al., 1997. Energy budget of Nile tilapia (Oreochromis niloticus) in relation to ration size. Aquaculture 154, 57–68. Yang, Y.O., Cui, Y.B., Xiong, B.X., et al., 2003. Comparative studies on nitrogen budget and energy budget of Jian Carp (Cyprinus carpiovar. Jian) and Gibel carp (Carassius auratus gibelio) fed diets with different qualities. Acta Hydrobiologica Sinica 27 (6), 572–579. Zhou, W.X., Bo, Z.L., Xin, J., et al., 1994. Food conditions of larvae, fry and juvenile of Epinephelus awoara in artificial culture. Journal of Zhejiang College of Fisheries 13 (2), 86–92. Zhu, X.M., Xie, S.Q., Cui, Y.B., et al., 2001. Effect of ration level on growth and energy budget of male and female rare minnow Gobiocypris rarus. Oceanologia et Limnologia Sinica 32 (3), 240–247.
Growth, faecal production, nitrogenous excretion and energy budget of juvenile yellow grouper (Epinephelus awoara) relative to ration level Lihua Sun ⁎, Haoru Chen, Liangmin Huang South China Sea Institute of Oceanology, Chinese Academy of Sciences, 164 Xingang west Road, Guangzhou 510301, PR China Marine Biology Research Station at Daya Bay, Chinese Academy of Sciences, Dongshan village Nan'ao town, Shenzhen 518120, PR China Received 24 August 2006; received in revised form 6 November 2006; accepted 20 December 2006
Abstract Growth, faecal production, nitrogenous excretion and energy budget of juvenile yellow grouper (initial body weight 5.5 g or so) at various ration levels (starvation, 0.5%, 1% and 2% of initial body weight per day, and satiation) were investigated in this study. Faecal production (f, mg g− 1 d− 1) and nitrogenous excretion (u, mg g− 1 d− 1) increased markedly with increased ration level (RL, % per day), described as f = 0.483RL + 0.112 for faecal production and u = 0.218RL + 0.219 for nitrogenous excretion, respectively. Feed absorption efficiency (FAE, %) increased as ration increased with ranges of 91.4–94.0%, 95.6–97.3% and 96.5–97.6% for FAEd, FAEp and FAEe, respectively, but all of the variations were small. Relationships between specific growth rate in wet weight (SGRw, % per day), dry weight (SGRd, % per day), protein (SGRp, % per day), energy (SGRe, % per day) and ration level (RL, % per day) were linear and described as simple equations SGRw = 0.738RL–0.764, SGRd = 0.871RL–0.928, SGRp = 0.904RL–0.966 and SGRe = 1.038RL–1.060. Feed conversion efficiency in wet weight (FCEw, %), dry weight (FCEd, %), protein (FCEp, %) and energy (FCEe, %) all increased as ration increased and maximized at ad libitum ration level. Energy budgets of juvenile Epinephelus awoara at satiation ration level was: 100C = 2F + 4U + 75R + 19G or 100A = 80R + 20G, where C is food energy, A is assimilated energy, F is faeces energy, U is excretion energy, R is metabolism energy and G is growth energy. © 2007 Elsevier B.V. All rights reserved. Keywords: Juvenile yellow grouper (Epinephelus awoara); Ration level; Growth; Faecal production; Nitrogenous excretion; Energy budget
1. Introduction Yellow grouper, Epinephelus awoara, is a rare, but economically important marine species distributed in south eastern China Sea, where there are island reefs. The products from yellow grouper are salable in home and overseas markets because of the palatability and ⁎ Corresponding author. Tel./fax: +86 755 8442 2460. E-mail address: [email protected] (L. Sun). 0044-8486/$ - see front matter © 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.aquaculture.2006.12.036
nutritional quality of its flesh and its high economic value. Yellow grouper does not migrate long distances. So it is regarded as having a great potential for offshore cage culture. In recent years, yellow grouper has become an important cultured species in the coastal waters of southern China. Most seed for large-scale aquaculture is obtained by artificial breeding. In the artificial breeding of yellow grouper, especially during the period of using artificial formulated feed, one of the key issues is how to optimize ration to support fast
L. Sun et al. / Aquaculture 264 (2007) 228–235 Table 1 Chemical composition and energy content of the commercial eel formulated feed used during yellow grouper growth experiments (percentage by weight) Composition
Percentage of wet matter (%)
Percentage of dry matter (%)
Moisture Crude protein Crude lipid Ash Gross energy (kJ g− 1)
8.48 44.63 10.42 12.24 16.71
– 48.77 11.39 13.37 18.26
growth and feed conversion, and to reduce feed waste and water pollution. Thus, it is necessary to investigate the effects of ration level on yellow grouper growth, faecal production, nitrogenous excretion and energy budget. There are only a few publications on the biology of yellow grouper. Bo et al. (1993) studied the ageing, morphology and growth of larvae, fry and juvenile of yellow grouper. Zhou et al. (1994) investigated feeding conditions of larvae, fry and juvenile of yellow grouper in artificial culture. Dai and Zhao (1994) determined O2 consumption of yellow grouper. Qin et al. (2004) reported the pathogeny of ulcer disease in yellow grouper. Little, however, is known about the bioenergetics of this species, so growth, faecal production, nitrogenous excretion and energy budget of juvenile yellow grouper relative to ration were investigated in this paper. The study aimed to characterize the bioenergetics of juvenile yellow grouper, but also to provide a scientific basis for feeding management in the large-scale artificial breeding of yellow grouper. 2. Materials and methods 2.1. Experimental fish and diet Juvenile yellow grouper for the experiment were from the artificial breeding by the research group at the Marine Biology Research Station at Daya Bay, Chinese Academy of Sciences (MBRS). The experimental diet for juvenile yellow grouper was a commercial eel formulated feed (Grobest brand, Quanxing aquatic feed L.T.D.). The main components of this feed include fish meal from Peru, α-starch, yeast powder, FeSO4, ZnSO4·7H2O, CuSO4·5H2O, MnSO4, Na2SeO3, Vitamin A, Vitamin D3, Vitamin E, Vitamin K3, Vitamin C, Vitamin B1, Vitamin B2, Vitamin B6, Vitamin B12, niacin, folic acid, inositol, etc. The chemical composition of this diet is listed in Table 1. Before the start of feeding the diet was added with a fixed proportion of water (water: eel feed = 1:2) and made into pellets (diameter 2–3mm) suitable for fish feeding.
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2.2. Fish acclimation Juvenile yellow grouper belonging to the same batch and in good health were collected from outside breeding ponds at MBRS. About one hundred and eighty fish were transferred into four indoor concrete ponds with about forty-five fish per pond (2 m × 1 m × 1 m, water volume 1.6 M3) and acclimated for 2 weeks. Then fish of similar body size and showing normal feeding behavior were captured randomly from the indoor ponds, marked as described by Russell et al. (1996), and then placed randomly into rectangular transparent plastic tanks (60 cm × 45 cm × 40 cm, water volume 90 L) for further acclimation 1 week. A pilot trial was conducted to estimate the maximal ration during this period, which would provide experimental evidence for designing the ration levels used in the growth experiment. During the whole acclimation period, no fish died. Enough feed was provided to satiation as judged by visual inspection once a day (about 09:00). All seawater in each tank was replaced by fresh, filtered and wellaerated seawater every 3–4 days. Aeration was provided continuously except for the feeding time and dissolved oxygen was maintained above 6 mg l− 1. Temperature and salinity were monitored daily. During this period water temperature was 25.7–29.1 °C, salinity was 29.4– 33.2, and fish were subjected to a natural photoperiod regime with similar light conditions for all tanks. 2.3. Growth experiment Five ration levels were tested in the growth experiment: starvation, 0.5, 1, 2% of initial body weight per day, and ad libitum, with five replicates for each level and five fish for each replicate. In addition, another twenty fish were sampled for measurement of initial body composition and energy content. One hundred and fifty fish, which had been starved for 2 days, were captured, blotted of excess water weighed and then placed into individual experimental tanks at the start of the growth experiment. During the experiment fish (mean weight about 5.5 g) in each tank were subjected to the five prescribed ration levels ranging from starvation to an ad libitum ration equal to feeding the fish to satiation once a day (about 09:00). An excess of feed was fed to the satiation (ad libitum) ration group, the daily feed supplied was recorded, and the uneaten feed was collected 30 min after feeding by pipetting and then ovendried at 70 °C. Potential loss of uneaten feed was determined by placing feed in water for 30 min and then collecting, drying and weighing. The proportion of the
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L. Sun et al. / Aquaculture 264 (2007) 228–235
Table 2 Body chemical composition (g g− 1 W.W.) and energy content (kJ g− 1 W.W.) of juvenile yellow grouper at different ration levels (RL, % per day) Ration level
Starvation
0.5
1
2
Ad libitum
Moisture content Protein content Lipid content Ash content Energy content
76.29 ± 0.85 c 14.69 ± 0.59 a 2.66 ± 0.10 a 6.33 ± 0.44 c 4.14 ± 0.13 a
76.13 ± 0.54 c 15.18 ± 0.27 bc 2.57 ± 0.17 a 5.92 ± 0.35 c 4.16 ± 0.06 a
75.94 ± 0.62 c 15.39 ± 0.38 bc 2.82 ± 0.12 ab 5.50 ± 0.34 b 4.37 ± 0.09 b
75.62 ± 0.63 ab 15.43 ± 0.32 ab 3.20 ± 0.14 ab 4.90 ± 0.20 a 4.51 ± 0.13 b
74.85 ± 0.69 a 16.02 ± 0.22 c 3.34 ± 0.17 b 4.84 ± 0.18 a 4.76 ± 0.08 c
Values (mean ± SD) in the same row with different letters are significantly different (P b 0.05).
food remaining was calculated and this value was used to adjust the amount of the feed intake. Faeces were collected twice a day by pipetting, ovendried at 70 °C, weighed, homogenized and stored at − 20 °C for later chemical and calorific analyses. All seawater in each plastic tank was replaced by fresh, filtered and well-aerated seawater every 4 days except that one water-replacement lasted 7 days, at the beginning and end of which period, water was sampled, and ammonia and urea contents in each tank were determined by the method of Chaney and Marbach (1962) and converted into energy by multiplying by 24.83 kJ g− 1 for ammonia and 23.03 kJ g− 1 for urea (Elliot, 1976a). Potential loss of nitrogenous compounds through bacterial action or diffusion was quantified by setting controls without fish and the value was used to adjust determined nitrogenous excretion. Aeration was provided continuously except during feeding and following faeces collecting, and dissolved oxygen was maintained above 6 mg l− 1. Temperature and salinity were monitored daily. During this period, water temperature was 25.2–28.4 °C, salinity was 30.2–33.6 and the experiment was conducted at the natural photoperiod conditions with similar light intensity for all tanks. The growth experiment lasted 21 days. After starvation for 2 days fish from the same tank were weighed, pooled, chopped, dried, reweighed, homogenized and then stored at − 20°C for later chemical and caloric analyses.
2.4. Chemical analysis Moisture contents of fish and feed were determined after oven-drying to constant weight at 105 °C for diet and 70 °C for fish. Protein contents of fish, faeces and feed were measured by the Kjeldahl method using an auto Kjeldahl system (BÜCHI K-370/K-437, Switzerland). Lipid contents of fish and feed were measured by ether extraction. Ash contents of fish and feed were determined by a muffle furnace at 550 °C for 8–10 h. Gross energy contents of fish, faeces and feed were measured by oxygen calorimetric bomb (model 1341EE, USA, calibrated by benzoic acid). For each variable, at least duplicate samples were determined and the mean of duplicate determination was taken as the result when the relative deviation was less than 2%. 2.5. Statistical analysis A one-way Analysis of Variance (ANOVA) followed by a multiple range test (Newman–Keuls) was used after previous determination of the normality and homescedasticity of the data. There are significant differences among various treatments when P b 0.05. Least squares regression was performed to evaluate the relationships between nitrogenous excretion, faecal production, specific growth rate and ration, and judged by coefficient of determination (R2) and residual analysis. Analysis of Covariance (ANCOVA) was made to investigate
Table 3 Nitrogenous excretion (u, mg g− 1 d− 1), faecal production (f, mg g− 1 d− 1) and feed absorption efficiency in dry weight (FAEd, %), protein (FAEp, %), energy (FAEe, %) of juvenile yellow grouper at different ration levels (RL, % per day) RL
Starvation
0.5
1
2
Ad libitum
u f FAEd a FAEp b FAEe c
0.18 ± 0.02 a 0.00 ± 0.00 a – – –
0.26 ± 0.03 b 0.42 ± 0.09 b 91.4 ± 1.8 a 95.6 ± 0.8 a 96.5 ± 0.7 a
0.43 ± 0.02 c 0.70 ± 0.10 c 92.2 ± 1.1 a 96.2 ± 0.4 a 96.9 ± 0.3 a
0.69 ± 0.08 d 1.01 ± 0.10 d 94.0 ± 0.5 b 97.2 ± 0.3 b 97.6 ± 0.3 b
0.77 ± 0.10 e 1.28 ± 0.23 e 93.6 ± 0.6 b 97.3 ± 0.3 b 97.6 ± 0.2 b
Values (mean ± SD) in the same row with different letters are significantly different (P b 0.05). a FAEd = 100 × (feed intake × dry matter content − faecal production) / feed intake × dry matter content. b FAEp = 100 × (feed intake × protein content − faecal production × protein content) / feed intake × protein content. c FAEe = 100 × (feed intake × energy content − faecal production × energy content) / feed intake × energy content.
L. Sun et al. / Aquaculture 264 (2007) 228–235 Table 4 Coefficients of the regression equation (Y = a + bRL) relating to specific growth rate in wet weight (SGRw, % per day), dry weight (SGRd, % per day), protein (SGRp, % per day) and energy (SGRe, % per day) as well as nitrogenous excretion (u, mg g− 1 d− 1) and faecal production (f, mg g− 1 d− 1) to ration level (RL, % per day) for juvenile yellow grouper Y
a
b
n
R2
P
u f SGRw SGRd SGRp SGRe
0.173 0.112 − 0.764 − 0.928 − 0.966 − 1.060
0.250 0.483 0.738 0.871 0.904 1.038
25 25 25 25 25 25
0.942 0.938 0.919 0.901 0.897 0.936
b0.01 b0.01 b0.01 b0.01 b0.01 b0.01
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lipid and energy contents, and a negative correlation for moisture and ash contents. 3.2. Nitrogenous excretion, faecal production and feed absorption efficiency Nitrogenous excretion, faecal production and feed absorption efficiency in dry weight, protein and energy of juvenile yellow grouper all increased as ration increased (Table 3). The relationship between nitrogenous excretion as well as faecal production and ration level could be described with a simple linear relationship as well as a power function (Table 4). 3.3. Specific growth rate and feed conversion efficiency
the effect of fish weight on growth across ration treatments. Data were expressed as mean ± SD of five replicate ration levels. The statistical analyses, using SPSS 11.0 for windows, were performed on tank means, with five replicate means per treatment. 3. Results 3.1. Body chemical composition and energy content The contents of moisture, protein, lipid, ash and energy in the body of juvenile yellow grouper at different ration levels are listed in Table 2. A positive correlation to ration level was observed for the protein,
Specific growth rate in wet weight (SGRw), dry weight (SGRd), protein (SGRp) and energy (SGRe) of juvenile yellow grouper increased with increased ration (Table 5). There was a positive, linear relationship between specific growth rate and ration (Table 4). ANCOVA showed that across ration treatments fish weight had no significant effect on SGRw (F = 0.237, P N 0.05), SGRd (F = 0.571, P N 0.05), SGRp (F = 0.515, P N 0.05) and SGRe (F = 0.484, P N 0.05). Feed conversion efficiency in wet weight, dry weight, protein and energy of juvenile yellow grouper also increased with increased ration and were highest at satiation ration (Table 5).
Table 5 Specific growth rate in wet weight (SGRw, % day− 1), dry weight (SGRd, % day− 1), protein (SGRp, % day− 1) and energy (SGRe, % day− 1) and feed conversation efficiency in wet weight (FCEw, %), dry weight (FCEd, %), protein (FCEp, %) and energy (FCEe, %) of juvenile yellow grouper at different ration levels (% per day) Ration level IBW (g per fish) SGRw b SGRd c SGRp d SGRe e FCEw f FCEd g FCEp h FCEe i
a
Starvation
0.5
1
2
Ad libitum
5.69 ± 0.75 a − 0.82 ± 0.14 a − 1.03 ± 0.26 a − 1.13 ± 0.22 a − 1.13 ± 0.19 a − − − −
6.36 ± 0.99 a − 0.35 ± 0.16 b − 0.40 ± 0.18 b − 0.38 ± 0.21 b − 0.51 ± 0.15 b − 66.58 ± 29.79 a − 20.20 ± 8.64 a − 24.71 ± 13.24 a − 24.99 ± 7.06 a
5.01 ± 0.78 a 0.07 ± 0.03 c 0.05 ± 0.14 c 0.10 ± 0.13 c 0.13 ± 0.11 c 6.93 ± 2.87 b 1.43 ± 3.84 b 3.60 ± 4.64 b 3.51 ± 2.80 b
5.04 ± 0.63 a 0.41 ± 0.12 d 0.46 ± 0.17 d 0.46 ± 0.12 d 0.63 ± 0.14 d 21.51 ± 6.56 b 6.34 ± 2.48 b 8.24 ± 2.29 b 8.75 ± 2.10 b
5.26 ± 0.86 a 1.24 ± 0.24 e 1.43 ± 0.26 e 1.46 ± 0.27 e 1.71 ± 0.30 e 49.89 ± 8.50 c 15.59 ± 2.64 c 20.78 ± 3.88 c 18.80 ± 2.49 c
Values (mean ± SD) in the same row with different letters are significantly different (P b 0.05). a IBW = initial body weight. b SGRw = 100 × [ln(final body weight) − ln(initial body weight)] / days of the experiment. c SGRd = 100 × [ln(final body weight × final dry matter content) − ln(initial body weight × initial dry matter content)] / days of the experiment. d SGRp = 100 × [ln(final body weight × final protein content) − ln(initial body weight × initial protein content)] / days of the experiment. e SGRe = 100 × [ln(final body weight × final energy content) − ln(initial body weight × initial energy content)] / days of the experiment. f FCEw = 100 × (final body weight − initial body weight) / feed intake. g FCEd = 100 × [(final body weight × final dry matter content) − (initial body weight × initial dry matter content)] / (feed intake × dry matter content). h FCEp = 100 × [(final body weight × final protein content) − (initial body weight × initial protein content)] / (feed intake × protein content). i FCEe = 100 × [(final body weight × final energy content) − (initial body weight × initial energy content)] / (feed intake × energy content).
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Table 6 Energy budgets a at different ration levels (RL, % per day) for juvenile yellow grouper Starvation b
RL −1
C (kJ g
−1
day )
0.000 ± 0.000
0.5
1
2
Ad libitum
0.087 ± 0.002
0.166 ± 0.002
0.320 ± 0.004
0.416 ± 0.072
As a percentage of C (%) F U R G
– 0.004 ± 0.001 0.044 ± 0.008 −0.048 ± 0.008
3.51 ± 0.68 b 6.80 ± 0.83 c 114.68 ± 7.75 c −24.99 ± 7.06 a
3.12 ± 0.33 b 5.79 ± 0.30 b 87.58 ± 2.85 b 3.51 ± 2.80 b
2.35 ± 0.25 a 4.81 ± 0.61 b 84.09 ± 2.20 b 8.75 ± 2.10 c
2.38 ± 0.21 a 4.19 ± 0.49 a 74.63 ± 2.43 a 18.80 ± 2.49 d
As a percentage of A (%) R G
– –
127.82 ± 7.69 c −27.82 ± 7.69 a
96.14 ± 3.08 b 3.86 ± 3.08 b
90.58 ± 2.27 b 9.42 ± 2.27 b
79.88 ± 2.65 a 20.12 ± 2.65 c
Values (mean ± SD) in the same row with different letters are significantly different (P b 0.05). a C = F + U + R + G or A = R + G (Brett and Groves, 1979), where C is food energy, A is assimilated energy, F is faeces energy, U is excretion energy, R is metabolism energy, calculated by difference R = C − F − U − G (Elliot, 1976b), and G is growth energy. b Values for the starving fish were expressed as kJ g− 1 day− 1.
3.4. Energy budget Energy budgets at each ration level for juvenile yellow grouper are shown in Table 6. The proportions of energy intake lost in faecal production and excretion were 2.38– 3.51% and 4.19–6.80%, respectively, and both proportions tended to decrease with an increase in ration size. As ration increased, the proportion of energy intake (or absorption) stored in body (growth) increased and was highest at satiation ration, whereas the proportions of energy intake (or absorption) spent in metabolism decreased and were lowest at satiation ration. 4. Discussion Faecal production of juvenile yellow grouper increased linearly with increased ration, which was consistent with the studies on bluegill sunfish Lepomis macrochirus (Gerking, 1955), bastard halibut Paralichthys olivaceus (Xian and Zhu, 2001a) and mullet Liza haematocheila (Xian and Zhu, 2001b) but different from the studies on south catfish Silurus meridionalis Chen (Xie and Sun, 1993) and cobia Rachycentron canadum (Sun et al., 2006), whose faecal production showed a curvilinear increase. Feed absorption efficiency in dry weight, protein and energy also tended to increase with ration level, though the variation was small, which agreed with a study of the cyprinid Phoxinus phoxinus (Cui and Wootton, 1988). However, the effect of ration on feed absorption efficiency will rarely be large as ration increases from low levels to ad libitum (Jobling, 1994). In some papers faecal production was also reported as a simple or exponential function of ration (Gerking, 1955; Allen and Wootton, 1982; Cui and Wootton, 1988).
Usually nitrogenous excretion increases with increased ration and a simple linear, power or exponential function has been used to describe the relationship (Savitz et al., 1977; Mortensen, 1985; Cui and Liu, 1990). Nitrogenous excretion for juvenile yellow grouper increased linearly as ration increased, which was similar to the results for largemouth bass Micropterus salmoides (Savitz et al., 1977), rainbow trout Oncorhynchus mykiss (Beamish and Thomas, 1984) and cyprinid P. phoxinus (Cui and Wootton, 1988). The relationship between growth and ration has usually been described by one of two patterns: one is a decelerating curve, which has been described by a variety of functions (Wayne et al., 1983; Zhu et al., 2001; Allen and Wootton, 1982; Tang et al., 2002; Cortes and Gruber, 1994; Xie et al., 1997; Rafail, 1968), and the other is a simple linear relationship (Niimi and Beamish, 1974; Paul et al., 1992, 1994; Cui et al., 1996). Cui et al. (1996) speculated that the curvilinear growth– ration relationship was caused by the inability of fish to convert food materials into body tissues at high rations efficiently and the relationship would be linear if: (1) the food intake or absorption (C–F) at the maximum ration was low, so that the decline in conversion efficiency did not occur; or (2) the fish could maintain a high foodconversion efficiency even at maximum ration. In this study the growth–ration relationship for juvenile yellow grouper produced a significant linear relationship and feed conversion efficiency also increased with increased ration. Low consumption but a high feed conversion efficiency at ad libitum ration might be the reasons for the linear growth-relationship of juvenile yellow grouper, which was in agreement with the studies on flathead sole Hippoglossoides elassodon (Paul et al., 1992), juvenile Pacific halibut Hippoglossus stenolepis
L. Sun et al. / Aquaculture 264 (2007) 228–235
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Table 7 Comparison of maximal ration level (RLmax) or maximal energy intake (Cmax), specific growth rate (SGRw) and energy budget among several fish species at satiation ration Fish species a
Yellow grouper (Epinephelus awoara)
Cobia (Rachycentron canadum)
Bastard habibut (Paralichthys olivaceus)
Rainbow trout (Oncorhynchus mykiss)
Initial average body weight (g) Temperature (°C) RLmax (% d− 1) / Cmax (kJ g− 1 d− 1) SGRw (% per day) As a percentage of C (%) F U R G As a percentage of A (%) R G Reference
5.47 25.2–28.4 2.49/0.42
9.91 27.2–30.4 12.84/1.50
2.27 24.0 6.39/1.55
3.62 11.4 3.04/0.37
1.24 2.38 4.19 74.63 18.80 79.88 20.12 Present study
5.08 7.07 75.91
6.62 0.95 5.52 44.31 49.21 47.38 52.62 Xian and Zhu (2000)
2.23 23.45
a
17.12
Sun et al. (2006)
35.68 40.87 46.61 53.39 Staples and Nomura (1976)
Fed on artificial formulated feed.
(Paul et al., 1994) and rainbow trout O. mykiss (Staples and Nomura, 1976). It is important for aquaculture to determine that whether the growth–ration relationship is linear or curvilinear. If it is curvilinear, feed conversion efficiency with increased ration usually shows a domed curve, in which case the ration that maximizes growth efficiency is an intermediate not a satiation ration, but if it is linear, feed conversion efficiency increases as ration increases, in which case the optimum feeding strategy would be that fish are fed to satiation to obtain both rapid growth and high feed conversion efficiency (Xie et al., 1997). The data on growth and feed conversion efficiency in the present study indicated that a satiation ration would maximize both growth rate and growth efficiency in juvenile yellow grouper at this ontogentic stage and given the artificial feed. Tang et al. (2003) calculated an average energy budget based on the published budgets of seven marine fish species fed satiation ration: 100A ¼ 71:5R þ 28:5G On the basis of this average energy budget, Tang et al. (2003) divided the mode of energy allocation into three styles: (1) Lower metabolism and higher growth, such as Schlegel's black rockfish Sebastes schlegeli and finespot goby Chaeturichthys stigmatias; (2) Higher metabolism and lower growth, such as black porgy Acanthopagrus schegeli and fat greenling Hexagrammos otakii; (3) Moderate metabolism and moderate growth, such as red seabream Pagrus major, tiger puffer Takifugu rubripes and chub mackerel Scomber japonicus.
Energy budget of juvenile yellow grouper at satiation ration in this paper was: 100A ¼ 80R þ 20G The proportion of assimilated energy spent in metabolism for juvenile yellow grouper was obviously higher than the average value. Referring to the energy budget modes of other marine fish the energy allocation mode of juvenile yellow grouper is a pattern of moderate metabolism and moderate growth with a tendency to higher metabolism and lower growth. Yellow grouper, whose natural habitat is areas with island reefs, were observed to consume little and hold still at the bottom of the tanks for a large part of time during the experiment. The large differences between the experimental conditions and the natural habitat may lead to stress in the experimental fish, with a consequent increase in metabolic rate and a decrease in food consumption. A study on the fat greenling H. otakii, whose natural habitat is also island reefs (Tang et al., 2003), showed a comparable phenomenon. However, for a given fish species, the growth–ration relationship and energy budget may be dependent on many factors such as experimental method (Tang et al., 2003), feed type or composition (Huisman and Valentijn, 1981; Cui et al., 1992, 1994; Jobling, 1994; Yang et al., 2003), body size (Niimi and Beamish, 1974; Staples and Nomura, 1976), water temperature (Elliot, 1976b; Malloy and Targett, 1994), etc. Further research is required to quantify these effects in juvenile yellow grouper. Table 7 lists the growth and energy budget of several fish species fed at maximum rations. A provisional explanation of bio-energetic mechanisms of the growth
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of different species can be based on their energy allocation patterns. Juvenile yellow grouper showed a low rate of food consumption combined with a small allocation of energy to growth. Consequently, their growth at maximum rations was low. Juvenile rainbow trout, O. mykiss, had a low rate of food consumption but allocated a higher proportion of energy to growth and consequently had a higher growth rate than juvenile yellow grouper (Staples and Nomura, 1976). Juvenile cobia, R. canadum, allocated a low proportion to growth but had high rates of food consumption and consequently showed a higher growth rate than rainbow trout (Sun et al., 2006). Juvenile bastard halibut, Paralichthys olivaceus, combined high rates of food consumption with a high proportion allocated to growth and so had high growth rates (Xian and Zhu, 2000). The ecological factors that select for particular patterns of food consumption and energy partitioning are still poorly understood. A better understanding of these factors may follow for the design of more effective holding and feeding regimes for species used in aquaculture. Acknowledgements The authors are grateful for the financial support by grant No. 2001A305020201 from the key project of Science and Technology of Guangdong Province, China. Thanks are given to three referees for their critical comments on the manuscript. References Allen, J.R.M., Wootton, R.J., 1982. The effect of ration and temperature on the growth of the three-spined stickleback, Gasterosteus aculeatus L. Journal of Fish Biology 20, 409–422. Beamish, F.W.H., Thomas, E., 1984. Effects of dietary protein and lipid on nitrogen losses in rainbow trout, Salmo gairdneri. Aquaculture 41, 359–371. Brett, J.R., Groves, T.D.D., 1979. Physiological energetics. In: Hoar, W.S., et al. (Ed.), Fish Physiology, vol. 8. Academic Press, New York, pp. 279–352. Bo, Z.L., Zhou, W.X., Xin, J., et al., 1993. Study on daily age, morphology and growth of larva, fry juvenile of Epinephelus awoara. Journal of Zhejiang College of Fisheries 12 (3), 165–173. Chaney, A.L., Marbach, E.P., 1962. Modified reagents for determination of urea and ammonia. Clinical Chemistry 8, 130–132. Cortes, E., Gruber, S.H., 1994. Effect of ration size on growth and gross conversion efficiency of young lemon sharks, Negaprion brevirostris. Journal of Fish Biology 44, 331–341. Cui, Y.B., Liu, J.K., 1990. Comparison of energy budget among six teleosts-I. food consumption, faecal production and nitrogenous excretion. Comparative Biochemistry and Physiology 96A (1), 163–171. Cui, Y., Wootton, R.J., 1988. Bioenergetics of growth of a cyprinid, Phoximus phoxinus (L.): the effect of ration, temperature and body size on food consumption, fecal production and nitrogenous excretion. Journal of Fish Biology 33, 431–443.
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