Energy Metabolism in Oreochromis niloticus
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1 Aquuculture, 79 (1989) Eisevier Science Pubhshers B.V., Amsterdam - Printed in The Netherlands 283 Energy Metabolism in Oreochromis niloticus K.-H. MEYER-BURGDORFF, M.F. OSMAN and K.D. GUNTHER Institute of Animal Physiology and Animal Nutrition, University of GGttingen, D-3400 GBttingen (Federal Republic of Germany) ABSTRACT Meyer-Burgdorff, K.-H., Osman, M.F. and Giinther, K.D., Energy metabolism in Oreochromis niloticus. Aquaculture, 79: A series of experiments was carried out to study the energy metabolism of Oreochromis niloticus. During starvation the energy loss of the fish was 25 kj kg-. d- (54 kj kg-l d-l). Maintenance requirement for energy amounted to 57 kj ME kg-, d-l (116 kj ME kg- d-l). Apparent utilization of metabolizable energy (ME) below maintenance requirement was determined as k, = In growing tilapia, increased feeding level ( g kg-. d- ) caused a continuous decline in availability of gross energy (GE) (q = ). The utilization of metabolizable energy for growth remained rather constant (k,=0.67), independent of feeding level. INTRODUCTION Several experiments have been conducted to study the quantitative and qualitative protein requirement of tilapia (Davis and Stickney, 1978; Viola and Arieli, 1983; Viola and Zohar, 1984). Likewise, investigations on the optimum protein/energy ratio in the diet of some tilapia species are reported in the literature (Mazid et al., 1979; Winfree and Stickney, 1981; Jauncey, 1982). Little information can be found on energy metabolism of tilapia. Hepher et al. ( 1983) calculated metabolizable energy (ME =0.75*GE) of red tilapia at different feeding levels without measuring non-fecal excretions and/or heat production. The only elaborated energy budgets in the literature were established by Musisi (1984) determining oxygen consumption, carbondioxide excretion and ammonia excretion of Sarotherodon ( = Oreochromis) mossambicus. We carried out a series of experiments to investigate the energy metabolism of 0. niloticus during starvation, at maintenance level and at different feeding levels. 0044~8486/89/$ Elsevier Science Publishers B.V.
2 284 TABLE 1 Composition and proximate analysis of the feed used in experiments II and III Feed composition (g kg- ) Fish meal 500 Wheat 420 Sunflower oil 40 Mineral mixture 20 Vitamin mixtureb 20 Proximate analysis Dry matter Crude ash Crude protein Ether extract Gross energy 88.7% 11.4% of DM 40.1% of DM 11.3% of DM 21.9 kj g-i DM Mineral mixture (g kg-i): 336 CaCO,, 502 KH2POI, 162 MgS04*7Hz0. bvitamin mixture (per kg): IU vit. A, IU vit. D,, 2500 mg vit. E, 1000 mg vit. KS, 5000 mg vit. Bi, 5000 mg vit. B,, 5000 mg vit. Be, 5000 pg vit. Blz, mg inositol, mg pantothenic acid, mg choline chloride, mg niacin, 1000 mg folic acid, 250 mg biotin, mg vit. C. MATERIAL AND METHODS All the experiments were carried out in a recirculation system at a water temperature of 26 C. In order to estimate the amount of energy which fasting 0. niloticus derived by filtration of the circulating water, duplicate tanks were supplied with tap water. During the experimental period, groups of 0. niloticus fingerlings (7-26 g initial weight; lo-25 fish/group) were kept in 350-l tanks or simultaneously in 12-1 metabolism chambers to measure oxygen consumption. Energy loss during starvation (experiment I) was determined following the principles of the comparative slaughter technique only. A combination of comparative slaughter technique and indirect calorimetry was used to follow the partition of gross energy (GE) at maintenance level (experiment II) and in growing 0. niloticus (experiment III). From oxygen consumption, the heat production (HP) was calculated using oxycalorific coefficients of kj/g 0, at maintenance level and W/g 0, for growing tilapia (Huisman, 1976). Metabolizable energy was calculated as the sum of net energy loss or net energy retention and heat production. Composition and proximate analysis of the ration used in experiments II and III are shown in Table 1. RESULTS AND DISCUSSION I. Energy metabolism in fasting 0. niloticus As can be seen from the data in Table 2, there were no differences in loss of weight, protein and lipid between triplicate groups of tilapia starved in recir-
3 285 TABLE 2 Loss of weight, nutrients and energy of fasting 0. niloticus in experiment I (A: g kg-.! d-, kj kg-. d-i; B: g kg- d-l, kj kg-id- ; S+SD) Tap water Recirculating water A B A B Wet weight LO f kO kO.29 Crude protein ) & * 0.14 Ether extract _ * _+O.lO Energy k ? k culating water or tap water. Independent of the origin of water, an energy loss of 25 kj kg-. d-l (54 kj kg-l d- ) was determined for fish weighing 22 g. Using a general equation derived from studies with 0. mossambicus (Caulton, 1978), a slightly higher routine metabolic expenditure of 61.4 kj kg- d-l was calculated. Hepher et al. (1983) observed an energy loss of fasting red tilapia (14 g; 24 C) of 40 kj kg-.8d-1 (94 kj kg-l d-l). The most important factors responsible for these differences are water temperature, duration of fasting, fish size and fish activity. Even during starvation, territorial tilapia show highly varying activity, depending on group size, sex ratio and density of fish. For sluggish fish like the mirror carp, energy loss during starvation ranged from 21 to 46 kj kg-. d-l (25 to 89 kj kg- d-l) (Huisman, 1976; Pfeffer et al., 1977). Although tilapia show higher activity and are normally kept at water temperatures 3 to 4 C higher than carp, energy metabolism was in the same range as found for carp. II. Energy metabolism of 0. niloticus at maintenance level The weight and nutrient balance of duplicate groups of 0. niloticus (26 g) at various feeding levels near to maintenance requirement are presented in Fig. 1. Increased ration size caused weight and protein gain while lipid remained in a negative balance indicating that lipid was the major fuel of energy metabolism in these fish. As can be seen from Table 3, even the highest feeding level resulted in a negative energy balance. A linear regression analysis was carried out to explain the relationship between metabolizable energy intake (MEi,~k,, X) and net energy loss (NEI,,,, y). According to the regression equation presented in Fig. 2, maintenance energy requirement of 0. niloticus amounted to 57 kj ME kg- - d-l or 116 kj kg-l d-l. The energy loss at zero intake derived from Fig. 2 was higher (35 kj kg-. d-l) than th e equivalent value from the first experiment (25 kj kg- - d- ). The differences might be due to the different methodical conditions involved, as discussed earlier. From the data of the second experiment the (ap-
4 286 g fish - 5 Body Weight 4 H Ether Extract 0 Crude Protein i o Feeding level, g kg-o.8 d-1 Fig. 1. Weight and nutrient balance of 0. niloticus in experiment II TABLE 3 Net energy loss (NE,,,,), total heat production and metabolizable energy intake (MEintik,) of 0. niloticus in experiment II (A: kj kg-. d-l; B: kj kg-l d- ; %+ SD) Feeding level (g kg-o.s d- ) NE,,, A B Heat production ME,,,, A B A B f f & f O.l& _ f f f f f f f _ f 0.7 loo.of 1.6 parent) utilization of metabolizable energy to meet maintenance requirement ( Iz,) was calculated as k, = Since apparent k, represents the amount of metabolizable energy needed to prevent a certain net energy loss (Van Es, 1972) and fish adapt to prolonged starvation periods, data of fasting fish were excluded from this calculation. Hepher et al. (1983) stated that maintenance requirement (ME ) of red tilapia was about twice as high as energy loss during starvation. For mirror carp (50 g, 20 C ) Schwarz and Kirchgessner (1984) determined a maintenance energy requirement of 45 kj digestible energy (DE) kg-o-75 d-l or 94 kj DE kg- d-l. A maintenance requirement of 66 kj ME kg-o.8 d- was found by Huisman (1976 ); a lower value was obtained by Becker et al. (1983) (22.7 kj ME kg-o.5 d-l) for the same species. Comparisons should be drawn carefully because different energy levels,
5 ME intake, kj kg- d- (x) kj kg-0.6d- (e) I I 1 I I I I I I I I I / 8 0 * kj kg- d-1 (x1 Nhoss, kj kg-o.8 d-1 (0) Fig. 2. Linear regression to explain the relationship between metabolizable energy intake (ME,*,, x) and net energy loss (NE,,.., y) of 0. niloticru in experiment II. weight exponents and methodical conditions were used. The utilization metabolizable energy for maintenance requirement calculated from net energy loss during starvation divided by maintenance requirement (ME) seems to be slightly higher in carp (km= 0.7; Huisman, 1976) than in tilapia. Although fish can be starved or fed below maintenance requirement for extremely long period, a & of 0.8 as found in homoeothermic monogastric animals (Van Es, 1972; Miiller and Kirchgessner, 1979) is not reached by tilapia or carp. III. Energy metabolism of 0. niloticus at different feeding levels In the third experiment, duplicate groups of 0. niloticus (7 g) were fed at six different feeding levels, ranging from, 14 to 25 g kg-*- d-l. As can be seen from Table 4, increased ration size caused improved growth rate (SGR), but inferior feed conversion (FC ) and protein utilization (PPV, PER). Fig. 3 shows that protein and lipid retention rose when feeding level was increased. But independent of feeding level, the relation between protein and lipid retention remained rather constant. Partition of gross energy in growing tilapia is summarized in Table 6. In relation to feed intake, energy metabolism of growing 0. niloticus ranged between 150 and 200 kj ME kg-o.8 d-l (360 and 440 kj ME kg-l d-l). The relative amount of metabolizable energy derived from gross energy (q) as presented in Table 6 dropped from almost 70% at low feeding level to 53% at high
6 288 TABLE 4 Specific growth rate (SGR), feed conversion (FC) and protein utilization (PPV, PER) of 0. niloticus in experiment III (x+_ SD) Feeding level SGR FC PPV PER (g kg-o.* d- ) (% d-l) (g DM feeding/ (% retention of intake ) (g gain/g crude ggain) protein intake) * ? kO kO k i kO f kO kO kO.W kO kO Iko k f0.11 g fish- Ether Extract 0 Crude Protein Feeding level. g kg -0.8 d -1 Fig. 3. Nutrient retention of 0. niloticus in experiment III. 24 feeding level. Because no feed loss was realized during the experimental period, increased feeding level might have caused a higher passage of feed through the digestive tract, resulting in depressed availability (digestibility) of gross energy. Independent of feeding level, about 52% of metabolizable energy was released as heat in 0. niloticus. Taking into account a maintenance requirement of 57 kj kg-. d-l, the utilization of metabolizable energy for growth above maintenance (&; Table 6) was not affected by feeding level, ranging from 0.65 to About 30% of gross energy was retained (ktot), but due to depressed availability (q) there was a tendency towards decreased figures when feeding
7 289 TABLE 5 Partition of feed energy (GE) in growing 0. niloticus in experiment III (A: kj kg-o.8 d- ; B: kj kg- d- ; af SD) Feeding level (g kg-o.8 d- ) Gross energy A 233.Ok kl.O f B ? f _ f 25.1 Metabolizable energy A 153.3kO kO f B 363.Ok kO h kll.l tl2.6 Heat production A 81.0 B Net energy retention A 72.3f kO f 6.8 B 165.5k kO Okll.l kll.l 213.7t-12.6 TABLE 6 Utilization of energy in growing 0. niloticus in experiment III ( kt: net energy retention/gross energy intake; q: metabolizable energy/gross energy intake; /q,,+,: net energy retention/metabolizable energy for maintenance and growth; &: net energy retention/ metabolizable energy for growth; X1 SD) Feeding level k tot 4 k m+g k, (g kg-o.8 d- ) ? f f _ * t k i IO ko i f * t level increased (Table 6). In comparison, only 10% of gross energy was retained in the energy budgets of 0. mossambicus established by Musisi (1984). The availability (4) of gross energy was in the same range as found in the present study. However, utilization of metabolizable energy for growth was much lower in 0. mossambicus because 84% of metabolizable energy was released as heat. Huisman (1976) found a similar relationship between ration size and relative amount of metabolizable energy (4) in mirror carp as in the present study.
8 290 In which way feeding level depressed the availability of gross energy is not clear because Schwarz and Kirchgessner (1982) found no effect of ration size on digestibility in carp. Very recently, the effect of feeding level on growth of mirror carp (33 g) was investigated in our institute by Miiller (1986) under similar conditions as in the present study. In comparison with 0. niloticus, stomachless carp could cope better with comparable ration size (q = ). The utilization of metabolizable energy for growth was slightly lower (k,= )) but improved when feeding level was increased due to high fat retention. As a practical implication from these results, a restricted feeding level (180 kj ME kg-o.8 d- ; 400 kj ME kg-l d-l) for intensive tilapia production must be recommended to ensure efficient utilization of feed energy. REFERENCES Becker, K., Eckhardt, 0. and Struck, J., Untersuchungen zum Erhaltungshedarf an ME von Spiegelkarpfen (Cyprinus carpio L.) bei unterschiedlichen Korpermassen. J. Anim. Physiol. Anim. Nutr., 50: Caulton, M.S., The effect of temperature and mass on routine metabolism in Sarotherodon mossambicus. J. Fish Biol., 13: Davis, A.T. and Stickney, R.R., Growth responses of Tilapia aurea to dietary protein quality and quantity. Trans. Am. Fish. Sot., 107: Hepher, B., Liao, I.C., Cheng, S.H. and Hsieh, C.S., Food utilization by red tilapia- effects of diet composition, feeding level and temperature on utilization efficiencies for maintenance and growth. Aquaculture, 32: Huisman, E.A., Food conversion efficiencies at maintenance and production levels for carp, Cyprinus carpio L., and rainbow trout, Salmo gairdneri Richardson. Aquaculture, 9: Jauncey, K., The effects of varying dietary protein level on the growth, food conversion, protein utilization and body composition of juvenile tilapias (Sarotherodon mossambicus). Aquaculture, 27: Mazid, M.A., Tanaka, Y., Katayama, T., Rahman, M.A., Simpson, K.L. and Chichester, C.O., Growth response of Tilupia zillii fingerlings fed isocaloric diets with variable protein levels. Aquaculture, 18: Miiller, C., Der EinfluR unterschiedlicher FiitterungsintensitLen auf einige Parameter des Energieumsatzes bei jungen wachsenden Spiegelkarpfen (Cyprinus carpio L.) im Erhaltungsund Leistungsstoffwechsel. Inst. Anim. Physiol. Anim. Nutr., Gottingen, Diplomarbeit (unpubl.). Miiller, H.L. and Kirchgessner, M., Untersuchungen zum energetischen Erhaltungsbedarf von Sauen. J. Anim. Physiol. Anim. Nutr., 42: Mu&i, L., The nutrition, growth and energetics of tilapia, Sarotherodon mossambicus. Cited from: Brafield, A.E., Laboratory studies of energy budgets. In: P. Tytler and P. Glow (Editors), Fish Energetics: New Perspectives. Croom Helm, London and Sydney, pp Pfeffer, E., Matthiesen, J., Potthast, V. and Meske, Ch., Untersuchungen zum Hungerumsatz von Karpfen. In: E. Pfeffer and Ch. Meske (Editors), Advances in Animal Physiology and Animal Nutrition; Studies on Nutrition of Carp and Trout. Paul Parey, Hamburg, pp Schwarz, F.J. and Kirchgessner, M., Zur Bestimmung der Ng-hrstoffverdaulichkeit beim Karpfen (Cyprinus carpio L.). 2. Mitteilung: Zum EinfluB von Futtermenge und Wassertemperatur. Bayer. Landwirtsch. Jahrb., 59:
9 Schwarz, F.J. and Kirchgessner, M., Untersuchungen zum energetischen Erhaltungsbedarf des Karpfens (Cyprinus carpio L. ). J. Anim. Physiol. Anim. Nutr., 52: Van Es, A.J.H., Maintenance. In: W. Lenkeit and K. Breirem (Editors), Handbuch der Tiererntirung, Vol. II. Paul Parey, Hamburg, pp. l-54. Viola, S. and Arieli, Y., Nutrition studies with tilapia. 1. Replacement of fishmeal by soybeanmeal in feeds for intensive tilapia culture. Bamidgeh, 35: Viola, S. and Zohar, G., Nutrition studies with market size hybrids of tilapia in intensive culture. 3. Protein levels and sources. Bamidgeh, 36: Winfree, R.A. and Stickney, R.R., Effects of dietary protein and energy on growth, feed conversion efficiency and body composition of Tilapiu aurea. J. Nutr., 111:
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