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A cost-benefit analysis of nocturnal feeding in the rat
Physiology & Behavior, Vol. 31, pp. 555-559. PergamonPress Ltd., 1983. Printedin the U.S.A.
A Cost-Benefit Analysis of Nocturnal Feeding in the Rat I G E O R G I A B. J E N S E N , 2 G E O R G E H. C O L L I E R a A N D M A N D Y B. M E D V I N 4
R u t g e r s U n i v e r s i t y , N e w B r u n s w i c k , N J 08903 R e c e i v e d 24 J a n u a r y 1983 JENSEN, G. B., G. H. COLLIER AND M. B. MEDVIN. A cost-benefit analysis of nocturnal feeding in the rat. PHYSIOL BEHAV 31(4)555-559, 1983.--Rats are nocturnal feeders. The present results show that when either the cost of procuring a meal or the cost of consuming it increases differentially in the dark relative to the light, rats shift their feeding activity to the light phase of the light/dark cycle. These results suggest that some of the same factors that presumably provided the selection pressure for nocturnal feeding in the phylogeny of the rat are still capable of modifying its current patterns of feeding. Cost-benefit
Meal patterns
Nocturnal feeding
MOST species of animals distribute their biologically significant activities differentially in the phases of the light/dark (L/D) cycle. Their activity patterns, together with various associated morphological specializations, are regarded as adaptations to different ecological niches, selected over the phylogenetic history of the species [1, 3, 9]. Rattus norvegicus, for example, confines most of its activities to the dark phase and relies on highly developed olfactory and auditory senses (for review, see [1] pp. 28-29, [15]). Like many generalists, however, it is capable of modifying its species-typical patterns of activities when low-cost and/or beneficial resources become available at other times within the 24-hr period [4, 5, 16]. For example, when foods of greater palatability are available only in the day, the rat will feed diurnally [14]. The present study was designed to explore the plasticity of this facet of the rat's behavior. Freely feeding laboratory rats eat approximately 10-15 meals per day of 1-3 g each when a standard lab chow and standard-sized cages are used. A recent series of studies has shown that when the cost of foraging (gaining access to food) is increased, freely feeding rats decrease the number of meals they initiate but increase the size of those they take. In this way, they minimize the cost of procuring food while, at the same time, defending their total intake. On the other hand, when the cost of consumption (cost per "bite" or portion within a meal) is increased, the rats increase their rate of eating, defending the time spent feeding (cf., [8]). In the present study, we explored the rats' solutions to the problem of an increasing cost of nocturnal feeding. In two experiments we sought to assess the separate contributions of foraging costs (Experiment 1) and consumption costs
Light/dark cycle
(Experiment 2) to the pattern of feeding (see also [13]). In each experiment we varied one of the costs in each phase of the L/D cycle while holding the other cost constant and measured the resulting changes in the parameters of mealtaking. EXPERIMENT 1 In this experiment, the fixed ratio (FR) bar press requirement for gaining access to food (the foraging or procurement cost) was varied [13]. In the first part of the experiment, the procurement cost was progressively increased in the dark phase but was held constant in the light phase. In the second part, the procurement cost was increased during the light phase only and was held constant in the dark phase. In both parts, however, consumption cost (the FR per pellet once a meal had been procured) remained constant in each phase of the L/D cycle. METHOD
Animals Four male albino rats (Sprague-Dawley, Charles River, North Wilmington, MA), 60-90 days old at the outset, were used. Rats 1 and 2 were control animals and Rats 3 and 4 were the experimental animals.
Apparatus The animals were housed individually in standard wire cages (Hoeltge, Cincinnati, OH). Mounted at the rear of each experimental cage was a T-shaped bar (BCS, Inc., South
~Portions of these data were presented by the third author at the meeting of the Eastern Psychological Association, Washington, D.C., March 1978. This research was supported in part by Grant No. HD 10588 from the National Institute of Health to George Collier. 2Now at the Department of Psychology, St. Louis University, St. Louis, MO 63103. 3Requests for reprints should be addressed to George Collier, Department of Psychology (Busch Campus), Rutgers University, New Brunswick, NJ 08903. 4Now at the Department of Psychology, University of Washington, Seattle, WA 98195.
Copyright © 1983 Pergamon Press Ltd.--0031-9384/83/100555-05503.00
55~
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Plainfield, N J) that required an operating tbrce of 0.35 N through a 2-cm excursion. A food magazine (Davis Scientific Instruments, Studio City, CA) dispensed 45-mg pellets (l,ab rat pellets, Diet A: Noyes, Lancaster, NH) into a food cup located on the cage floor immediately adjacent to the bar. A dim 6-W cue light, capped with a white lens, was mounted in the Plexiglas ceiling directly over the food cup in the experimental cages and over the tunnel feeder in the control cages. The cue light in each control cage was yoked to that of a corresponding experimental cage such that it was lit only when and for as long as the light in the paired experimental cage was lit. All animals were maintained on a 12:12 L/D cycle, with light onset at 0845 hr. The room temperature was stabilized at 23°C and humidity, at 50c~.
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Pro('edure All animals lived in the apparatus continuously, with the two experimental animals obtaining all food by completing the specified bar press requirements. Completion of the initial FR, the procurement ratio, illuminated the cue light and turned on the pellet dispenser. Each completion of a second FR requirement (the consumption ratio) while the cue light was on resulted in the delivery o f a 45-mg pellet into the food cup. The cue light remained on (and the consumption ratio remained in effect) until 10 consecutive minutes had elapsed without a bar press. At this time the cue light and the pellet dispenser were turned off, and completion of the original procurement ratio was again required in order to turn on the cue light that signalled access to the consumption contingency. Initially following magazine training, both ratio costs in both phases of the L/D cycle were fixed at FR 40. In Procedure 1, the procurement cost in the dark phase was increased stepwise every 6--8 days: FR 80, 160, 320, 640, 1280, and 2560. The criterion for changing this FR was four days of stable behavior with respect to the number of meals obtained daily. After FR 2560, a descending series of procurement ratios was in effect. The procurement cost in the light phase and the consumption cost in both phases remained fixed at FR 40 throughout this procedure. In Procedure 2, after one week with procurement and consumption costs in both L/D phases fixed at FR 40, the experimental animals were placed on an ascending series of procurement costs in the light phase: FR 80, 160, 640. Procurement cost in the dark phase and consumption cost in both phases were fixed at FR 40. As before, each ratio was in effect for 6--8 days. Animals had ad lib access to water. Body weight, food intake, and water intake were recorded daily at light onset. The data presented below are derived from the last four days of each schedule condition. Initiation of a meal was defined by the acquisition of three food pellets, and meals were considered to have terminated when no bar-pressing occurred for 10 consecutive minutes following the last pellet delivery. Records of bar pressing, pellet delivery, and the temporal sequence of meal patterns were obtained on cumulative recorders (Gerbrands, Arlington, MA). RESULTS
As the nocturnal cost of gaining access to the feeder increased, the frequency of initiating meals in the dark decreased monotonically for both experimental animals (see Fig. 1). Meal size (g/meal) of Rat 3 in the dark increased as a function of procurement cost to FR 640 and then decreased
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to zero by FR 2560 (see Fig. 2). The values of these factors (meal frequency, meal size) combined to yield a lower total intake in the dark at procurement costs greater than FR 640 (see Fig. 3). Rat 4 increased meal size at the higher costs, taking only a single large meal in the dark at FR 2560 (see Fig. 2); again, the combined result was a decrease in total intake in the dark at procurement costs greater than FR 640 (see Fig. 3). The reduction in total intake in the dark, when procurement costs were high, was compensated for in each instance by a simultaneous increase in both the frequency and size of meals taken in the light. Although the total number of meals taken in a 24-hr period decreased, total intakes remained relatively constant. The data points obtained during the ascending series were recovered when a descending series of FR procurement costs was imposed during the dark phase. Procurement barpress rates were variable and did not differ significantly either between light/dark phases or across ratios for a given animal, averaging approximately 60-70/min for the first and 40-50/min for the second. For one rat, bar-press rates associated with the FR 40 consumption cost increased from approximately 45/min at the lowest procurement cost to 95/min at the highest (FR 2560); the response rate of the second rat during the consumption component varied from 85-100/min over all procurement costs. Introduction of an ascending series of procurement costs in the light phase caused both animals to reduce the frequency of meals initiated in the light to zero at FR 640. Rat 4 increased the number of meals taken in the dark compensatorily and thus maintained a constant number of meals (and a constant intake) in each 24-hr period. However, Rat 3 did not increase the number of meals initiated in the dark sufficiently to compensate for the reduction in light-phase meals. As a result, his total daily number of meals, and his total daily intake, decreased. RESULTS AND DISCUSSION
It is clear from these results that the relation between procurement cost and the meal frequency-meal size function is not symmetrical over the two phases of the L/D cycle. A
NOCTURNAL FEEDING
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substantially larger procurement cost in the dark is required for the rat to begin feeding exclusively in the light than is required in the light for the rat to begin feeding exclusively in the dark. That is, it is more difficult to reverse the asymmetry that already exists (rats being nocturnal) than it is to exaggerate it. However, it is also clear that the rat is sensitive to the costs of nocturnal feeding. The effect of procurement cost on the meal frequency-meal size relation is situation-dependent: The decline in meal frequency and the accompanying increase in meal size occurred in the dark when the dark procurement cost was increased; at the same time, meal frequency in the light (fixed procurement cost) remained stable while meal size increased. Only when the dark meal frequency fell to zero did the frequency of meals taken in the light also begin to increase. The two control animals (Rats 1 and 2) ate 67% (_+0.7) and 72% (_+2. l) of their meals in the dark, respectively. The initial difference in body weights of the control and experimental animals, a result of the introduction of FR schedules for the experimental rats, persisted until the end of the experiment; however, following their initial loss, experimental animals grew at the same rate as the controls. EXPERIMENT 2 In this experiment, the cost of consuming a meal (i.e., the FR per pellet) in the dark, once access to a meal had been gained, was varied, first in an ascending and then in a descending series. This procedure was completed twice, first with the cost per pellet in the light fixed at FR 1 and, following this, with the cost per pellet in the light fixed at FR 40. METHOD
Animals Subjects were four male albino rats, obtained as before and 90 days old at the start of the study. Rats 1 and 2 were experimental animals and Rats 3 and 4 were control animals.
Apparatus Caging was the same as before, except that a Hoeltge tunnel feeder was mounted on the control animals' cages.
and total intake as a function of the cost (FR) of procuring access to meals in the dark (left panel) and in the light (right panel) when consumption cost was fixed at FR 40.
Two cups were placed beneath the tunnel. One, the " d a y " food cup, was available during the light phase of the L/D cycle. When the lights went out during the dark phase, a motor moved the second cup, the "night" food cup, under the tunnel opening. Thus light and dark food intake levels for the controls could be measured separately.
Procedure The animals were again housed in the apparatus continuously. Initially an FR 1 per pellet schedule was in effect for the experimental animals in both phases of the L/D cycle. An increasing series of consumption costs (FR 5, 10, 20, 40, 80, 160, 320) per pellet was then imposed during the dark phase while the consumption cost per pellet in the light was maintained at FR 1. The increase in dark phase consumption cost continued until an animal's total food intake occurred in the light phase of the L/D cycle. Each consumption ratio (FR) was then replicated by decreasing the FR in the dark in a descending sequence. Finally, an F R 40 consumption cost was instituted in both phases of the L/D cycle. Consumption cost was then increased (FR 80, 160, 320) in the dark phase until the animal's total food intake again occurred in the light phase. This was followed, as before, by a descending series of FRs. For each schedule condition, the FR was in effect for 6-8 days. The cue lights above the food trays and the tunnel feeders were not used in this experiment. RESULTS AND DISCUSSION
Meal frequencies in the dark and in the light were relatively unaffected by changes in consumption cost with two exceptions: Rat 2 showed a decline in meal frequency when consumption cost was first increased from FR 1 to FR 5, and both rats stopped feeding in the dark (zero frequency) at the point at which consumption cost became too high. When light consumption cost was raised to FR 40 (right panel) it
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NOCTURNAL FEEDING
559
competition, and resource availability and abundance, have favored the rat's adoption of a nocturnal niche. These are reflected in the rat's morphology as well as in its speciesspecific behaviors, including the rat's tendency to consume most of its food in the dark. This periodicity in feeding behavior has been the basis of extensive laboratory studies of both circadian rhythms and homeostatic models of the regulation of food intake (for reviews, see [2, 3, 9, 10]). However, these same factors can be shown to be operative in the current life history of this generalist omnivore [1, 4, 11, 12, 14, 17]. The present results provide convergent evidence, showing that when the cost of either foraging or consumption is different in the light and dark phases of the L/D cycle, the rat adjusts its pattern of feeding in the direction of minimizing feeding cost. The contribution of endogenous factors to this pattern of feeding is reflected in the asymmetry of this cost function; that is, the cost differential must be greater in the dark compared to the light to produce a shift in feeding activity to the phase of the L/D cycle in which current costs are minimal. The means by which the shift is accomplished becomes clear in the present results. Confirming previous results [6,8], increases in the cost of foraging in the dark result in a decrease in the frequency of meals in the dark and an in-
crease in the size of meals until the meal frequency in the dark drops to zero. At the same time, meal frequency in the light phase remains constant, but the size of meals taken in the light increases. As a consequence, total 24-hr intake is defended. On the other hand, when consumption costs increase in the dark, meal frequency in both phases of the L/D cycle remains relatively constant over the middle range of costs while meal size decreases in the dark and increases in the light until meal size in the dark declines to zero. Again, however, total intake is defended. At higher combined dark and light consumption costs, total 24-hr intake decreases (see also [8]). As predicted by previous data, response rates increased in the particular phase of the L/D cycle in which consumption costs selectively increased [8]. In summary, the effects of foraging and consumption costs on feeding patterns are similar in those phases of the L/D cycle in which they are varied to those that have been observed when these costs are varied uniformly across the entire L/D cycle. These results add to the growing body of data which suggest that the major determinants of the pattern of intake over 24 hours (that is, the pattern of meals) reside in the economic structure of the environment [6]. Regulation of intake as a result of endogenous factors appears to have a longer time frame than is usually assumed [10].
REFERENCES 1. Armstrong, S. A chronometric approach to the study of feeding behavior. Neurosci Biobehav Rev 4: 27-53, 1980. 2. Aschoff, J. Exogenous and endogenous components in circadian rhythms. Cold Spring Harbor Syrup Quan Biol 25: I 1-28, 1960. 3. Aschoff, J. Survival value of diurnal rhythms. Zool Sot" Lond Syrup 13: 79-98, 1964. 4. Calhoun, J. F. The ecology and sociobiology of the Norway rat. U.S. Dept. of Health, Education & Welfare (PHS Monograph 1008), 1963. 5. Canby, T. Y. The rat: Lapdog of the devil. Nat Geog 152: 60-86. 1977. 6. Collier, G. H. Determinants of choice. In: Nebraska Symposium on Motivation, edited by D. Bernstein. Lincoln: University of Nebraska Press, 1982. 7. Collier, G., E. Hirsch and R. Kanarek. The operant revisited. In: Handbook of Operant Behavior, edited by W. K. Honig and J. E. R. Staddon. New York: Prentice-Hall, 1977. 8. Collier, G. and C. K. Rovee-Collier. A comparative analysis of optimal foraging behavior: Laboratory simulations. In: Foraging Behavior: Ecological, Ethological. and Psychological Approaches, edited by A. C. Kamil and T. D. Sargent. New York: Garland STPM Press, 1980.
9. Enright, J. T. Ecological aspects of endogenous rhythmicity. Ann Rev Ecol Syst 1: 221-238, 1970. 10. Le Magnen, J. The metabolic basis of dual periodicity of feeding in rats. Behav Brain Sci 4: 561-607, 1981. 11. Levin, R. and S. Levine. Ecological determinants of circadian rhythms in rats. Paper presented at the Meeting of the EPA, Philadelphia, April 1974. 12. Levin, R. and J. M. Stern. The ontogeny of nocturnal feeding in the rat. J Comp Physiol Psychol 89:711-721, 1975. 13. Marwine, A. and G. Collier. The rat at the waterhole. J Comp Physiol Psychol 93: 391-402, 1979. 14. Panksepp, J. and K. Krost. Modification of diurnal feeding patterns by palatability. Physiol Behav 15: 673-677, 1975. 15. Richter, C. P. Inborn nature of the rat's 24-hour clock. J Comp Physiol Psychol 75: 1-4, 1971. 16. Rovee-Collier, C. K., B. A. Clapp and G. H. Collier. The economics of food choice in chicks. Physiol Behav 28:1097-1102, 1982. 17. Stern, J. M. and R. Levin. Food availability as a determinant of the rats' circadian rhythm in maternal behavior. Dev Psychobiol 9" 137-148, 1976.
A Cost-Benefit Analysis of Nocturnal Feeding in the Rat I G E O R G I A B. J E N S E N , 2 G E O R G E H. C O L L I E R a A N D M A N D Y B. M E D V I N 4
R u t g e r s U n i v e r s i t y , N e w B r u n s w i c k , N J 08903 R e c e i v e d 24 J a n u a r y 1983 JENSEN, G. B., G. H. COLLIER AND M. B. MEDVIN. A cost-benefit analysis of nocturnal feeding in the rat. PHYSIOL BEHAV 31(4)555-559, 1983.--Rats are nocturnal feeders. The present results show that when either the cost of procuring a meal or the cost of consuming it increases differentially in the dark relative to the light, rats shift their feeding activity to the light phase of the light/dark cycle. These results suggest that some of the same factors that presumably provided the selection pressure for nocturnal feeding in the phylogeny of the rat are still capable of modifying its current patterns of feeding. Cost-benefit
Meal patterns
Nocturnal feeding
MOST species of animals distribute their biologically significant activities differentially in the phases of the light/dark (L/D) cycle. Their activity patterns, together with various associated morphological specializations, are regarded as adaptations to different ecological niches, selected over the phylogenetic history of the species [1, 3, 9]. Rattus norvegicus, for example, confines most of its activities to the dark phase and relies on highly developed olfactory and auditory senses (for review, see [1] pp. 28-29, [15]). Like many generalists, however, it is capable of modifying its species-typical patterns of activities when low-cost and/or beneficial resources become available at other times within the 24-hr period [4, 5, 16]. For example, when foods of greater palatability are available only in the day, the rat will feed diurnally [14]. The present study was designed to explore the plasticity of this facet of the rat's behavior. Freely feeding laboratory rats eat approximately 10-15 meals per day of 1-3 g each when a standard lab chow and standard-sized cages are used. A recent series of studies has shown that when the cost of foraging (gaining access to food) is increased, freely feeding rats decrease the number of meals they initiate but increase the size of those they take. In this way, they minimize the cost of procuring food while, at the same time, defending their total intake. On the other hand, when the cost of consumption (cost per "bite" or portion within a meal) is increased, the rats increase their rate of eating, defending the time spent feeding (cf., [8]). In the present study, we explored the rats' solutions to the problem of an increasing cost of nocturnal feeding. In two experiments we sought to assess the separate contributions of foraging costs (Experiment 1) and consumption costs
Light/dark cycle
(Experiment 2) to the pattern of feeding (see also [13]). In each experiment we varied one of the costs in each phase of the L/D cycle while holding the other cost constant and measured the resulting changes in the parameters of mealtaking. EXPERIMENT 1 In this experiment, the fixed ratio (FR) bar press requirement for gaining access to food (the foraging or procurement cost) was varied [13]. In the first part of the experiment, the procurement cost was progressively increased in the dark phase but was held constant in the light phase. In the second part, the procurement cost was increased during the light phase only and was held constant in the dark phase. In both parts, however, consumption cost (the FR per pellet once a meal had been procured) remained constant in each phase of the L/D cycle. METHOD
Animals Four male albino rats (Sprague-Dawley, Charles River, North Wilmington, MA), 60-90 days old at the outset, were used. Rats 1 and 2 were control animals and Rats 3 and 4 were the experimental animals.
Apparatus The animals were housed individually in standard wire cages (Hoeltge, Cincinnati, OH). Mounted at the rear of each experimental cage was a T-shaped bar (BCS, Inc., South
~Portions of these data were presented by the third author at the meeting of the Eastern Psychological Association, Washington, D.C., March 1978. This research was supported in part by Grant No. HD 10588 from the National Institute of Health to George Collier. 2Now at the Department of Psychology, St. Louis University, St. Louis, MO 63103. 3Requests for reprints should be addressed to George Collier, Department of Psychology (Busch Campus), Rutgers University, New Brunswick, NJ 08903. 4Now at the Department of Psychology, University of Washington, Seattle, WA 98195.
Copyright © 1983 Pergamon Press Ltd.--0031-9384/83/100555-05503.00
55~
I E N S E N , ('OI~I,IER ANI) Mt I)VIN
Plainfield, N J) that required an operating tbrce of 0.35 N through a 2-cm excursion. A food magazine (Davis Scientific Instruments, Studio City, CA) dispensed 45-mg pellets (l,ab rat pellets, Diet A: Noyes, Lancaster, NH) into a food cup located on the cage floor immediately adjacent to the bar. A dim 6-W cue light, capped with a white lens, was mounted in the Plexiglas ceiling directly over the food cup in the experimental cages and over the tunnel feeder in the control cages. The cue light in each control cage was yoked to that of a corresponding experimental cage such that it was lit only when and for as long as the light in the paired experimental cage was lit. All animals were maintained on a 12:12 L/D cycle, with light onset at 0845 hr. The room temperature was stabilized at 23°C and humidity, at 50c~.
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Pro('edure All animals lived in the apparatus continuously, with the two experimental animals obtaining all food by completing the specified bar press requirements. Completion of the initial FR, the procurement ratio, illuminated the cue light and turned on the pellet dispenser. Each completion of a second FR requirement (the consumption ratio) while the cue light was on resulted in the delivery o f a 45-mg pellet into the food cup. The cue light remained on (and the consumption ratio remained in effect) until 10 consecutive minutes had elapsed without a bar press. At this time the cue light and the pellet dispenser were turned off, and completion of the original procurement ratio was again required in order to turn on the cue light that signalled access to the consumption contingency. Initially following magazine training, both ratio costs in both phases of the L/D cycle were fixed at FR 40. In Procedure 1, the procurement cost in the dark phase was increased stepwise every 6--8 days: FR 80, 160, 320, 640, 1280, and 2560. The criterion for changing this FR was four days of stable behavior with respect to the number of meals obtained daily. After FR 2560, a descending series of procurement ratios was in effect. The procurement cost in the light phase and the consumption cost in both phases remained fixed at FR 40 throughout this procedure. In Procedure 2, after one week with procurement and consumption costs in both L/D phases fixed at FR 40, the experimental animals were placed on an ascending series of procurement costs in the light phase: FR 80, 160, 640. Procurement cost in the dark phase and consumption cost in both phases were fixed at FR 40. As before, each ratio was in effect for 6--8 days. Animals had ad lib access to water. Body weight, food intake, and water intake were recorded daily at light onset. The data presented below are derived from the last four days of each schedule condition. Initiation of a meal was defined by the acquisition of three food pellets, and meals were considered to have terminated when no bar-pressing occurred for 10 consecutive minutes following the last pellet delivery. Records of bar pressing, pellet delivery, and the temporal sequence of meal patterns were obtained on cumulative recorders (Gerbrands, Arlington, MA). RESULTS
As the nocturnal cost of gaining access to the feeder increased, the frequency of initiating meals in the dark decreased monotonically for both experimental animals (see Fig. 1). Meal size (g/meal) of Rat 3 in the dark increased as a function of procurement cost to FR 640 and then decreased
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FIG. 1. The number of meals taken in the light, the dark, and their total as a function of the cost of procuring access to a meal in the dark (left panel), and as a function of the cost of procuring access to a meal in the light (right panel). Vertical lines = _+(SE).
to zero by FR 2560 (see Fig. 2). The values of these factors (meal frequency, meal size) combined to yield a lower total intake in the dark at procurement costs greater than FR 640 (see Fig. 3). Rat 4 increased meal size at the higher costs, taking only a single large meal in the dark at FR 2560 (see Fig. 2); again, the combined result was a decrease in total intake in the dark at procurement costs greater than FR 640 (see Fig. 3). The reduction in total intake in the dark, when procurement costs were high, was compensated for in each instance by a simultaneous increase in both the frequency and size of meals taken in the light. Although the total number of meals taken in a 24-hr period decreased, total intakes remained relatively constant. The data points obtained during the ascending series were recovered when a descending series of FR procurement costs was imposed during the dark phase. Procurement barpress rates were variable and did not differ significantly either between light/dark phases or across ratios for a given animal, averaging approximately 60-70/min for the first and 40-50/min for the second. For one rat, bar-press rates associated with the FR 40 consumption cost increased from approximately 45/min at the lowest procurement cost to 95/min at the highest (FR 2560); the response rate of the second rat during the consumption component varied from 85-100/min over all procurement costs. Introduction of an ascending series of procurement costs in the light phase caused both animals to reduce the frequency of meals initiated in the light to zero at FR 640. Rat 4 increased the number of meals taken in the dark compensatorily and thus maintained a constant number of meals (and a constant intake) in each 24-hr period. However, Rat 3 did not increase the number of meals initiated in the dark sufficiently to compensate for the reduction in light-phase meals. As a result, his total daily number of meals, and his total daily intake, decreased. RESULTS AND DISCUSSION
It is clear from these results that the relation between procurement cost and the meal frequency-meal size function is not symmetrical over the two phases of the L/D cycle. A
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substantially larger procurement cost in the dark is required for the rat to begin feeding exclusively in the light than is required in the light for the rat to begin feeding exclusively in the dark. That is, it is more difficult to reverse the asymmetry that already exists (rats being nocturnal) than it is to exaggerate it. However, it is also clear that the rat is sensitive to the costs of nocturnal feeding. The effect of procurement cost on the meal frequency-meal size relation is situation-dependent: The decline in meal frequency and the accompanying increase in meal size occurred in the dark when the dark procurement cost was increased; at the same time, meal frequency in the light (fixed procurement cost) remained stable while meal size increased. Only when the dark meal frequency fell to zero did the frequency of meals taken in the light also begin to increase. The two control animals (Rats 1 and 2) ate 67% (_+0.7) and 72% (_+2. l) of their meals in the dark, respectively. The initial difference in body weights of the control and experimental animals, a result of the introduction of FR schedules for the experimental rats, persisted until the end of the experiment; however, following their initial loss, experimental animals grew at the same rate as the controls. EXPERIMENT 2 In this experiment, the cost of consuming a meal (i.e., the FR per pellet) in the dark, once access to a meal had been gained, was varied, first in an ascending and then in a descending series. This procedure was completed twice, first with the cost per pellet in the light fixed at FR 1 and, following this, with the cost per pellet in the light fixed at FR 40. METHOD
Animals Subjects were four male albino rats, obtained as before and 90 days old at the start of the study. Rats 1 and 2 were experimental animals and Rats 3 and 4 were control animals.
Apparatus Caging was the same as before, except that a Hoeltge tunnel feeder was mounted on the control animals' cages.
and total intake as a function of the cost (FR) of procuring access to meals in the dark (left panel) and in the light (right panel) when consumption cost was fixed at FR 40.
Two cups were placed beneath the tunnel. One, the " d a y " food cup, was available during the light phase of the L/D cycle. When the lights went out during the dark phase, a motor moved the second cup, the "night" food cup, under the tunnel opening. Thus light and dark food intake levels for the controls could be measured separately.
Procedure The animals were again housed in the apparatus continuously. Initially an FR 1 per pellet schedule was in effect for the experimental animals in both phases of the L/D cycle. An increasing series of consumption costs (FR 5, 10, 20, 40, 80, 160, 320) per pellet was then imposed during the dark phase while the consumption cost per pellet in the light was maintained at FR 1. The increase in dark phase consumption cost continued until an animal's total food intake occurred in the light phase of the L/D cycle. Each consumption ratio (FR) was then replicated by decreasing the FR in the dark in a descending sequence. Finally, an F R 40 consumption cost was instituted in both phases of the L/D cycle. Consumption cost was then increased (FR 80, 160, 320) in the dark phase until the animal's total food intake again occurred in the light phase. This was followed, as before, by a descending series of FRs. For each schedule condition, the FR was in effect for 6-8 days. The cue lights above the food trays and the tunnel feeders were not used in this experiment. RESULTS AND DISCUSSION
Meal frequencies in the dark and in the light were relatively unaffected by changes in consumption cost with two exceptions: Rat 2 showed a decline in meal frequency when consumption cost was first increased from FR 1 to FR 5, and both rats stopped feeding in the dark (zero frequency) at the point at which consumption cost became too high. When light consumption cost was raised to FR 40 (right panel) it
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had little effect on the pattern of meal frequencies. These curves almost exactly replicated those for FR 40-320 when light consumption cost was FR 1 (see Fig. 4). This general result is similar to previous findings that meal (or drinking) frequency is relatively unaffected by changes in consumption cost when consumption cost remains constant across the L/D cycle [7,13]. In all cases, meal size decreased in the dark and increased in the light as the dark phase consumption cost increased (see Fig. 5). This result differs from previous data, obtained when consumption cost remained constant across the L/D cycle, that showed meal size to be unaffected by changes in consumption cost [7,13]. Thus the basic adjustment to a differential L/D phase consumption cost is by means of meal size. Rate of bar pressing in the dark increased from 6/min to FR 1 to 60/rain at FR 80 for one rat, and from 6/min at FR I to 110/rain at FR 80 for the other rat. Rates of bar pressing in the light remained constant. The total amount of food consumed per day as a result of these changes is meal patterns remained relatively constant. Food intake in the light phase gradually increased and food intake in the dark phase gradually decreased until all feeding occurred in the light (see Fig. 6). These shifts in the feeding pattern can be contrasted to the L/D cycle of feeding exhibited by the control animals. The final percent of food intake in the dark was 51% (---2.0) for one rat and 63% (_+2.0) for the other. GENERAL A
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NOCTURNAL FEEDING
559
competition, and resource availability and abundance, have favored the rat's adoption of a nocturnal niche. These are reflected in the rat's morphology as well as in its speciesspecific behaviors, including the rat's tendency to consume most of its food in the dark. This periodicity in feeding behavior has been the basis of extensive laboratory studies of both circadian rhythms and homeostatic models of the regulation of food intake (for reviews, see [2, 3, 9, 10]). However, these same factors can be shown to be operative in the current life history of this generalist omnivore [1, 4, 11, 12, 14, 17]. The present results provide convergent evidence, showing that when the cost of either foraging or consumption is different in the light and dark phases of the L/D cycle, the rat adjusts its pattern of feeding in the direction of minimizing feeding cost. The contribution of endogenous factors to this pattern of feeding is reflected in the asymmetry of this cost function; that is, the cost differential must be greater in the dark compared to the light to produce a shift in feeding activity to the phase of the L/D cycle in which current costs are minimal. The means by which the shift is accomplished becomes clear in the present results. Confirming previous results [6,8], increases in the cost of foraging in the dark result in a decrease in the frequency of meals in the dark and an in-
crease in the size of meals until the meal frequency in the dark drops to zero. At the same time, meal frequency in the light phase remains constant, but the size of meals taken in the light increases. As a consequence, total 24-hr intake is defended. On the other hand, when consumption costs increase in the dark, meal frequency in both phases of the L/D cycle remains relatively constant over the middle range of costs while meal size decreases in the dark and increases in the light until meal size in the dark declines to zero. Again, however, total intake is defended. At higher combined dark and light consumption costs, total 24-hr intake decreases (see also [8]). As predicted by previous data, response rates increased in the particular phase of the L/D cycle in which consumption costs selectively increased [8]. In summary, the effects of foraging and consumption costs on feeding patterns are similar in those phases of the L/D cycle in which they are varied to those that have been observed when these costs are varied uniformly across the entire L/D cycle. These results add to the growing body of data which suggest that the major determinants of the pattern of intake over 24 hours (that is, the pattern of meals) reside in the economic structure of the environment [6]. Regulation of intake as a result of endogenous factors appears to have a longer time frame than is usually assumed [10].
REFERENCES 1. Armstrong, S. A chronometric approach to the study of feeding behavior. Neurosci Biobehav Rev 4: 27-53, 1980. 2. Aschoff, J. Exogenous and endogenous components in circadian rhythms. Cold Spring Harbor Syrup Quan Biol 25: I 1-28, 1960. 3. Aschoff, J. Survival value of diurnal rhythms. Zool Sot" Lond Syrup 13: 79-98, 1964. 4. Calhoun, J. F. The ecology and sociobiology of the Norway rat. U.S. Dept. of Health, Education & Welfare (PHS Monograph 1008), 1963. 5. Canby, T. Y. The rat: Lapdog of the devil. Nat Geog 152: 60-86. 1977. 6. Collier, G. H. Determinants of choice. In: Nebraska Symposium on Motivation, edited by D. Bernstein. Lincoln: University of Nebraska Press, 1982. 7. Collier, G., E. Hirsch and R. Kanarek. The operant revisited. In: Handbook of Operant Behavior, edited by W. K. Honig and J. E. R. Staddon. New York: Prentice-Hall, 1977. 8. Collier, G. and C. K. Rovee-Collier. A comparative analysis of optimal foraging behavior: Laboratory simulations. In: Foraging Behavior: Ecological, Ethological. and Psychological Approaches, edited by A. C. Kamil and T. D. Sargent. New York: Garland STPM Press, 1980.
9. Enright, J. T. Ecological aspects of endogenous rhythmicity. Ann Rev Ecol Syst 1: 221-238, 1970. 10. Le Magnen, J. The metabolic basis of dual periodicity of feeding in rats. Behav Brain Sci 4: 561-607, 1981. 11. Levin, R. and S. Levine. Ecological determinants of circadian rhythms in rats. Paper presented at the Meeting of the EPA, Philadelphia, April 1974. 12. Levin, R. and J. M. Stern. The ontogeny of nocturnal feeding in the rat. J Comp Physiol Psychol 89:711-721, 1975. 13. Marwine, A. and G. Collier. The rat at the waterhole. J Comp Physiol Psychol 93: 391-402, 1979. 14. Panksepp, J. and K. Krost. Modification of diurnal feeding patterns by palatability. Physiol Behav 15: 673-677, 1975. 15. Richter, C. P. Inborn nature of the rat's 24-hour clock. J Comp Physiol Psychol 75: 1-4, 1971. 16. Rovee-Collier, C. K., B. A. Clapp and G. H. Collier. The economics of food choice in chicks. Physiol Behav 28:1097-1102, 1982. 17. Stern, J. M. and R. Levin. Food availability as a determinant of the rats' circadian rhythm in maternal behavior. Dev Psychobiol 9" 137-148, 1976.