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Effect of ration size on the growth and energy budget of the grass carp, Ctenopharyngodon idella Val.
AquaCUlture ELSEVIER
Aquaculture 123 (1994) 95-107
Effect of ration size on the growth and energy budget of the grass carp, Ctenopharyngodon idella Val. Yibo Cui*, Shaolian
Chen, Shaomei
Wang
Institute of Hydrobiology, Academia Sinica, Wuhan, People’s Republic of China 430072
(Accepted 20 December 1993 )
Abstract Young grass carp ( 12- 13 g ) were kept at five ration levels ranging from starvation to ad libitum feeding at 30°C. They were fed duckweed. Food consumption, absorption efftciency and growth were determined directly, and metabolism and nitrogenous excretion calculated indirectly from energy and nitrogen budgets, respectively. The relationship between specific growth rate and ration size was linear. Absorption efficiency for energy was not affected by ration size and averaged 50.6 k 0.57% (mean I!Ise. ). Depending on ration size, energy lost in excretion accounted for 4.55.9% of the food energy, energy channelled to metabolism accounted for 34.4-48.3% of the food energy, and energy retained as growth accounted for 6.7-l 1.9% of the food energy. Regardless of ration, a constant proportion of food energy (30.7%) was accounted for by feeding metabolism (total metabolism minus fasting metabolism). The energy budget at the maximum ration was: 100C=49.1F+4.5U+3.6Rfa+30.9Rfe+ ll.9G, where C, F, U, Rf, Rfe and G represent food consumption, faecal production, excretion, fasting metabolism, feeding metabolism and growth, respectively.
1. Introduction Ration size is an important factor affecting the growth and energy budget of fish (Brett and Groves, 1979). The effects of ration size on the energy budget have been studied in carnivorous and omnivorous fishes (Elliott, 1976b; Brett and Groves, 1979; From and Rasmussen, 1984; Cui and Wootton, 1988a), but less is known about herbivorous fishes. Under natural conditions, the diet of the grass carp consists almost entirely of *Corresponding author. Current address: Department Davis, CA 956 16, USA.
of Animal Science, University
0044-8486/94/$07.00 0 1994 Elsevier Science B.V. All rights reserved SSDI 0044-84860044-8486 (94)00002-6
of California,
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Y. Cui et al. /Aquaculture 123 (1994) 95-107
macrophytes (He and Xie, 1966; Wen, 1990). In China, macrophytes are the major food used in the culture of this species. This study investigated the effects of ration size on the growth and energy budget in the grass carp fed a macrophyte diet. The energy budget of fish can be written as:
C=F+U+R+G where C is energy intake from food, F is energy lost in faeces, U is energy lost in nitrogenous excreta, R is energy expended in metabolism and G is energy deposited as growth. Metabolism is conventionally divided into three components: standard metabolism, specific dynamic action (SDA) and activity metabolism (Brett and Groves, 1979). Standard metabolism is defined as the metabolic rate of resting, unfed fish, but since fish are rarely at complete rest, it is difficult to obtain accurate estimates of standard metabolism unless the activity level of the fish can be quantified. SDA is often difficult to separate from activity metabolism. Therefore, in this paper, we have adopted the concepts of Ursin ( 1967 ) and divided metabolism into fasting metabolism (R,) and feeding metabolism (R, ) . Fasting metabolism is defined as the metabolic rate of undisturbed fish during long-term starvation, which is an approximation of standard metabolism (Elliott, 1976b). Feeding metabolism is the metabolic rate of a feeding fish over the fasting level, which is approximately equivalent to the sum of SDA and activity metabolism (From and Rasmussen, 1984).
2. Materials and methods Growth experiment Most parameters of the energy budget were obtained from data of a growth experiment. The fish were held in 250-litre glass aquaria, each connected to a filter tank containing 40 litres of clinoptilolite (diameter 3-5 mm), a natural zeolite which has a strong adsorption capacity for ammonia (Spotte, 1979). Water re-circulation was maintained by an air-lift pump at about 1 l/min, with dechlorinated tap water introduced at about 0.1 l/min to each aquarium. Additional aeration was provided intermittently for about 30 min each hour. A submersed heater, controlled by a thermostat, was used to maintain water temperature at the desired level. One hundred and fifty young-of-the-year grass carp were obtained from a hatchery and reared in the laboratory for 5 weeks before the experiment. Water temperature was gradually adjusted (2-3 "C/day) to the experimental temperature (30°C). The fish were then held at this temperature for a week before the start of the experiment. The photoperiod was 12L/ 12D. The fish were fed duckweed during the acclimatization period. The experiment lasted 3 weeks. The initial sizes of the fish are presented in Table 2. At the start of the experiment, 45 fish, which had been starved for 2 days, were weighed and placed into 15 aquaria (3 fish per aquarium). Fish in each
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aquarium were individually identified by fin-clipping. The aquaria were divided into 5 groups, with 3 aquaria in each group. The initial rations imposed were 0, 25%, 50%, 75% of the initial fish weight per day, and ad libitum. As fish fed the higher rations were expected to exhibit significant weight gains during the experiment, rations for the 50% and 7 5% groups were increased to 55% and 8 5% of the initial weight during the second week, and to 65% and 100% during the third week, respectively. Each day, the prescribed quantity of duckweed (Spirodela poZyrhiza) was weighed and put in each aquarium. Excess food was provided to fish in the ad libitum ration group. Any uneaten food was collected the next day and weighed. To remove excess water, both supplied and recovered duckweed were centrifuged for 3 min before being weighed. Each day a subsample of food was dried to constant weight at 70’ C to determine the dry matter content. Dry matter content was also determined for samples of uneaten food. The weight of food consumed was estimated in terms of dry weight using the mean dry matter contents of supplied and recovered duckweed. Faeces from each aquarium were collected daily by siphoning and dried to constant weight at 70 ’ C. At the end of the experiment, the fish were starved for 2 days and weighed. They were dried to constant weight at 70’ C, reweighed and homogenized. Nitrogen and energy contents were determined for each experimental fish, and for 10 control fish killed at the start of the experiment. In addition to the nitrogen and energy measurements, content of crude fibre was determined for the faecal sample from each aquarium, and lipid, ash and crude fibre measured for the duckweed. Nitrogen was determined by the Kjeldahl method, lipid by chloroformmethanol extraction (Lambert and Dehnel, 1974)) ash by combustion at 550 oC, and energy by bomb calorimetry. Protein content was calculated from nitrogen content by multiplying by 6.25. Crude fibre was determined in a Fibertec System (Tecator) by digestion sequentially with 0.128 M HzS04 and 0.223 M KOH, followed by combustion at 500°C. Two to four measurements were performed for each sample. Calculation of results
Absorption efficiency ( l-F/C) was calculated using crude tibre as an inert indicator (Cai and Curtis, 1989) : Absorption efficiency = I _ % crude fibre in food/nutrient or energy content in faeces x 1o. % crude fibre in faeces/nutrient or energy content in food Nitrogen excretion (En) was indirectly estimated from the nitrogen budget equation, a method suggested by Cho ( 1992 ) : En=C,-F,-G, where C,, is nitrogen intake from food, F,, nitrogen lost in faeces, and G, nitrogen retained in the fish body. Energy lost in excretion ( U) was calculated from nitro-
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gen excretion, assuming that all the nitrogen excreted was in the form of ammonia and that a calorific value of 24.8 J/mg N was appropriate for ammonia (Elliott, 1976a). Energy growth (G) was calculated as the change in the total energy content of the fish; the initial energy content per unit weight of the experimental fish was estimated from the average value of the control fish. Total metabolism (R) was estimated as the difference between C and I;, U and G (Elliott, 1976b). Fasting metabolism (I&) was calculated from a regression equation relating Rf, @J/day) to body weight ( W, g) for grass carp at 30°C (Cui et al., 1993b): In Rf, = -2.372+0.753
In W
The equation was calculated from data of a 5-week starvation experiment. mean value of the initial and final weight of the fish was used for calculation. difference between R and Rfa was feeding metabolism (R,) . The specific growth rate in wet weight (SGRw ) was calculated as: SGRw= 100x (In w,-ln
The The
?K,)/t
where I+‘,is the final and W, the initial weight of the fish, and t the experimental period (2 1 days). Specific growth rates in dry matter ( SGRd), protein ( SGRp) and energy (SGRe) were calculated similarly. Validation of use of crudefibre as an inert indicator for digestibility measurement To justify the use of crude fibre as an inert indicator for digestibility measurement, an experiment was conducted to compare the absorption efficiencies determined by complete quantification of faeces and by using crude fibre as an indicator. Grass carp weighing 33.7-46.1 g (mean 40.3 g) were obtained from a hatchery and reared in the laboratory for 10 days before the experiment. The food used was leaves of the green Chinese cabbage (Brassica chinensis) . The fish were randomly divided into two groups. Group A was used for complete quantification of faeces, and Group B for the crude fibre method. Fish in Group A were reared in 8 rectagular plexiglass tanks containing 40 litres of water (2 fish per tank), and fish in Group B in 5 circular tanks with conical bottoms (water volume, 50 litres; 6 fish per tank). Water in each tank was replenished once a day. For complete quantification of faeces, fish in Group A were starved for 3 days and, on the day of experiment, each tank received a weighed quantity of food at 9:O0. Five subsamples of food were weighed and dried to constant weight at 70” C to determine dry matter content. At 15:00, uneaten food was recovered, dried at 70°C and weighed. Faeces produced during 15:00-23:00 were collected by pippeting as soon as they were egested, and dried at 70°C. An additional faecal collection was made the next morning. Since the amount of faeces produced overnight was very small, errors associated with leaching during this period were regarded as negligible. For the crude fibre method, fish in Group B were fed excess quantities of food daily. Faecal samples accumulated in the faecal trap at the bottom of each tank were collected 4 times a day for 3 days and dried at 70°C. The content of crude fibre was measured for the food and faeces. Water temperature during the experiment was 17- 18 ‘C.
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Statistical analysis
Statistical analyses were made based on the mean values for each aquarium. One-way analysis of variance was used to test the significance of differences among ration groups. Bartlett’s test was used to check the homogeneity of variance among treatments. Since this assumption was met in all the analyses, no transformations were made on the data. Least-squares regression was applied to develop predictive relationships (Steel and Torrie, 1980).
3. Results Validation of use of crudefibre as an inert indicator for digestibility measurement
Absorption efficiency for dry matter determined by complete quantification of faeces was 65.77 + 0.76% (mean + s.e. ), and that determined using crude Iibre as an indicator was 66.73 + 0.6 1%. A t-test showed no significant difference between the two measurements (t = 0.88, I’= 0.40). It was concluded that crude fibre was a reliable inert indicator for digestibility measurement for the grass carp. Chemical composition and energy content of duckweed andfish body
Chemical composition and energy content of duckweed and fish body are shown in Table 1. Analysis of variance showed significant differences in the final dry matter, protein and energy content of fish body among ration groups (PC 0.0 1 in all cases). Regression analysis showed the following relationships between dry matter (DRY: % wet weight), protein (PROTEIN: % wet weight) or energy (ENERGY: kJ/g wet weight) content and ration level (RLz % body weight/day) : DRY= 16.45+O.O396RL
(n= 15,
PROTEIN = 11.4 1 + 0.0289RL
Sample Duckweed Fish
(n= 15, (n= 15,
ENERGY=2.77+0.01llRL Table 1 Chemical composition
r*=0.900) r*=0.786)
r2=0.91 1)
and energy content of food and fish body (mean + s.e. ) ’
Ration group
Dry matte?
Energy3
Protein*
Lipid2
Ash*
Crnde fibre’
6.06 * 0.08 19.24kO.37 16.30+0.66a 17.69+0.35’= 18.38f0.10” 18.99+0.25” 21.07f0.12”
1.08 3.64jrO.10 2.74?~0.16~ 3.13f0.07b 3.31?0.02b 3.42 + 0.02b 4.10+0.07c
2.17 12.24kO.14 10.87 + 0.45” 12.40*0.26b 13.331f-0.26ti 13.44rtO.26”= 14.46kO.26’
0.19
0.89
0.68
Control 0% 25% 50% 75% Ad libitum
‘Letters after each value indicate results of multiple comparison tests (Tukey’s procedure); letter are not significantly different from each other at the 0.05 level. ‘As % wet weight. ‘As kJ/g wet weight.
means with the same
0 25.0*0.2 48.220.4 68.3+ 1.6 116.0f2.9
Starvation 25% 50% 75% Ad libitum
12.3? 1.8 12.1k1.9 12.3* 1.7 12.1+ 1.8 13.3+ 1.7
Initial weight (g)
-0.49+0.11” 0.34 f 0.06b 1.47+0.12” 2.04 + 0.22” 3.41 f0.99d
Wet weight
- 1.47 * 0.25” 0.00 * 0.06b 1.49 * 0.04” 2.10f0.19” 3.81 +0.04d
Protein
- 1.87?0.31a -0.39fO.lOb 1.031tO.11” 1.74k0.20c 3.97&0.04d
Energy
means with the same letter are not significantly different
- 1.30+0.22” - 0.07 * 0.07b 1.26kO.10’ 1.98+0.16d 3.84f 0.07’
Dry weight
Specific growth rate (%/day)
tests (Tukey’s procedure);
11.0+1.1 13.0+ 1.9 16.8f2.3 18.8k3.1 27.2 + 3.8
Final weight (9)
‘Letters after each value indicate results of multiple comparison from each other at the 0.05 level.
Ration (% day)
Ration group
Table 2 Effect of ration size on the specific growth rates in the grass carp fed duckweed at 30” C (mean f s.e.) l
E,
S
s 2 S J F
!? E $
2
R
0 Et. 2
!?
0
Y. Cui et al. /Aquaculture 123 (1994) 9.5-107
Ration Fig. 1. Relationship 30°C.
(96 body weight
101
day-l)
between specific growth rates and ration size for the grass carp fed duckweed at
Table 3 Effect of ration size on the conversion efficiencies in the grass carp fed duckweed at 30°C (mean & s.e. ) ’ Ration group
25% 50% 75% Ad libitum
Conversion efficiency (%) Wet weight
Dry weight’
Protein
Energy
1.4OI!ZO.30” 3.03+0.30b 2.95 ? 0.36b 2.82+0.11b
Negative growth 8.00 I!Y 0.70 9.99kO.85 10.62kO.28
0.59+ 1.53” 18.71 +0.53b 18.64 f 2.03b 20.28 I!I0.83b
Negative growth 6.75 kO.78” 8.17* l.Ola 1 1.86+0.48b
‘Letters after each value indicate results of multiple comparison test (Tukey’s procedure); with the same letter are not significantly different from each other at the 0.05 level. *No significant difference among ration groups.
means
Growth Mean values of specific growth rates at each ration are shown in Table 2. SGR linearly with increased ration (Fig. 1) . Regression analysis showed the following relationships between SGR (%/day) and ration level (RL: % body weight/day): increased
SGRw= -0.385+0.0338RL
(n= 15,
r2=0.960)
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123 (1994) 95-107
SGRd= - 1.123+0.0440RL
(n= 15, A0.973)
SGRp= - 1.122+0.0448RL
(n= 15, A0.954)
SGRe= - 1.657+0.0496RL
(n= 15, r2=0.969)
Conversion efficiencies ( 100 x G/C) were calculated for groups where growth rate was positive (Table 3 ). Analysis of variance showed significant differences in conversion efficiencies for wet weight, protein and energy among ration groups (P
Absorption
25% 50% 75% Ad libitum
efficiency (%)
Dry matter
Protein
Energy2
41.1 43.1 43.1 46.6
74.220.1” 76.6f0.7b 77.6f0.1b 76.4+0.3b
49.5 I!I1.3 51.2rtl.111 51.0* 1.3 50.8 & 0.9
f 1.5” f0.6” kO.9” 2 0.7b
‘Letters after each value indicate results of multiple comparison tests (Tukey’s procedure); with the same letter are not significantly different from each other at the 0.05 level. ‘No significant difference among ration groups.
means
Table 5 Effect of ration size on the energy budget of the grass carp fed duckweed at 30 ’ C (mean + s.e. ) ’ Ration group Starvation2 C W/g/day)
0
50%
75%
Ad libitum
0.271 kO.003
0.522+0.010
0.740+0.176
1.256kO.031
50.54? 1.26 5.86kO.13 18.60f0.87 29.66 + 0.24 48.26 kO.24 -4.66+ 1.77
48.78? 1.09 4.61 kO.08 9.28kO.31 30.58 + 0.39 39.87kO.68 6.75 +0.78
49.00* 1.27 4.69kO.17 6.47f0.15 31.70+ 1.99 38.17k2.07 8.17f 1.01
49.241!~0.86 4.47 + 0.04 3.56kO.10 30.87k1.11 34.43kl.11 11.861LO.48
42.69 I!Z1.66 68.21k3.15 110.90f3.12 -10.90?3.12
19.92kO.57 65.65 f0.98 85.57* 1.40 14.43* 1.40
13.97LO.42 68.29k2.61 82.26 + 2.50 17.74k2.50
7.7020.36 66.66 + 1.48 74.36 Y?1.26 25.64f 1.26
25%
As percentages of C
F u
Ra, Rr,
R
G
0
0.006 f 0.001 0.05 1 IL0.002 0.05 1 rt 0.008 -0.058 f 0.009
As percentages of A Rf, Rfe R G
‘Symbols: C=food consumption; A=assimilated energy (C-F-U); F=faecal U=excretion; Rf,=fasting metabolism; R,=feeding metabolism; R= total metabolism; ‘Values for the starving fish were expressed as H/g/day.
production; G=growth.
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efficiency for dry weight (P> 0.05 ). Conversion efficiencies tended to increase with increased ration. Absorption efficiency Absorption efficiencies of dry matter, protein and energy are shown in Table 4. Analysis of variance showed significant differences in absorption efficiency of dry matter (P< 0.05) and protein (P< 0.01) among ration groups. There was a tendency for absorption efficiency to increase at higher rations. However, absorption efficiency of energy was not significantly different among the ration groups (P> 0.05); the mean absorption efficiency of energy was 50.6 2 0.57% ( + s.e. ). Energy budget Table 5 shows the energy budget at each ration level. The pattern of energy allocation varied with ration size. The proportion of food energy lost in excreta ranged from 4.5 to 5.9% (Table 5), and the mean proportion was 4.9%. There was a tendency for this proportion to decrease with increased ration. The proportions of food and assimilated (C-F-U) energy channelled to fasting metabolism tended to decrease with increased ration, but the proportions channelled to feeding metabolism were relatively constant; on average, feeding metabolism accounted for 30.7% of the food energy, or 67.2% of the assimilated energy. 4. Discussion The absorption efficiency of the grass carp determined using crude fibre as an inert indicator agreed well with that determined by complete quantification of faeces, suggesting that grass carp could hardly digest crude fibre. This result is consistent with the findings of several other studies, which indicated that the cellulase activity in the intestine of the grass carp was very low (Lindsay and Harris, 1980; Lesel et al., 1986). Crude fibre can thus be regarded as a reliable inert indicator for the measurement of absorption efficiency in the grass carp. In the present study, two components of the energy budget were indirectly estimated by difference. Energy lost in excretion was calculated from the nitrogen budget, and metabolism from the energy budget. Theoretically, both the nitrogen and energy budgets should be balanced. However, the pooled errors associated with the directly determined components were added to the calculated component. Thus, the reliability of the indirectly determined components depends on the accuracy of the directly determined ones. The measurement of food consumption should be accurate. Estimation of nitrogen and energy growth should be accurate too, since the final nitrogen and energy content was determined for each individual. Errors may arise from the estimation of initial nitrogen and energy content from the mean values of the control tish, but the variations in the nitrogen and energy contents among the control fish were reasonably small (95% CL was 1.98-2.26% for nitrogen content and 3.35-3.94 kJ/g for energy content; see Table 1). The accuracy of absorption
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Y. Cui et al. /Aquaculture 123 (1994) 95-107
efficiency measurement depends largely on the validity of using crude libre as an inert indicator, which was justified in the present study, although some errors may arise from nutrient leaching in the faeces. The assumption that all the nitrogen excreted was in the form of ammonia should not introduce great errors, since ammonia is usually the predominant nitrogenous compound excreted in teleosts, and the calorific values of ammonia-nitrogen (21.83 J/mg) and urea-nitrogen (23.03 J/mg) were reasonably close (Elliott, 1979). Also, excretion is usually a small component of energy budget and errors associated with its estimation are unlikely to greatly influence the estimation of metabolism. In most carnivorous and omnivorous fishes, the relationship between growth rate and ration size is a decelerating curve (Brett and Groves, 1979); the conversion efficiency is highest at an intermediate ration, and decreases with further increases in ration. Grass carp fed a pelleted feed showed a similar pattern of growth-ration relationship (Huisman and Valentijn, 198 1). In the present study, the growth rate of the grass carp fed duckweed was linearly related to ration size, and there was no decrease in conversion efficiency at high rations. There are two possible reasons for this discrepancy. One reason may be that the grass carp in the ad libitum group were not feeding to their maximum rates, although the rate of food consumption in this group ( 116%) was probably among the highest reported for this species (Shireman and Smith, 1983; Cai and Curtis, 1989; Chen et al., 1993). The second possibility was that, because of the low energy content and absorption efficiency of the plant food, grass carp fed plants may not be able to achieve the level of absorbed energy when conversion efficiency starts to decline; thus a linear growth-ration relationship may be typical for grass carp fed plants. In the present study, energy lost through nitrogenous excretion accounted for 4.47-5.86% of the food energy in the grass carp. A similar value (5%) was obtained by Cui et al. ( 1992) for grass carp fed duckweed (a mixture of Lemna minor and Spirodela polyrhiza). These indirect estimates were close to the values of 3.1-4.7% directly determined by Carter and Bralield ( 1991) for grass carp. These values were within the range reported for carnivorous and omnivorous fishes (Cui and Wootton, 1988b; Du Preez and Co&oft, 1988a,b; Cui and Liu, 1990a). Brett and Groves ( 1979) hypothesized that the proportion of food energy lost in excretion should be much lower in herbivorous fishes than in carnivorous fishes because of the low protein content of plant diets. The results of this study do not support this hypothesis. Although plant diets usually have lower protein content than animal diets, plant protein may be of a lower quality than animal protein, and hence a larger proportion of dietary protein may be catabolized in lish fed plant rather than animal protein. In the present study, two independent estimates were available for the metabolic rate of starving fish. The fasting metabolism was calculated from a regression equation from Cui et al. ( 1993b), and the total metabolism (equal to fasting metabolism by definition) was estimated from data of this study. The two estimates were very similar (Table 5). At the maximum ration, fasting metabolism was only 3.56% of food energy, which was similar to the value of 4.1% for grass
Y. Cui et al. / Aquaculture 123 (1994) 95-l 07
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carp fed pelleted feeds at the ration of 12% body weight per day (calculated from data in H&man and Valentijn, 198 1), but much lower than the values (6.815.4%) reported for 6 fish species fed tub&id worms (Cui and Liu, 199Ob). The lower proportion in the grass carp may be a result of the higher feeding rate in this species. The proportion of food energy allocated to total metabolism tended to decrease with increased ration, but the proportion allocated to feeding metabolism was rather constant, suggesting that the decrease in allocation to total metabolism was simply a result of decreasing allocation to fasting metabolism. Based on the published energy budgets for 14 fish species, Cui and Liu ( 199Oc) calculated the following average energy budget for fish fed ad libitum rations: lOOA=60R+40G
(A=C-F-U)
s
In the present study, grass carp fed ad libitum allocated 74.4% of the assimilated energy to metabolism, and 25.6% to growth. Grass carp allocated 73-84% of the assimilated energy to metabolism and 16-27% to growth in a study by Cui et al. ( 1992). In grass carp fed pelleted diets, 69.0-72.6% of the assimilated energy was channelled to metabolism and 27.4-3 1.O%to growth (calculated from the data in Carter and Brafield, 199 1). These results suggest that the grass carp has a low growth efficiency and high metabolic expenditure. This conclusion is inconsistent with that from two previous studies on the energy budget of the grass carp, which suggested that grass carp had a low metabolic expenditure (Stanley, 1974; Wiley and Wike, 1986)) Cui et al. ( 1992) have suggested that there may be some erroneous or unjustified assumptions in the calculation of the energy budget in these two earlier studies. The low nutritional quality of the plant diet and the high proportion of time needed for feeding (Cui et al., 1993a) in the herbivorous grass carp may partly account for their high metabolic expenditure. Acknowledgements
This study was supported by the Natural Science Foundation of China and partly by the State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Academia Sinica. Thanks are due to Miss Zou Hong for technical assistance, and to R.J. Wootton and an anonymous referee for critical comments on the manuscript. References Brett, J.R. and Groves, T.D.D., 1979. Physiological energetics. In: W.S. Hoar, D.J. Randall and J.R. Brett (Editors), Fish Physiology, Vol. VIII, Academic Press, New York, pp. 279-352. Cai, Z. and Curtis, L.R., 1989. Effects of diet on consumption, growth and fatty acid composition in young grass carp. Aquaculture, 8 1: 47-60. Carter, C.G. and Bralield, A.E., 1991. The bioenergetics of grass carp, Ctenopharyngodon idella (Val.): energy allocation at different planes of nutrition. J. Fish Biol., 39: 873-887. Chen, S., Liu, X. and Su, Z., 1993. Nutrition and bioenergetics of the Chinese herbivorous fishes with
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important food values. II. Maximum consumption and digestion of seven aquatic plants by Ctenopharyngodon idella and Megalobrama amblycephala. Acta Hydrobiol. Sin., 17: l-12. Cho, C.Y., 1992. The role of nutritional energetics research in formulating cost-effective diets for fish, with particular reference to salmonids. In: G.L. Allan and W. Dal1 (Editors), Proceedings, Aquaculture Nutrition Workshop, Salamander Bay. NSW Fisheries, Salamander Bay, Australia, pp. 916. Cui, Y. and Liu, J., 1990a. Comparison of energy budget among six teleosts. I. Food consumption, faecal production and nitrogenous excretion. Comp. Biochem. Physiol., 96A: 163-l 7 1. Cui, Y. and Liu, J., 199Ob. Comparison of energy budget among six teleosts. II. Metabolic rates. Comp. Biochem. Physiol., 97A: 169-174. Cui, Y. and Liu, J., 1990~. Comparison of energy budget among six teleosts. III. Growth rate and energy budget. Comp. Biochem. Physiol., 97A: 381-384. Cui, Y. and Wootton, R.J., 1988a. Pattern of energy allocation in the minnow, Phoxinus phoxinus (L.) (Pisces: Cyprinidae). Fun&. Ecol., 2: 57-62. Cui, Y. and Wootton, R.J., 1988b. Bioenergetics of growth of a cyprinid, Phoxinusphoxinus (L. ): the effect of ration, temperature and body size on food consumption, faecal production and nitrogenous excretion. J. Fish Biol., 33: 431-443. Cui, Y., Liu, S., Wang, S. and Chen, S., 1992. Growth and energy budget of young grass carp, Ctenopharyngodon idella Val., fed plant and animal diets. J. Fish Biol., 41: 23 l-238. Cui, Y., Chen, S., Wang, S. and Liu, S., 1993a. Laboratory observations on the circadian feeding patterns in the grass carp (Ctenopharyngodon idella Val.) fed three different diets. Aquaculture, 113: 57-64. Cui, Y., Wang, S. and Chen, S., 1993b. Rates of metabolism and nitrogen excretion in starving grass carp in relation to body weight. Acta Hydrobiol. Sin., 17: 375-376. Du Preez, H.H. and Cockroft, A.C., 1988a. Nonfaecal and faecal losses of Pomadasys commersonni (Teleostei: Pomadasyidae) feeding on the surf clam, Donaxserra. Comp. Biochem. Physiol., 9OA: 63-70. Du Preez, H.H. and Co&oft, AC., 1988b. Nonfaecal and faecal losses of the marine teleost, Lichia amia (Linnaeus, 1758 ) , feeding on live southern mullet, Liza richardsonii (Smith, 1864). Comp. Biochem. Physiol., 9OA: 71-77. Elliott, J.M., 1976a. Energy losses in the waste products of brown trout (Safmo trutta L.). J. Anim. Ecol., 45: 561-580. Elliott, J.M., 1976b. The energetics of feeding, metabolism and growth of brown trout (Salmo trutta L.) in relation to body weight, water temperature and ration size. J. Anim. Ecol., 45: 923-948. Elliott, J.M., 1979. Energetics of freshwater teleosts. Symp. Zool. Sot. Lond., 44: 29-61. From, J. and Rasmussen, G., 1984. A growth model, gastric evacuation, and body composition in rainbow trout, Salmo gairdneri Richardson, 1836. Dana, 3: 6 l-l 39. He, X. and Xie, H., 1966. Feeding habits of the grass carp (Ctenopharyngodon idellus) from the East Lake, Wuchang. In: Collected Papers of the 9th Plenary Congress of the Fisheries Research Committee of the West Pacific. Science Press, Beijing, pp_ 6-13. Huisman, E.A. and Valentijn, P., 1981. Conversion efficiencies in grass carp (Ctenopharyngodon idella Val.) using a feed for commercial production. Aquaculture, 22: 279-288. Lambert, P. and Dehnel, P.A., 1974. Seasonal variations in biochemical composition during the reproductive cycle of the intertidal gastropod Thais lamellosa Gmelin (Gastropoda, Prosobranchia). Can. J. Zool., 52: 305-3 18. Lesel, R., Fromageot, C. and Lesel, M., 1986. Cellulose digestibility in grass carp, Ctenopharyngodon idella and in goldfish, Carassius auratus. Aquaculture, 54: 1 l-l 7. Lindsay, G.J. and Harris, J-E., 1980. Carboxymethylcellulase activity in the digestive tract of fish. J. Fish Biol., 16: 219-233. Shireman, J.V. and Smith, C.R., 1983. Synopsis of biological data on the grass carp. FAO Fish Syn., 135: 86pp. Spotte, S., 1979. Fish and Invertebrate Culture - Water Management in Closed Systems. Wiley-Interscience, New York. Stanley, J.G., 1974. Energy balance of white amur fed Egeria. Water Hyacinth Control J., 12: 62-66.
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Steel, R.G.D. and Torrie, J.H., 1980. Principles and Procedures of Statistics. McGraw-Hill, New York. Ursin, E., 1967. A mathematical model of some aspects of fish growth, respiration, and mortality. J. Fish. Res. Bd Can., 24: 2355-2453. Wiley, M.J. and Wike, L.D., 1986. Energy balances of diploid, triploid and hybrid grass carp. Trans. Am. Fish. Sot., 115: 853-861. Wen, Z., 1990. Studies on aquatic vegetation and rational carrying capacity of grass carp, Ctenopharyngodon idella Val., in Lake Niushanhu, M.Sc. Thesis, Institute of Hydrobiology, Academia Sinica, Wuhan, P.R. China.
Aquaculture 123 (1994) 95-107
Effect of ration size on the growth and energy budget of the grass carp, Ctenopharyngodon idella Val. Yibo Cui*, Shaolian
Chen, Shaomei
Wang
Institute of Hydrobiology, Academia Sinica, Wuhan, People’s Republic of China 430072
(Accepted 20 December 1993 )
Abstract Young grass carp ( 12- 13 g ) were kept at five ration levels ranging from starvation to ad libitum feeding at 30°C. They were fed duckweed. Food consumption, absorption efftciency and growth were determined directly, and metabolism and nitrogenous excretion calculated indirectly from energy and nitrogen budgets, respectively. The relationship between specific growth rate and ration size was linear. Absorption efficiency for energy was not affected by ration size and averaged 50.6 k 0.57% (mean I!Ise. ). Depending on ration size, energy lost in excretion accounted for 4.55.9% of the food energy, energy channelled to metabolism accounted for 34.4-48.3% of the food energy, and energy retained as growth accounted for 6.7-l 1.9% of the food energy. Regardless of ration, a constant proportion of food energy (30.7%) was accounted for by feeding metabolism (total metabolism minus fasting metabolism). The energy budget at the maximum ration was: 100C=49.1F+4.5U+3.6Rfa+30.9Rfe+ ll.9G, where C, F, U, Rf, Rfe and G represent food consumption, faecal production, excretion, fasting metabolism, feeding metabolism and growth, respectively.
1. Introduction Ration size is an important factor affecting the growth and energy budget of fish (Brett and Groves, 1979). The effects of ration size on the energy budget have been studied in carnivorous and omnivorous fishes (Elliott, 1976b; Brett and Groves, 1979; From and Rasmussen, 1984; Cui and Wootton, 1988a), but less is known about herbivorous fishes. Under natural conditions, the diet of the grass carp consists almost entirely of *Corresponding author. Current address: Department Davis, CA 956 16, USA.
of Animal Science, University
0044-8486/94/$07.00 0 1994 Elsevier Science B.V. All rights reserved SSDI 0044-84860044-8486 (94)00002-6
of California,
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macrophytes (He and Xie, 1966; Wen, 1990). In China, macrophytes are the major food used in the culture of this species. This study investigated the effects of ration size on the growth and energy budget in the grass carp fed a macrophyte diet. The energy budget of fish can be written as:
C=F+U+R+G where C is energy intake from food, F is energy lost in faeces, U is energy lost in nitrogenous excreta, R is energy expended in metabolism and G is energy deposited as growth. Metabolism is conventionally divided into three components: standard metabolism, specific dynamic action (SDA) and activity metabolism (Brett and Groves, 1979). Standard metabolism is defined as the metabolic rate of resting, unfed fish, but since fish are rarely at complete rest, it is difficult to obtain accurate estimates of standard metabolism unless the activity level of the fish can be quantified. SDA is often difficult to separate from activity metabolism. Therefore, in this paper, we have adopted the concepts of Ursin ( 1967 ) and divided metabolism into fasting metabolism (R,) and feeding metabolism (R, ) . Fasting metabolism is defined as the metabolic rate of undisturbed fish during long-term starvation, which is an approximation of standard metabolism (Elliott, 1976b). Feeding metabolism is the metabolic rate of a feeding fish over the fasting level, which is approximately equivalent to the sum of SDA and activity metabolism (From and Rasmussen, 1984).
2. Materials and methods Growth experiment Most parameters of the energy budget were obtained from data of a growth experiment. The fish were held in 250-litre glass aquaria, each connected to a filter tank containing 40 litres of clinoptilolite (diameter 3-5 mm), a natural zeolite which has a strong adsorption capacity for ammonia (Spotte, 1979). Water re-circulation was maintained by an air-lift pump at about 1 l/min, with dechlorinated tap water introduced at about 0.1 l/min to each aquarium. Additional aeration was provided intermittently for about 30 min each hour. A submersed heater, controlled by a thermostat, was used to maintain water temperature at the desired level. One hundred and fifty young-of-the-year grass carp were obtained from a hatchery and reared in the laboratory for 5 weeks before the experiment. Water temperature was gradually adjusted (2-3 "C/day) to the experimental temperature (30°C). The fish were then held at this temperature for a week before the start of the experiment. The photoperiod was 12L/ 12D. The fish were fed duckweed during the acclimatization period. The experiment lasted 3 weeks. The initial sizes of the fish are presented in Table 2. At the start of the experiment, 45 fish, which had been starved for 2 days, were weighed and placed into 15 aquaria (3 fish per aquarium). Fish in each
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aquarium were individually identified by fin-clipping. The aquaria were divided into 5 groups, with 3 aquaria in each group. The initial rations imposed were 0, 25%, 50%, 75% of the initial fish weight per day, and ad libitum. As fish fed the higher rations were expected to exhibit significant weight gains during the experiment, rations for the 50% and 7 5% groups were increased to 55% and 8 5% of the initial weight during the second week, and to 65% and 100% during the third week, respectively. Each day, the prescribed quantity of duckweed (Spirodela poZyrhiza) was weighed and put in each aquarium. Excess food was provided to fish in the ad libitum ration group. Any uneaten food was collected the next day and weighed. To remove excess water, both supplied and recovered duckweed were centrifuged for 3 min before being weighed. Each day a subsample of food was dried to constant weight at 70’ C to determine the dry matter content. Dry matter content was also determined for samples of uneaten food. The weight of food consumed was estimated in terms of dry weight using the mean dry matter contents of supplied and recovered duckweed. Faeces from each aquarium were collected daily by siphoning and dried to constant weight at 70 ’ C. At the end of the experiment, the fish were starved for 2 days and weighed. They were dried to constant weight at 70’ C, reweighed and homogenized. Nitrogen and energy contents were determined for each experimental fish, and for 10 control fish killed at the start of the experiment. In addition to the nitrogen and energy measurements, content of crude fibre was determined for the faecal sample from each aquarium, and lipid, ash and crude fibre measured for the duckweed. Nitrogen was determined by the Kjeldahl method, lipid by chloroformmethanol extraction (Lambert and Dehnel, 1974)) ash by combustion at 550 oC, and energy by bomb calorimetry. Protein content was calculated from nitrogen content by multiplying by 6.25. Crude fibre was determined in a Fibertec System (Tecator) by digestion sequentially with 0.128 M HzS04 and 0.223 M KOH, followed by combustion at 500°C. Two to four measurements were performed for each sample. Calculation of results
Absorption efficiency ( l-F/C) was calculated using crude tibre as an inert indicator (Cai and Curtis, 1989) : Absorption efficiency = I _ % crude fibre in food/nutrient or energy content in faeces x 1o. % crude fibre in faeces/nutrient or energy content in food Nitrogen excretion (En) was indirectly estimated from the nitrogen budget equation, a method suggested by Cho ( 1992 ) : En=C,-F,-G, where C,, is nitrogen intake from food, F,, nitrogen lost in faeces, and G, nitrogen retained in the fish body. Energy lost in excretion ( U) was calculated from nitro-
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gen excretion, assuming that all the nitrogen excreted was in the form of ammonia and that a calorific value of 24.8 J/mg N was appropriate for ammonia (Elliott, 1976a). Energy growth (G) was calculated as the change in the total energy content of the fish; the initial energy content per unit weight of the experimental fish was estimated from the average value of the control fish. Total metabolism (R) was estimated as the difference between C and I;, U and G (Elliott, 1976b). Fasting metabolism (I&) was calculated from a regression equation relating Rf, @J/day) to body weight ( W, g) for grass carp at 30°C (Cui et al., 1993b): In Rf, = -2.372+0.753
In W
The equation was calculated from data of a 5-week starvation experiment. mean value of the initial and final weight of the fish was used for calculation. difference between R and Rfa was feeding metabolism (R,) . The specific growth rate in wet weight (SGRw ) was calculated as: SGRw= 100x (In w,-ln
The The
?K,)/t
where I+‘,is the final and W, the initial weight of the fish, and t the experimental period (2 1 days). Specific growth rates in dry matter ( SGRd), protein ( SGRp) and energy (SGRe) were calculated similarly. Validation of use of crudefibre as an inert indicator for digestibility measurement To justify the use of crude fibre as an inert indicator for digestibility measurement, an experiment was conducted to compare the absorption efficiencies determined by complete quantification of faeces and by using crude fibre as an indicator. Grass carp weighing 33.7-46.1 g (mean 40.3 g) were obtained from a hatchery and reared in the laboratory for 10 days before the experiment. The food used was leaves of the green Chinese cabbage (Brassica chinensis) . The fish were randomly divided into two groups. Group A was used for complete quantification of faeces, and Group B for the crude fibre method. Fish in Group A were reared in 8 rectagular plexiglass tanks containing 40 litres of water (2 fish per tank), and fish in Group B in 5 circular tanks with conical bottoms (water volume, 50 litres; 6 fish per tank). Water in each tank was replenished once a day. For complete quantification of faeces, fish in Group A were starved for 3 days and, on the day of experiment, each tank received a weighed quantity of food at 9:O0. Five subsamples of food were weighed and dried to constant weight at 70” C to determine dry matter content. At 15:00, uneaten food was recovered, dried at 70°C and weighed. Faeces produced during 15:00-23:00 were collected by pippeting as soon as they were egested, and dried at 70°C. An additional faecal collection was made the next morning. Since the amount of faeces produced overnight was very small, errors associated with leaching during this period were regarded as negligible. For the crude fibre method, fish in Group B were fed excess quantities of food daily. Faecal samples accumulated in the faecal trap at the bottom of each tank were collected 4 times a day for 3 days and dried at 70°C. The content of crude fibre was measured for the food and faeces. Water temperature during the experiment was 17- 18 ‘C.
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Statistical analysis
Statistical analyses were made based on the mean values for each aquarium. One-way analysis of variance was used to test the significance of differences among ration groups. Bartlett’s test was used to check the homogeneity of variance among treatments. Since this assumption was met in all the analyses, no transformations were made on the data. Least-squares regression was applied to develop predictive relationships (Steel and Torrie, 1980).
3. Results Validation of use of crudefibre as an inert indicator for digestibility measurement
Absorption efficiency for dry matter determined by complete quantification of faeces was 65.77 + 0.76% (mean + s.e. ), and that determined using crude Iibre as an indicator was 66.73 + 0.6 1%. A t-test showed no significant difference between the two measurements (t = 0.88, I’= 0.40). It was concluded that crude fibre was a reliable inert indicator for digestibility measurement for the grass carp. Chemical composition and energy content of duckweed andfish body
Chemical composition and energy content of duckweed and fish body are shown in Table 1. Analysis of variance showed significant differences in the final dry matter, protein and energy content of fish body among ration groups (PC 0.0 1 in all cases). Regression analysis showed the following relationships between dry matter (DRY: % wet weight), protein (PROTEIN: % wet weight) or energy (ENERGY: kJ/g wet weight) content and ration level (RLz % body weight/day) : DRY= 16.45+O.O396RL
(n= 15,
PROTEIN = 11.4 1 + 0.0289RL
Sample Duckweed Fish
(n= 15, (n= 15,
ENERGY=2.77+0.01llRL Table 1 Chemical composition
r*=0.900) r*=0.786)
r2=0.91 1)
and energy content of food and fish body (mean + s.e. ) ’
Ration group
Dry matte?
Energy3
Protein*
Lipid2
Ash*
Crnde fibre’
6.06 * 0.08 19.24kO.37 16.30+0.66a 17.69+0.35’= 18.38f0.10” 18.99+0.25” 21.07f0.12”
1.08 3.64jrO.10 2.74?~0.16~ 3.13f0.07b 3.31?0.02b 3.42 + 0.02b 4.10+0.07c
2.17 12.24kO.14 10.87 + 0.45” 12.40*0.26b 13.331f-0.26ti 13.44rtO.26”= 14.46kO.26’
0.19
0.89
0.68
Control 0% 25% 50% 75% Ad libitum
‘Letters after each value indicate results of multiple comparison tests (Tukey’s procedure); letter are not significantly different from each other at the 0.05 level. ‘As % wet weight. ‘As kJ/g wet weight.
means with the same
0 25.0*0.2 48.220.4 68.3+ 1.6 116.0f2.9
Starvation 25% 50% 75% Ad libitum
12.3? 1.8 12.1k1.9 12.3* 1.7 12.1+ 1.8 13.3+ 1.7
Initial weight (g)
-0.49+0.11” 0.34 f 0.06b 1.47+0.12” 2.04 + 0.22” 3.41 f0.99d
Wet weight
- 1.47 * 0.25” 0.00 * 0.06b 1.49 * 0.04” 2.10f0.19” 3.81 +0.04d
Protein
- 1.87?0.31a -0.39fO.lOb 1.031tO.11” 1.74k0.20c 3.97&0.04d
Energy
means with the same letter are not significantly different
- 1.30+0.22” - 0.07 * 0.07b 1.26kO.10’ 1.98+0.16d 3.84f 0.07’
Dry weight
Specific growth rate (%/day)
tests (Tukey’s procedure);
11.0+1.1 13.0+ 1.9 16.8f2.3 18.8k3.1 27.2 + 3.8
Final weight (9)
‘Letters after each value indicate results of multiple comparison from each other at the 0.05 level.
Ration (% day)
Ration group
Table 2 Effect of ration size on the specific growth rates in the grass carp fed duckweed at 30” C (mean f s.e.) l
E,
S
s 2 S J F
!? E $
2
R
0 Et. 2
!?
0
Y. Cui et al. /Aquaculture 123 (1994) 9.5-107
Ration Fig. 1. Relationship 30°C.
(96 body weight
101
day-l)
between specific growth rates and ration size for the grass carp fed duckweed at
Table 3 Effect of ration size on the conversion efficiencies in the grass carp fed duckweed at 30°C (mean & s.e. ) ’ Ration group
25% 50% 75% Ad libitum
Conversion efficiency (%) Wet weight
Dry weight’
Protein
Energy
1.4OI!ZO.30” 3.03+0.30b 2.95 ? 0.36b 2.82+0.11b
Negative growth 8.00 I!Y 0.70 9.99kO.85 10.62kO.28
0.59+ 1.53” 18.71 +0.53b 18.64 f 2.03b 20.28 I!I0.83b
Negative growth 6.75 kO.78” 8.17* l.Ola 1 1.86+0.48b
‘Letters after each value indicate results of multiple comparison test (Tukey’s procedure); with the same letter are not significantly different from each other at the 0.05 level. *No significant difference among ration groups.
means
Growth Mean values of specific growth rates at each ration are shown in Table 2. SGR linearly with increased ration (Fig. 1) . Regression analysis showed the following relationships between SGR (%/day) and ration level (RL: % body weight/day): increased
SGRw= -0.385+0.0338RL
(n= 15,
r2=0.960)
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123 (1994) 95-107
SGRd= - 1.123+0.0440RL
(n= 15, A0.973)
SGRp= - 1.122+0.0448RL
(n= 15, A0.954)
SGRe= - 1.657+0.0496RL
(n= 15, r2=0.969)
Conversion efficiencies ( 100 x G/C) were calculated for groups where growth rate was positive (Table 3 ). Analysis of variance showed significant differences in conversion efficiencies for wet weight, protein and energy among ration groups (P
Absorption
25% 50% 75% Ad libitum
efficiency (%)
Dry matter
Protein
Energy2
41.1 43.1 43.1 46.6
74.220.1” 76.6f0.7b 77.6f0.1b 76.4+0.3b
49.5 I!I1.3 51.2rtl.111 51.0* 1.3 50.8 & 0.9
f 1.5” f0.6” kO.9” 2 0.7b
‘Letters after each value indicate results of multiple comparison tests (Tukey’s procedure); with the same letter are not significantly different from each other at the 0.05 level. ‘No significant difference among ration groups.
means
Table 5 Effect of ration size on the energy budget of the grass carp fed duckweed at 30 ’ C (mean + s.e. ) ’ Ration group Starvation2 C W/g/day)
0
50%
75%
Ad libitum
0.271 kO.003
0.522+0.010
0.740+0.176
1.256kO.031
50.54? 1.26 5.86kO.13 18.60f0.87 29.66 + 0.24 48.26 kO.24 -4.66+ 1.77
48.78? 1.09 4.61 kO.08 9.28kO.31 30.58 + 0.39 39.87kO.68 6.75 +0.78
49.00* 1.27 4.69kO.17 6.47f0.15 31.70+ 1.99 38.17k2.07 8.17f 1.01
49.241!~0.86 4.47 + 0.04 3.56kO.10 30.87k1.11 34.43kl.11 11.861LO.48
42.69 I!Z1.66 68.21k3.15 110.90f3.12 -10.90?3.12
19.92kO.57 65.65 f0.98 85.57* 1.40 14.43* 1.40
13.97LO.42 68.29k2.61 82.26 + 2.50 17.74k2.50
7.7020.36 66.66 + 1.48 74.36 Y?1.26 25.64f 1.26
25%
As percentages of C
F u
Ra, Rr,
R
G
0
0.006 f 0.001 0.05 1 IL0.002 0.05 1 rt 0.008 -0.058 f 0.009
As percentages of A Rf, Rfe R G
‘Symbols: C=food consumption; A=assimilated energy (C-F-U); F=faecal U=excretion; Rf,=fasting metabolism; R,=feeding metabolism; R= total metabolism; ‘Values for the starving fish were expressed as H/g/day.
production; G=growth.
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efficiency for dry weight (P> 0.05 ). Conversion efficiencies tended to increase with increased ration. Absorption efficiency Absorption efficiencies of dry matter, protein and energy are shown in Table 4. Analysis of variance showed significant differences in absorption efficiency of dry matter (P< 0.05) and protein (P< 0.01) among ration groups. There was a tendency for absorption efficiency to increase at higher rations. However, absorption efficiency of energy was not significantly different among the ration groups (P> 0.05); the mean absorption efficiency of energy was 50.6 2 0.57% ( + s.e. ). Energy budget Table 5 shows the energy budget at each ration level. The pattern of energy allocation varied with ration size. The proportion of food energy lost in excreta ranged from 4.5 to 5.9% (Table 5), and the mean proportion was 4.9%. There was a tendency for this proportion to decrease with increased ration. The proportions of food and assimilated (C-F-U) energy channelled to fasting metabolism tended to decrease with increased ration, but the proportions channelled to feeding metabolism were relatively constant; on average, feeding metabolism accounted for 30.7% of the food energy, or 67.2% of the assimilated energy. 4. Discussion The absorption efficiency of the grass carp determined using crude fibre as an inert indicator agreed well with that determined by complete quantification of faeces, suggesting that grass carp could hardly digest crude fibre. This result is consistent with the findings of several other studies, which indicated that the cellulase activity in the intestine of the grass carp was very low (Lindsay and Harris, 1980; Lesel et al., 1986). Crude fibre can thus be regarded as a reliable inert indicator for the measurement of absorption efficiency in the grass carp. In the present study, two components of the energy budget were indirectly estimated by difference. Energy lost in excretion was calculated from the nitrogen budget, and metabolism from the energy budget. Theoretically, both the nitrogen and energy budgets should be balanced. However, the pooled errors associated with the directly determined components were added to the calculated component. Thus, the reliability of the indirectly determined components depends on the accuracy of the directly determined ones. The measurement of food consumption should be accurate. Estimation of nitrogen and energy growth should be accurate too, since the final nitrogen and energy content was determined for each individual. Errors may arise from the estimation of initial nitrogen and energy content from the mean values of the control tish, but the variations in the nitrogen and energy contents among the control fish were reasonably small (95% CL was 1.98-2.26% for nitrogen content and 3.35-3.94 kJ/g for energy content; see Table 1). The accuracy of absorption
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Y. Cui et al. /Aquaculture 123 (1994) 95-107
efficiency measurement depends largely on the validity of using crude libre as an inert indicator, which was justified in the present study, although some errors may arise from nutrient leaching in the faeces. The assumption that all the nitrogen excreted was in the form of ammonia should not introduce great errors, since ammonia is usually the predominant nitrogenous compound excreted in teleosts, and the calorific values of ammonia-nitrogen (21.83 J/mg) and urea-nitrogen (23.03 J/mg) were reasonably close (Elliott, 1979). Also, excretion is usually a small component of energy budget and errors associated with its estimation are unlikely to greatly influence the estimation of metabolism. In most carnivorous and omnivorous fishes, the relationship between growth rate and ration size is a decelerating curve (Brett and Groves, 1979); the conversion efficiency is highest at an intermediate ration, and decreases with further increases in ration. Grass carp fed a pelleted feed showed a similar pattern of growth-ration relationship (Huisman and Valentijn, 198 1). In the present study, the growth rate of the grass carp fed duckweed was linearly related to ration size, and there was no decrease in conversion efficiency at high rations. There are two possible reasons for this discrepancy. One reason may be that the grass carp in the ad libitum group were not feeding to their maximum rates, although the rate of food consumption in this group ( 116%) was probably among the highest reported for this species (Shireman and Smith, 1983; Cai and Curtis, 1989; Chen et al., 1993). The second possibility was that, because of the low energy content and absorption efficiency of the plant food, grass carp fed plants may not be able to achieve the level of absorbed energy when conversion efficiency starts to decline; thus a linear growth-ration relationship may be typical for grass carp fed plants. In the present study, energy lost through nitrogenous excretion accounted for 4.47-5.86% of the food energy in the grass carp. A similar value (5%) was obtained by Cui et al. ( 1992) for grass carp fed duckweed (a mixture of Lemna minor and Spirodela polyrhiza). These indirect estimates were close to the values of 3.1-4.7% directly determined by Carter and Bralield ( 1991) for grass carp. These values were within the range reported for carnivorous and omnivorous fishes (Cui and Wootton, 1988b; Du Preez and Co&oft, 1988a,b; Cui and Liu, 1990a). Brett and Groves ( 1979) hypothesized that the proportion of food energy lost in excretion should be much lower in herbivorous fishes than in carnivorous fishes because of the low protein content of plant diets. The results of this study do not support this hypothesis. Although plant diets usually have lower protein content than animal diets, plant protein may be of a lower quality than animal protein, and hence a larger proportion of dietary protein may be catabolized in lish fed plant rather than animal protein. In the present study, two independent estimates were available for the metabolic rate of starving fish. The fasting metabolism was calculated from a regression equation from Cui et al. ( 1993b), and the total metabolism (equal to fasting metabolism by definition) was estimated from data of this study. The two estimates were very similar (Table 5). At the maximum ration, fasting metabolism was only 3.56% of food energy, which was similar to the value of 4.1% for grass
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carp fed pelleted feeds at the ration of 12% body weight per day (calculated from data in H&man and Valentijn, 198 1), but much lower than the values (6.815.4%) reported for 6 fish species fed tub&id worms (Cui and Liu, 199Ob). The lower proportion in the grass carp may be a result of the higher feeding rate in this species. The proportion of food energy allocated to total metabolism tended to decrease with increased ration, but the proportion allocated to feeding metabolism was rather constant, suggesting that the decrease in allocation to total metabolism was simply a result of decreasing allocation to fasting metabolism. Based on the published energy budgets for 14 fish species, Cui and Liu ( 199Oc) calculated the following average energy budget for fish fed ad libitum rations: lOOA=60R+40G
(A=C-F-U)
s
In the present study, grass carp fed ad libitum allocated 74.4% of the assimilated energy to metabolism, and 25.6% to growth. Grass carp allocated 73-84% of the assimilated energy to metabolism and 16-27% to growth in a study by Cui et al. ( 1992). In grass carp fed pelleted diets, 69.0-72.6% of the assimilated energy was channelled to metabolism and 27.4-3 1.O%to growth (calculated from the data in Carter and Brafield, 199 1). These results suggest that the grass carp has a low growth efficiency and high metabolic expenditure. This conclusion is inconsistent with that from two previous studies on the energy budget of the grass carp, which suggested that grass carp had a low metabolic expenditure (Stanley, 1974; Wiley and Wike, 1986)) Cui et al. ( 1992) have suggested that there may be some erroneous or unjustified assumptions in the calculation of the energy budget in these two earlier studies. The low nutritional quality of the plant diet and the high proportion of time needed for feeding (Cui et al., 1993a) in the herbivorous grass carp may partly account for their high metabolic expenditure. Acknowledgements
This study was supported by the Natural Science Foundation of China and partly by the State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Academia Sinica. Thanks are due to Miss Zou Hong for technical assistance, and to R.J. Wootton and an anonymous referee for critical comments on the manuscript. References Brett, J.R. and Groves, T.D.D., 1979. Physiological energetics. In: W.S. Hoar, D.J. Randall and J.R. Brett (Editors), Fish Physiology, Vol. VIII, Academic Press, New York, pp. 279-352. Cai, Z. and Curtis, L.R., 1989. Effects of diet on consumption, growth and fatty acid composition in young grass carp. Aquaculture, 8 1: 47-60. Carter, C.G. and Bralield, A.E., 1991. The bioenergetics of grass carp, Ctenopharyngodon idella (Val.): energy allocation at different planes of nutrition. J. Fish Biol., 39: 873-887. Chen, S., Liu, X. and Su, Z., 1993. Nutrition and bioenergetics of the Chinese herbivorous fishes with
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