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An hypothesis on the control of food intake in fish
Aquaculture, 17 11979) 221-229 0 Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands
221
AN HYPOTHESIS ON THE CONTROL OF FOOD INTAKE IN FISH
OLA VAHL Institute
of Fisheries,
Uniuersity
of Tromsd,
P.O. Box
790,
9001
Tromsd
(Norway)
(Accepted 6 March 1979)
ABSTRACT Vahl, O., 1979. An hypothesis on the control of food intake in fish. Aquaculture, 221-229.
17:
An hypothesis on the control of voluntary food intake (appetite) in fish is presented. According to the hypothesis, only two parameters are necessary to design a feeding regime which might result in maximum growth of fish in an aquaculture system. The necessary parameters are maximum voluntary food intake in one meal, and evacuation rate of the stomach. This hypothesis is discussed in relation to empirical data.
INTRODUCTION
On the basis of experimental evidence Paloheimo and Dickie (1965) found that Winberg’s ‘basic energy equation’ adequately predicts growth in fish. The equation is AW --=R_T At
(I)
where the velocity of growth (5:) equals the rate of food consumption (R) minus the metabolic rate (T) expressed in equivalent energy terms. Both R and T are dependent upon a variety of biotic and abiotic factors (Ivlev, 1961; Brett et al., 1969; Brett and Sutherland, 1970). Given a set of abiotic factors, however, the daily rate at which food can be consumed is a prime factor, In the poultry, swine, and cattle industries such husbandry techniques as the use of ad Zibitum or increased feeding frequencies have been employed to increase feed consumption and growth, and to reduce production times. Although aquaculturists have used frequent feeding techniques for many years, few studies have been reported on the effects of frequency of feeding on the growth of fish (Palmer et al., 1951; Kono and Nose, 1971; Andrews and Page, 1975). A carefully designed feeding regime must depend on a knowledge of the control of food intake. The purpose of the present paper is to present an hypothesis for this control and a simple model based on the hypothesis.
222
CONTROL
OF FOOD INTAKE
The control of food intake in the central nervous system is relatively well known. It appears that the hypothalamus contains centers for feeding and satiety and that the satiety center acts by inhibiting the feeding center (Hightower and Janowitz, 1973). In spite of extensive study, the peripheral mechanisms controlling food intake are poorly known (Hightower and Janowitz, 1973). Intake of food, however, induces satiety and stimulates the mechanisms that are inhibitory to the feeding reflexes. Starvation, on the other hand, induces hunger and stimulates the feeding centers. Gastrointestinal and metabolic mechanisms are recognized as possible operating devices. The most important gastrointestinal mechanism is undoubtedly the stretch receptors in the stomach wall (Paintal, 1954). Severance of their connection to the central nervous system induces a hyperphagous condition comparable to that caused by lesion of the satiety center (Hightower and Janowitz, 1973). The effect of these stretch receptors is therefore to give information on available space in the stomach for a new meal. This available space corresponds to Ivlev’s (1961) concept of hunger. However, there is a delay between the development of voluntary food intake and gastric evacuation (emptiness of the stomach) (Brett, 1971; Elliott, 1975 a). Therefore, these stimuli are not the only agents in regulating the food intake. Presumably, metabolic factors are responsible for the delay in the development of hunger. Mayer (1955) has suggested that food intake is controlled in some way through the metabolism of glucose and Kennedy (1953) has put forward the theory that the total energy stores of the body are maintained at a certain predetermined level through the action of receptors monitoring the total level of metabolites in the blood. Whatever the mechanism may be, it is highly probable that metabolic factors play an important role in regulating the food intake. THE MODEL
The consumption of a meal gives rise to an increase in heat production and hence the oxygen consumption of an animal (Kleiber, 1961). This increase in metabolic rate is known as the specific dynamic action (SDA) of the food consumed. In fish, the SDA increases abruptly after feeding reaches a maximum and thereafter decreases more or less regularly to pre-feeding level (Averett, 1969; Muir and Niimi, 1972; Beamish, 1974; Vahl and Davenport, 1979). The biochemistry of SDA is incompletely understood, but the energy liberated is generally assumed to be largely due to the deamination of amino acids. The seemingly simple change in metabolic rate, which appears to be caused by processes in the liver (Buttery and Annison, 1973), is only the final result of many changes in the intermediary metabolism. If the rate of ingestion of amino acids is greater than their rate of utilization in protein synthesis,
223
excess amino acids must be deaminated, permitting biological oxidation or storage of the remaining carbon skeletons and excretion of the amino moieties. Accumulation of free amino acids or their amino fractions can create a condition toxic to the animal (Warren and Doudoroff, 1971). Therefore, it is reasonable to assume that the blood has a maximum carrying capacity for these substances and that their level might be an agent in controlling food intake. Accepting this hypothesis, the level of SDA reflects the degree of negative feed-back from the metabolites in the blood. Accordingly, a simplified flow diagram showing the fate of the ingested materials and the control of appetite can be put forward (Fig. 1).
Stomach
intestine
time-lag
*
Flow of materials
+
Flow of Information
Lwer
Blood
Receptors monltorlng the level of metabolltes in blood
Fig. 1. The basis for the hypothesis. Simplified diagram showing the flow of ingested materials and assumed flow of information and control of voluntary food intake (appetite).
After ingestion of a meal, the fullness of the stomach is monitored by the stretch receptors in the stomach. The fullness at any time is dependent on the evacuation rate, which in turn is proportional to the mass of food remaining in the stomach (Brett and Higgs, 1970). This can be expressed by the relation (Elliott, 1972) M, = Aoeekf
(2)
where M, is the amount in the stomach at time t, when A0 is a maximum meal ingested at time zero, and h is the instantaneous rate of gastric evacuation. Therefore the amount of A0 evacuated from the stomach, D,, at time t is D, = Ao(l - e-“f)
(3)
which is the information conveyed to higher centers by the stretch receptors. Thus the satiety center in the hypothalamus receives information about the free volume available in the stomach.
224
When the food is absorbed and processed further it will give rise to a higher level of metabolites in the blood. The level will be determined by the size and composition of the meal and by the time elapsed after ingestion. Since the SDA reaches a maximum some time after ingestion (Averett, 1969; Muir and Niimi, 1972; Beamish, 1974; Vahl and Davenport, 1979) there is a time-lag between the ingestion and the contribution of the meal to the level of metabolites. The extent of the time lag depends on the rates of stomach evacuation, absorption, and processing of the absorbed materials. The level of metabolites from the absorbed materials obviously cannot go below zero, and the simplest assumption regarding the processing rate is that it is always a constant fraction of the amount absorbed. The simplest expression satisfying these assumptions is the one describing a first order reaction. Accordingly, the simplest expression giving the level of metabolites from the absorbed materials at time t is L, a Dte-mt
= Ao(l - &t)e-mt
(4)
where L, is the level of metabolites from the absorbed materials at time t and m is the instantaneous rate of processing. For simplicity, the time-lag between evacuation of the stomach and absbrption is disregarded, as is the fact that not all ingested material is absorbed. This does not, however, affect the general conclusions. As the duration of SDA seems to be approximately equal to the time needed for absorption (Beamish, 1974), the instantaneous processing rate of absorbed materials cannot differ much from the rate of absorption, and under the assumptions made in Eqn. 4, from evacuation rate. Therefore, only a small error is made in assuming m = k. Eqn. 4 may then be written L, = A,,(1 - e-ht)ePkt
(5)
Eqn. 5 gives a curve which increases from zero to reach a maximum, whereafter it decreases. The time, a, to reach maximum is the time when.2 = 0 and depends on the value of k, but is independent of the size of the meal. The curve apparently belongs to the same family of curves as those assumed by Muir and Niimi (1972, their fig. 6) and shown by Vahl and Davenport (1979, their fig. l), describing the progress of SDA after ingesting a meal, and presumably the degree of negative feedback from the metabolites in the blood. The time, a, is therefore the time-lag from ingesting a meal till it has its largest effect on food uptake. If, in fact, there is a maximum level, L,, of metabolites in the blood which the animal can tolerate (Warren and Doudoroff, 1971), this will occur at the time a after ingesting a maximum meal. As all meals prior to time t contribute to the existing level, a new meal at time t must not be so large as to cause the level of metabolites to exceed the maximum level (L,) at time t + a. Accordingly, the carrying capacity as a fraction of L, for metabolites in the blood available for a new meal at time t is
225
The largest meal a fish can tolerate at time t is thus dependent on the available space in the stomach, D,, and the carrying capacity for metabolites available at time t + a. If hunger is defined as the largest meal tolerated, and the fish will eat to satisfy its hunger completely, the maximum voluntary food intake at the time t, V,, after ingesting a maximum meal is
Eqn. 6 disregards differences in the quality (e.g. moisture and protein contents) of the meals, and foraging and handling times. In an aquaculture system, food quality is assumed to be constant, and foraging and handling times are probably negligible (Kerr, 1971). Inherent in Eqn. 5 is the premise that L, = Ao/4. Substituting D, from Eqn. 3 and L, and Lt+a from Eqn. 5 in Eqn. 6 gives V, * Ao(l
- echt) (1-
Ao(l - e-h(t+al)e-b(t+al - -.0A
1
4 = Ao(l - c-ht) (1 - 2e-~(f+Q))2
(7)
Eqn. 7 shows that maximum voluntary food intake increases in a sigmoid pattern with time and approaches a plateau which corresponds to the maximum food intake in a single meal, Ao. DISCUSSION
Elliott (1975 a) studied the daily food consumption of brown trout and also measured the voluntary food intake in a group of fish (Fig. 2A). After being fed to satiation the voluntary food intake (and presumably hunger) per unit time of 90 g fish at 15°C increased in a sigmoid pattern with increasing deprivation time and approached a plateau after about 12-15 h. The greatest increase in food intake occurred between 7.5 and 10 h. The gastric evacuation rate (=h) of 90 g fish at 15°C is 0.284 (Elliott, 1972) and a = 2.5 h. The satiation time for a 90 g trout is 53 min (Elliott, 1975 b) but, assuming the maximum voluntary food intake in 15 min (A,) to be 160 mg (Elliott, 1975 a, his fig. 4), Vt can be calculated. It appears that Eqn. 7 predicts the development of voluntary food intake in brown trout fairly well. The plateau is reached after about 15 h, but the greatest increase according to the present model occurs after about 7 h, whereas the observed voluntary food intake increases at the highest rate from 8 to 10 h (Fig. 2A). Brett (1971) measured stomach capacity and voluntary food intake in sockeye salmon. His data show the same general pattern as Elliott’s. At 15°C
226
range. from (1975 b. fig.41
mean and Elliott
t 160
-
Vt = predicted voluntary hod Intake -
Of = gastric
******
vt/t
I 4
8
12
16
20
24
B x
+
0
I
I
4
8
12 Hours
evacuation
1 28
, 32
sangle observatwxx. Brett (1971, fag. 3)
from
6
I
I
/
I
16
20
24
28
32
of food
deprivation
(t)
Fig. 2. Abscissa: hours of food deprivation. Ordinate: observed voluntary food intake and gastric evacuation (Dt) and predicted voluntary food intake (V,) after a maximum meal (A,,) at time zero. A - brown trout (Salmo frutta); A,, and V, = mg dry weight of food eaten/l5 min, D, = mg dry weight (Elliott, 1972; 1975 b). B - sockeye salmon (Oncorhynchus nerka); A,, V, and D, = % of dry body weight (Brett and Higgs, 1970; Brett, 1971).
the voluntary food intake increased in a sigmoid pattern with increasing deprivation time, reaching a plateau after 25-30 h and the greatest increase in appetite occurred between 7 and 11 h of food deprivation (Fig. 2B). Brett’s (1971) data of stomach capacity (A,) is somewhat variable. It appears, however, that A0 for a 51 g sockeye is about 4.6% on a dry food/dry fish basis. The gastric evacuation rate (iz) of this size of fish at 15°C is 0.2038 (Brett and Higgs, 1970) and a = 3.4 h. Using these data in Eqn. 7 gives a good fit
227
to the observed data on the development of voluntary food intake with increasing deprivation time (Fig. 2B). Several workers (e.g., Bajkov, 1935; Darnell and Meierotto, 1962; Windell, 1966) have suggested #at once the rate of gastric evacuation is known, the daily food consumption may be calculated. The underlying assumption is usually unrealistic, i.e. the fish is assumed to feed continuously. The literature on stomach content in fishes is replete with records on observed ‘mass’ measured by various methods. There are, however, relatively few studies made on stomach capacity. Ivlev (1961) and Beukema (1968) found that maximal rations differed widely, depending upon species, size, diets, and food concentration. Probably the two extremes are represented by suspension feeders (sensu J$rgensen, 1966) with an almost continuous food uptake and by sit-and-wait predators (sensu Schoener, 1971) examples of which are the anolis lizard (Schoener, 1971), the polychaete GZyceru ah (Ockelmann and Vahl, 1970), and fishes like largemouth bass (Sterba, 1973), pike and anglerfish, and certain bathypelagic fishes, e.g., Malacosteus spp. (Hanstr$m and Johnels, 1965). Since brown trout (Elliott, 1975 b) and sockeye salmon (Brett, 1971) need some time to reach satiety, even when superfluous food is present, they do not fall into any of these clearly defined groups, but take an intermediary position. Eqn. 7 overestimates the voluntary food intake per unit time of these species (Fig. 2A, B) since an underlying assumption in the equation is that hunger is satisfied immediately. In salmonids this is not the case. This overestimation is compensated for by disregarding the time-lag between gastric evacuation and absorption. The extent of the compensation depends mainly on the time taken to reach satiety, which in turn depends on the size and spatial distribution of the food particles. Another uncertainty in the model is the time, a, for L, to reach maximum. The model presupposes that a is independent of ration size. At present this is not known with certainty. Beamish (1974) found an increase with ration size, but the increase was probably not significant. On the other hand Muir and Niimi (1972) and Vahl and Davenport (1979) found no difference, and Beamish (1972) found that in largemouth bass (Micropterus salmonides) both dry weight and nitrogen content of the contents of the intestine and pyloric caeca reached a maximum at the same time after ingestion irrespective of the size of the meal. According to Eqn. 1 maximum growth will occur when the rate of food intake is maximum and the total metabolism is minimum. The total metabolism has three components: the ‘standard’ and the ‘active’ metabolism and the SDA. The standard metabolism is independent of food intake, whereas feeding increases the active metabolism because of handling and foraging. The handling and foraging costs are probably insignificant in an aquaculture system (Kerr, 1971) and can be disregarded for practical purposes. The loss through SDA is probably a constant fraction of the energy intake (Kerr, 1971)
228
and, therefore, this loss may also be disregarded in maximizing food uptake in an aquaculture system. .Therefore, to achieve maximum growth, only food uptake needs to be maximized. The maximum rate of food uptake occurs when V,/t (food uptake per unit time) is maximum (Fig. ZA, B). It appears that in brown trout this maximum is about 7 h of food deprivation, and the voluntary food intake at this time is 64,6% of maximum food eaten/l5 min. A maximum meal is 545 mg (Elliott, 1975 b) and a maximum food consumption per day is (545 X 64.6/100) X (24/7) = 1208 mg. According to Elliott (1975 a, his equation 4), the maximum empirical food intake per day is 1244 mg, which results in a 2.9% error. In sockeye salmon feeding to satiety every 11 h gave a daily food intake of 6.52% on a dry food/dry fish basis (Brett, 1971). This was not an ‘optimum’ feeding regime as the size of two successive meals was inversely correlated (P < 0.01). A relatively large meal was usually followed by a relatively small and vice versa. Brett (1971) realized this and suggested a restricted ration of 3% feed at 11 h intervals would be optimal. This would give a daily food intake of 6.55%. The maximum rate of food uptake (V,/t) will, however, occur when a 2.88% meal is fed on a 9.5 h schedule. This would give a daily food intake of 7.28% which is slightly higher than the 6.55% suggested by Brett (1971). ACKNOWLEDGEMENTS
I would like to thank Professor T. Backiel for the discussions and helpful critique which contributed to the clarifying of concepts, and Professor J. Raa, and Drs. A. Sutterlin and D. Grove for their critical reading of the manuscript.
REFERENCES Andrews, J.M. and Page, J.W., 1915. The effects of frequency of feeding on culture of catfish. Trans. Am. Fish. Sot., 104: 317-321. Averett, R.C., 1969. Influence of Temperature and Material Utilization by Juvenile Coho Salmon. Ph.D. Thesis, Oregon State University, Corvahis, Ore., 74 pp. Bajkov, AD., 1935. How to estimate the daily food consumption of fish under natural conditions. Trans. Am. Fish. Sot., 65: 288-289. Beamish, F.W.H., 1972. Ration size and digestion in largemouth bass, Micropterus salmonides Lacepde. Can. J. Zool., 50: 153-164. Beamish, F.W.H., 1974. Apparent specific dynamic action of food in largemouth bass, Micropterus salmonides. J. Fish. Res. Board Can., 31: 1763-1769. Beukema, J.J., 1968. Predation by the three-spined stickleback (Gasterosteus aculeatus L.). The influence of hunger and experience. Behaviour, 31: l-126. Brett, J.R., 1971. Satiation time, appetite, and maximum food intake of sockeye salmon (Oncorhynchus nerka). J. Fish. Res. Board Can., 28: 409-415. Brett, J.R. and Higgs, D.A., 1970. Effect of temperature on the rate of gastric digestion in fingerling sockeye salmon, Oncorhynchus nerka. J. Fish. Res. Board Can., 27: 17671779. Brett, J.R. and Sutherland, D.B., 1970. Improvement in the artificial rearing of sockeye salmon by environmental control. Fish. Res. Board Can. Gen. Ser. Circ., 89: 14 pp.
229
Brett, J.R., Shelbourn, J.E. and Shoop, C.T., 1969. Growth rate and body composition of fingerling Sockeye salmon, Oncorhynchus nerka, in relation to temperature and ration size. J. Fish. Res. Board Can., 26: 2363-2394. Buttery, P.J. and Annison, E.F., 1973. Considerations of the efficiency of amino acid and protein metabolism in animals. In: J.G.W. Jones (Editor), The Biological Efficiency of Protein Production. Cambridge University Press, London, pp. 141-171. Darnell, R.M. and Meierotto, R.R., 1962. Determination of feeding chronology in fishes. Trans. Am. Fish. Sot., 9: 313-320. Elliott, J.M., 1972. Rates of gastric evacuation in brown trout, Salmo trutta L. Freshwater Biol., 2: l-18. Elliott, J.M., 1975 a. Number of meals in a day, maximum weight of food consumed in a day and maximum rate of feeding for brown trout, Salmo trutta L. Freshwater Biol., 5: 287-303. Elliott, J.M., 1975 b. Weight of food and time required to satiate brown trout, Salmo trutta L. Freshwater Biol., 5: 51-64. Hanstrdm, B. and Johnels, A.G., 1965. Fiskar 2. Benfiskar. In: B. Hanstrom (Editor), Djurens Varld, vol. 2. Forlagshuset Norden AB, Malmo, pp. 125-128. Hightower, N.C. Jr. and Janowitz, H.D., 1973. Digestion. In: J.R. Brobeck (Editor), Physiological Basis of Medical Practice. The Williams and Wilkins Company, Baltimore, Md., pp. 2-1-2-128. Ivlev, V.S., 1961. Experimental Ecology of the Feeding of Fishes. Yale Univ. Press, New Haven, Conn, 302 pp. Jorgensen, C.B., 1966. Biology of Suspension Feeding. Pergamon Press, London, 357 pp. Kennedy, G.C., 1953. The role of depot fat in the hypothalamic control of food intake in the rat. Proc. R. Sot. London, B, 140: 578-592. Kerr, S.R., 1971. Analysis of laboratory experiments on growth efficiency of fishes. J. Fish. Res. Board Can., 28: 801-808. Kleiber, M., 1961. The Fire of Life. John Wiley and Sons Inc., New York, N.Y., 454 pp. Kono, H. and Nose, Y., 1971. Relationship between the amount of food taken and growth in fishes - 1. Frequency of feeding for a maximum daily ration. Bull. Jap. Sot. Sci. Fish., 37: 169-174. Mayer, J., 1955. Genetic, traumatic and environmental factors in the etiology of obesity. Physiol. Rev., 33: 472-508. Muir, B.S. and Niimi, A.J., 1972. Oxygen consumption of the euryhaline fish aholehole (Kuhlia sanduicencis) with reference to salinity, swimming, and food consumption. J. Fish. Res. Board. Can., 29: 67-77. Ockelmann, K.W. and Vahl, O., 1970. On the biology of Glycera alba, especially its burrowing and feeding. Ophelia, 8: 275-294. Paintal, A.S., 1954. A study of gastric stretch receptors. Their role in the peripheral mechanism of satiation of hunger and thirst. J. Physiol., 126: 271-285. Palmer, D.D., Robinson, L.A. and Burrows, R.E., 1951. Feeding frequency: its role in the rearing of blueback salmon fingerlings in troughs. Prog. Fish Cult., 13: 205-212. Paloheimo, J.E. and Dickie, J.E., 1965. Food and growth of fishes. I. A growth curve derived from experimental data. J. Fish. Res. Board Can., 22: 521-542. Schoener, T.W., 1971. Theory of feeding strategies. Ann. Rev. Ecol. Syst., 2: 369-404. Sterba, Gj., 1973. Freshwater Fishes of the World. Studio Vista Ltd., London, 877 pp. Vahl, 0. and Davenport, J., 1979. Apparent specific dynamic action of food in the blenny (Blennins pholis L.). Mar. Ecol. Progr. Ser., in press. Warren, C.E. and Doudoroff, P., 1971. Biology and water pollution control. W.B. Saunders, Philadelphia, Pa., 434 pp. Windell, J.T., 1966. Rate of digestion in the bluegill sunfish. Invest. Indiana Lakes Streams, 7: 185-214.
221
AN HYPOTHESIS ON THE CONTROL OF FOOD INTAKE IN FISH
OLA VAHL Institute
of Fisheries,
Uniuersity
of Tromsd,
P.O. Box
790,
9001
Tromsd
(Norway)
(Accepted 6 March 1979)
ABSTRACT Vahl, O., 1979. An hypothesis on the control of food intake in fish. Aquaculture, 221-229.
17:
An hypothesis on the control of voluntary food intake (appetite) in fish is presented. According to the hypothesis, only two parameters are necessary to design a feeding regime which might result in maximum growth of fish in an aquaculture system. The necessary parameters are maximum voluntary food intake in one meal, and evacuation rate of the stomach. This hypothesis is discussed in relation to empirical data.
INTRODUCTION
On the basis of experimental evidence Paloheimo and Dickie (1965) found that Winberg’s ‘basic energy equation’ adequately predicts growth in fish. The equation is AW --=R_T At
(I)
where the velocity of growth (5:) equals the rate of food consumption (R) minus the metabolic rate (T) expressed in equivalent energy terms. Both R and T are dependent upon a variety of biotic and abiotic factors (Ivlev, 1961; Brett et al., 1969; Brett and Sutherland, 1970). Given a set of abiotic factors, however, the daily rate at which food can be consumed is a prime factor, In the poultry, swine, and cattle industries such husbandry techniques as the use of ad Zibitum or increased feeding frequencies have been employed to increase feed consumption and growth, and to reduce production times. Although aquaculturists have used frequent feeding techniques for many years, few studies have been reported on the effects of frequency of feeding on the growth of fish (Palmer et al., 1951; Kono and Nose, 1971; Andrews and Page, 1975). A carefully designed feeding regime must depend on a knowledge of the control of food intake. The purpose of the present paper is to present an hypothesis for this control and a simple model based on the hypothesis.
222
CONTROL
OF FOOD INTAKE
The control of food intake in the central nervous system is relatively well known. It appears that the hypothalamus contains centers for feeding and satiety and that the satiety center acts by inhibiting the feeding center (Hightower and Janowitz, 1973). In spite of extensive study, the peripheral mechanisms controlling food intake are poorly known (Hightower and Janowitz, 1973). Intake of food, however, induces satiety and stimulates the mechanisms that are inhibitory to the feeding reflexes. Starvation, on the other hand, induces hunger and stimulates the feeding centers. Gastrointestinal and metabolic mechanisms are recognized as possible operating devices. The most important gastrointestinal mechanism is undoubtedly the stretch receptors in the stomach wall (Paintal, 1954). Severance of their connection to the central nervous system induces a hyperphagous condition comparable to that caused by lesion of the satiety center (Hightower and Janowitz, 1973). The effect of these stretch receptors is therefore to give information on available space in the stomach for a new meal. This available space corresponds to Ivlev’s (1961) concept of hunger. However, there is a delay between the development of voluntary food intake and gastric evacuation (emptiness of the stomach) (Brett, 1971; Elliott, 1975 a). Therefore, these stimuli are not the only agents in regulating the food intake. Presumably, metabolic factors are responsible for the delay in the development of hunger. Mayer (1955) has suggested that food intake is controlled in some way through the metabolism of glucose and Kennedy (1953) has put forward the theory that the total energy stores of the body are maintained at a certain predetermined level through the action of receptors monitoring the total level of metabolites in the blood. Whatever the mechanism may be, it is highly probable that metabolic factors play an important role in regulating the food intake. THE MODEL
The consumption of a meal gives rise to an increase in heat production and hence the oxygen consumption of an animal (Kleiber, 1961). This increase in metabolic rate is known as the specific dynamic action (SDA) of the food consumed. In fish, the SDA increases abruptly after feeding reaches a maximum and thereafter decreases more or less regularly to pre-feeding level (Averett, 1969; Muir and Niimi, 1972; Beamish, 1974; Vahl and Davenport, 1979). The biochemistry of SDA is incompletely understood, but the energy liberated is generally assumed to be largely due to the deamination of amino acids. The seemingly simple change in metabolic rate, which appears to be caused by processes in the liver (Buttery and Annison, 1973), is only the final result of many changes in the intermediary metabolism. If the rate of ingestion of amino acids is greater than their rate of utilization in protein synthesis,
223
excess amino acids must be deaminated, permitting biological oxidation or storage of the remaining carbon skeletons and excretion of the amino moieties. Accumulation of free amino acids or their amino fractions can create a condition toxic to the animal (Warren and Doudoroff, 1971). Therefore, it is reasonable to assume that the blood has a maximum carrying capacity for these substances and that their level might be an agent in controlling food intake. Accepting this hypothesis, the level of SDA reflects the degree of negative feed-back from the metabolites in the blood. Accordingly, a simplified flow diagram showing the fate of the ingested materials and the control of appetite can be put forward (Fig. 1).
Stomach
intestine
time-lag
*
Flow of materials
+
Flow of Information
Lwer
Blood
Receptors monltorlng the level of metabolltes in blood
Fig. 1. The basis for the hypothesis. Simplified diagram showing the flow of ingested materials and assumed flow of information and control of voluntary food intake (appetite).
After ingestion of a meal, the fullness of the stomach is monitored by the stretch receptors in the stomach. The fullness at any time is dependent on the evacuation rate, which in turn is proportional to the mass of food remaining in the stomach (Brett and Higgs, 1970). This can be expressed by the relation (Elliott, 1972) M, = Aoeekf
(2)
where M, is the amount in the stomach at time t, when A0 is a maximum meal ingested at time zero, and h is the instantaneous rate of gastric evacuation. Therefore the amount of A0 evacuated from the stomach, D,, at time t is D, = Ao(l - e-“f)
(3)
which is the information conveyed to higher centers by the stretch receptors. Thus the satiety center in the hypothalamus receives information about the free volume available in the stomach.
224
When the food is absorbed and processed further it will give rise to a higher level of metabolites in the blood. The level will be determined by the size and composition of the meal and by the time elapsed after ingestion. Since the SDA reaches a maximum some time after ingestion (Averett, 1969; Muir and Niimi, 1972; Beamish, 1974; Vahl and Davenport, 1979) there is a time-lag between the ingestion and the contribution of the meal to the level of metabolites. The extent of the time lag depends on the rates of stomach evacuation, absorption, and processing of the absorbed materials. The level of metabolites from the absorbed materials obviously cannot go below zero, and the simplest assumption regarding the processing rate is that it is always a constant fraction of the amount absorbed. The simplest expression satisfying these assumptions is the one describing a first order reaction. Accordingly, the simplest expression giving the level of metabolites from the absorbed materials at time t is L, a Dte-mt
= Ao(l - &t)e-mt
(4)
where L, is the level of metabolites from the absorbed materials at time t and m is the instantaneous rate of processing. For simplicity, the time-lag between evacuation of the stomach and absbrption is disregarded, as is the fact that not all ingested material is absorbed. This does not, however, affect the general conclusions. As the duration of SDA seems to be approximately equal to the time needed for absorption (Beamish, 1974), the instantaneous processing rate of absorbed materials cannot differ much from the rate of absorption, and under the assumptions made in Eqn. 4, from evacuation rate. Therefore, only a small error is made in assuming m = k. Eqn. 4 may then be written L, = A,,(1 - e-ht)ePkt
(5)
Eqn. 5 gives a curve which increases from zero to reach a maximum, whereafter it decreases. The time, a, to reach maximum is the time when.2 = 0 and depends on the value of k, but is independent of the size of the meal. The curve apparently belongs to the same family of curves as those assumed by Muir and Niimi (1972, their fig. 6) and shown by Vahl and Davenport (1979, their fig. l), describing the progress of SDA after ingesting a meal, and presumably the degree of negative feedback from the metabolites in the blood. The time, a, is therefore the time-lag from ingesting a meal till it has its largest effect on food uptake. If, in fact, there is a maximum level, L,, of metabolites in the blood which the animal can tolerate (Warren and Doudoroff, 1971), this will occur at the time a after ingesting a maximum meal. As all meals prior to time t contribute to the existing level, a new meal at time t must not be so large as to cause the level of metabolites to exceed the maximum level (L,) at time t + a. Accordingly, the carrying capacity as a fraction of L, for metabolites in the blood available for a new meal at time t is
225
The largest meal a fish can tolerate at time t is thus dependent on the available space in the stomach, D,, and the carrying capacity for metabolites available at time t + a. If hunger is defined as the largest meal tolerated, and the fish will eat to satisfy its hunger completely, the maximum voluntary food intake at the time t, V,, after ingesting a maximum meal is
Eqn. 6 disregards differences in the quality (e.g. moisture and protein contents) of the meals, and foraging and handling times. In an aquaculture system, food quality is assumed to be constant, and foraging and handling times are probably negligible (Kerr, 1971). Inherent in Eqn. 5 is the premise that L, = Ao/4. Substituting D, from Eqn. 3 and L, and Lt+a from Eqn. 5 in Eqn. 6 gives V, * Ao(l
- echt) (1-
Ao(l - e-h(t+al)e-b(t+al - -.0A
1
4 = Ao(l - c-ht) (1 - 2e-~(f+Q))2
(7)
Eqn. 7 shows that maximum voluntary food intake increases in a sigmoid pattern with time and approaches a plateau which corresponds to the maximum food intake in a single meal, Ao. DISCUSSION
Elliott (1975 a) studied the daily food consumption of brown trout and also measured the voluntary food intake in a group of fish (Fig. 2A). After being fed to satiation the voluntary food intake (and presumably hunger) per unit time of 90 g fish at 15°C increased in a sigmoid pattern with increasing deprivation time and approached a plateau after about 12-15 h. The greatest increase in food intake occurred between 7.5 and 10 h. The gastric evacuation rate (=h) of 90 g fish at 15°C is 0.284 (Elliott, 1972) and a = 2.5 h. The satiation time for a 90 g trout is 53 min (Elliott, 1975 b) but, assuming the maximum voluntary food intake in 15 min (A,) to be 160 mg (Elliott, 1975 a, his fig. 4), Vt can be calculated. It appears that Eqn. 7 predicts the development of voluntary food intake in brown trout fairly well. The plateau is reached after about 15 h, but the greatest increase according to the present model occurs after about 7 h, whereas the observed voluntary food intake increases at the highest rate from 8 to 10 h (Fig. 2A). Brett (1971) measured stomach capacity and voluntary food intake in sockeye salmon. His data show the same general pattern as Elliott’s. At 15°C
226
range. from (1975 b. fig.41
mean and Elliott
t 160
-
Vt = predicted voluntary hod Intake -
Of = gastric
******
vt/t
I 4
8
12
16
20
24
B x
+
0
I
I
4
8
12 Hours
evacuation
1 28
, 32
sangle observatwxx. Brett (1971, fag. 3)
from
6
I
I
/
I
16
20
24
28
32
of food
deprivation
(t)
Fig. 2. Abscissa: hours of food deprivation. Ordinate: observed voluntary food intake and gastric evacuation (Dt) and predicted voluntary food intake (V,) after a maximum meal (A,,) at time zero. A - brown trout (Salmo frutta); A,, and V, = mg dry weight of food eaten/l5 min, D, = mg dry weight (Elliott, 1972; 1975 b). B - sockeye salmon (Oncorhynchus nerka); A,, V, and D, = % of dry body weight (Brett and Higgs, 1970; Brett, 1971).
the voluntary food intake increased in a sigmoid pattern with increasing deprivation time, reaching a plateau after 25-30 h and the greatest increase in appetite occurred between 7 and 11 h of food deprivation (Fig. 2B). Brett’s (1971) data of stomach capacity (A,) is somewhat variable. It appears, however, that A0 for a 51 g sockeye is about 4.6% on a dry food/dry fish basis. The gastric evacuation rate (iz) of this size of fish at 15°C is 0.2038 (Brett and Higgs, 1970) and a = 3.4 h. Using these data in Eqn. 7 gives a good fit
227
to the observed data on the development of voluntary food intake with increasing deprivation time (Fig. 2B). Several workers (e.g., Bajkov, 1935; Darnell and Meierotto, 1962; Windell, 1966) have suggested #at once the rate of gastric evacuation is known, the daily food consumption may be calculated. The underlying assumption is usually unrealistic, i.e. the fish is assumed to feed continuously. The literature on stomach content in fishes is replete with records on observed ‘mass’ measured by various methods. There are, however, relatively few studies made on stomach capacity. Ivlev (1961) and Beukema (1968) found that maximal rations differed widely, depending upon species, size, diets, and food concentration. Probably the two extremes are represented by suspension feeders (sensu J$rgensen, 1966) with an almost continuous food uptake and by sit-and-wait predators (sensu Schoener, 1971) examples of which are the anolis lizard (Schoener, 1971), the polychaete GZyceru ah (Ockelmann and Vahl, 1970), and fishes like largemouth bass (Sterba, 1973), pike and anglerfish, and certain bathypelagic fishes, e.g., Malacosteus spp. (Hanstr$m and Johnels, 1965). Since brown trout (Elliott, 1975 b) and sockeye salmon (Brett, 1971) need some time to reach satiety, even when superfluous food is present, they do not fall into any of these clearly defined groups, but take an intermediary position. Eqn. 7 overestimates the voluntary food intake per unit time of these species (Fig. 2A, B) since an underlying assumption in the equation is that hunger is satisfied immediately. In salmonids this is not the case. This overestimation is compensated for by disregarding the time-lag between gastric evacuation and absorption. The extent of the compensation depends mainly on the time taken to reach satiety, which in turn depends on the size and spatial distribution of the food particles. Another uncertainty in the model is the time, a, for L, to reach maximum. The model presupposes that a is independent of ration size. At present this is not known with certainty. Beamish (1974) found an increase with ration size, but the increase was probably not significant. On the other hand Muir and Niimi (1972) and Vahl and Davenport (1979) found no difference, and Beamish (1972) found that in largemouth bass (Micropterus salmonides) both dry weight and nitrogen content of the contents of the intestine and pyloric caeca reached a maximum at the same time after ingestion irrespective of the size of the meal. According to Eqn. 1 maximum growth will occur when the rate of food intake is maximum and the total metabolism is minimum. The total metabolism has three components: the ‘standard’ and the ‘active’ metabolism and the SDA. The standard metabolism is independent of food intake, whereas feeding increases the active metabolism because of handling and foraging. The handling and foraging costs are probably insignificant in an aquaculture system (Kerr, 1971) and can be disregarded for practical purposes. The loss through SDA is probably a constant fraction of the energy intake (Kerr, 1971)
228
and, therefore, this loss may also be disregarded in maximizing food uptake in an aquaculture system. .Therefore, to achieve maximum growth, only food uptake needs to be maximized. The maximum rate of food uptake occurs when V,/t (food uptake per unit time) is maximum (Fig. ZA, B). It appears that in brown trout this maximum is about 7 h of food deprivation, and the voluntary food intake at this time is 64,6% of maximum food eaten/l5 min. A maximum meal is 545 mg (Elliott, 1975 b) and a maximum food consumption per day is (545 X 64.6/100) X (24/7) = 1208 mg. According to Elliott (1975 a, his equation 4), the maximum empirical food intake per day is 1244 mg, which results in a 2.9% error. In sockeye salmon feeding to satiety every 11 h gave a daily food intake of 6.52% on a dry food/dry fish basis (Brett, 1971). This was not an ‘optimum’ feeding regime as the size of two successive meals was inversely correlated (P < 0.01). A relatively large meal was usually followed by a relatively small and vice versa. Brett (1971) realized this and suggested a restricted ration of 3% feed at 11 h intervals would be optimal. This would give a daily food intake of 6.55%. The maximum rate of food uptake (V,/t) will, however, occur when a 2.88% meal is fed on a 9.5 h schedule. This would give a daily food intake of 7.28% which is slightly higher than the 6.55% suggested by Brett (1971). ACKNOWLEDGEMENTS
I would like to thank Professor T. Backiel for the discussions and helpful critique which contributed to the clarifying of concepts, and Professor J. Raa, and Drs. A. Sutterlin and D. Grove for their critical reading of the manuscript.
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Brett, J.R., Shelbourn, J.E. and Shoop, C.T., 1969. Growth rate and body composition of fingerling Sockeye salmon, Oncorhynchus nerka, in relation to temperature and ration size. J. Fish. Res. Board Can., 26: 2363-2394. Buttery, P.J. and Annison, E.F., 1973. Considerations of the efficiency of amino acid and protein metabolism in animals. In: J.G.W. Jones (Editor), The Biological Efficiency of Protein Production. Cambridge University Press, London, pp. 141-171. Darnell, R.M. and Meierotto, R.R., 1962. Determination of feeding chronology in fishes. Trans. Am. Fish. Sot., 9: 313-320. Elliott, J.M., 1972. Rates of gastric evacuation in brown trout, Salmo trutta L. Freshwater Biol., 2: l-18. Elliott, J.M., 1975 a. Number of meals in a day, maximum weight of food consumed in a day and maximum rate of feeding for brown trout, Salmo trutta L. Freshwater Biol., 5: 287-303. Elliott, J.M., 1975 b. Weight of food and time required to satiate brown trout, Salmo trutta L. Freshwater Biol., 5: 51-64. Hanstrdm, B. and Johnels, A.G., 1965. Fiskar 2. Benfiskar. In: B. Hanstrom (Editor), Djurens Varld, vol. 2. Forlagshuset Norden AB, Malmo, pp. 125-128. Hightower, N.C. Jr. and Janowitz, H.D., 1973. Digestion. In: J.R. Brobeck (Editor), Physiological Basis of Medical Practice. The Williams and Wilkins Company, Baltimore, Md., pp. 2-1-2-128. Ivlev, V.S., 1961. Experimental Ecology of the Feeding of Fishes. Yale Univ. Press, New Haven, Conn, 302 pp. Jorgensen, C.B., 1966. Biology of Suspension Feeding. Pergamon Press, London, 357 pp. Kennedy, G.C., 1953. The role of depot fat in the hypothalamic control of food intake in the rat. Proc. R. Sot. London, B, 140: 578-592. Kerr, S.R., 1971. Analysis of laboratory experiments on growth efficiency of fishes. J. Fish. Res. Board Can., 28: 801-808. Kleiber, M., 1961. The Fire of Life. John Wiley and Sons Inc., New York, N.Y., 454 pp. Kono, H. and Nose, Y., 1971. Relationship between the amount of food taken and growth in fishes - 1. Frequency of feeding for a maximum daily ration. Bull. Jap. Sot. Sci. Fish., 37: 169-174. Mayer, J., 1955. Genetic, traumatic and environmental factors in the etiology of obesity. Physiol. Rev., 33: 472-508. Muir, B.S. and Niimi, A.J., 1972. Oxygen consumption of the euryhaline fish aholehole (Kuhlia sanduicencis) with reference to salinity, swimming, and food consumption. J. Fish. Res. Board. Can., 29: 67-77. Ockelmann, K.W. and Vahl, O., 1970. On the biology of Glycera alba, especially its burrowing and feeding. Ophelia, 8: 275-294. Paintal, A.S., 1954. A study of gastric stretch receptors. Their role in the peripheral mechanism of satiation of hunger and thirst. J. Physiol., 126: 271-285. Palmer, D.D., Robinson, L.A. and Burrows, R.E., 1951. Feeding frequency: its role in the rearing of blueback salmon fingerlings in troughs. Prog. Fish Cult., 13: 205-212. Paloheimo, J.E. and Dickie, J.E., 1965. Food and growth of fishes. I. A growth curve derived from experimental data. J. Fish. Res. Board Can., 22: 521-542. Schoener, T.W., 1971. Theory of feeding strategies. Ann. Rev. Ecol. Syst., 2: 369-404. Sterba, Gj., 1973. Freshwater Fishes of the World. Studio Vista Ltd., London, 877 pp. Vahl, 0. and Davenport, J., 1979. Apparent specific dynamic action of food in the blenny (Blennins pholis L.). Mar. Ecol. Progr. Ser., in press. Warren, C.E. and Doudoroff, P., 1971. Biology and water pollution control. W.B. Saunders, Philadelphia, Pa., 434 pp. Windell, J.T., 1966. Rate of digestion in the bluegill sunfish. Invest. Indiana Lakes Streams, 7: 185-214.