Meal-taking by domestic chicks (Gallus gallus)

Anim. Behav., 1983, 31, 397-403

MEAL-TAKING BY DOMESTIC CHICKS

(CALLUS CALLUS)

BY LYNN K A U F M A N * & GEORGE COLLIER~ * Walter Reed Army Institute of Research, Washington, D.C. 20012, U.S.A. ~Department of Psychology, Rutgers University, New Brunswick, NJ 08903, U.S.A. Abstract. Caged, isolated granivorous birds feed in frequent, brief bouts from which it is difficult to define a meal. This pattern has been viewed as a fundamental difference between the feeding behaviour of avians and mamlr/als. The present results demonstrate that this pattern of feeding is an artifact of the test situation. When the cost of access to food (foraging cost) is increased, chickens (Gallus gallus) exhibit the same pattern of feeding and the same functional relations between foraging cost, meal frequency, and meal size as mammals. Caged, isolated chickens (Gallus gallus) with food continuously present feed almost without interruption i n short, frequent bursts (Jensen et al. 1962; Duncan et al. 1970; Clifton 1979a; Squibb & Collier 1979). Because a similar feeding pattern has been observed in laboratory studies of related avian species (McFarland 1971; Stater 1974; Zeigler 1976), this pattern has been thought to characterize a significant difference between avian and mammalian species. These studies were conducted in experimental chambers which isolated the bird from extraneous events and provided minimal stimulation and response opportunities (the 'refinement' paradigm) on the assumption that this procedure would permit a more exact determination of a given individual's intrinsic pattern of feeding. However, this experimental setting does not adequately simulate essential aspects of the animal's niche, preventing the animal from exhibiting its phylogenetic and ontogenetic strategies for efficiently harvesting the available resources within the time and energy constraints of its other biologically significant activities (McFarland 1977; McCleery 1978; Collier & Rovee-Collier 1981). Because the major feeding response (pecking) of avians is also the response exhibited during exploration and social interaction, the high incidence of pecking observed in previous studies cannot be attributed solely to feeding. Further, the tendency to peck at whatever few stimuli are present is even greater when the subjects are young social birds who exhibit a high level of distress-calling, hyperactivity, asocial aggression, and other agitated behaviours when isolated (Kaufman & Royce 1975). This capricious activity may account in part for the large inter- and intraindividual variability reported in previous studies (Duncan et al. 1970; Slater t974; Clifton 1979a, b).

The pattern of avian feeding that is obtained when the refinement paradigm is used has made the experimental definition of a meal difficult. Different bout termination criteria yield a continuous function rather than the discontinuous function typically used to define meals (LeMagnen & Tallon 1966; Levitsky & Collier 1968; Wiepkema 1968; Kissileff 1970; Levitsky 1970; Collier et al. 1972; Panksepp 1973; Slater 1974) and fail to separate reliably feeding from other activities. Attempts to solve this problem by means of survivorship functions have resulted in different meal criteria for different individuals and even for the same individual at different times of day (Slater 1974; Clifton 1979a). However, statistical solutions to this problem are unlikely to yield a valid measure of avian feeding patterns that relates to current hypotheses of the determinants of the initiation and termination of meals. Traditional research on feeding pattern~ has been based on the hypothesis that metabolic rhythins associated with cycles of depletion and repletion determine meal initiation and termination, respectively (Richter 1927, 1947; Brobeck 1955; Thomas & Mayer 1968; Novin et al. 1976; Booth 1978; LeMagnen 1981). The refinement paradigm was viewed as an ideal means of eliminating 'extraneous' sources of input that presumably interfered with the expression of these rhythms. However, demonstration of an intrinsic, homeostatic feeding rhythm has proven elusive (Baker 1953; Duncan et al. 1970; Slater 1974; Panksepp 1978, 1980; Clifton 197%). Richter (1927) was the first to hypothesize a relationship between meal patterns and momentary metabolic states. However, his observations also laid the groundwork for an alternative hypothesis that the structure of the environment 397

398

ANIMAL

BEHAVIOUR,

determines when meals begin and end. His first observation was that meal frequency declined and meal size increased compensatorily as a function of the number, variety, and significance of the activities concurrently available to his rats. This suggests that meals could be more accurately determined in an enriched environment because they would be less frequent and more clearly distinguished from other activities. While this has been confirmed in anecdotal field observations of chickens, there have been few systematic studies of this conjecture (cf. Hill & Demchak 1977). Richter also observed that meal frequency decreased when more effort was required to gain access to food. This has been confirmed in both laboratory and field observations of a number of mammalian species (for review see Collier & Rovee-Collier 1981). While previous studies of avian feeding have considered the cost of feeding (Duncan et al. 1970; Clifton 1979a), they have not distinguished between the cost of foraging (gaining access to food) and the cost of consumption (ingestion per se) which are functionally distinct in natural settings (Schoener 1971; Collier et al. 1977; Pyke et al. 1977; Marwine & Collier 1979; Collier & Rovee-Collier 1981). When food is readily available, most animals eat small, frequent meals. This may be an antipredator strategy but may also reflect the fact that the consumption and processing of large meals entail some costs (Collier 1980). When the cost of procuring food increases, animals can maintain a constant total cost of feeding by initiating meals less often but consuming more on each occasion. These changes in meal patterns are seen only when the animal can control both the initiation and termination of its own bouts of feeding and its total intake. Thus small, frequent meals are not a defining species characteristic but are a function of environmental costs. On the other hand, changing the cost of eating a meal (i.e. the cost per portion within a given meal) does not affect feeding patterns. If the animal must pay the same price 'per bite' no matter how it distributes its bites over time, then changes in meal frequency or size will not enable the animal to minimize these costs or the total cost of intake. In laboratory simulations of consumption cost, increasing the operant requirement for each single food pellet within a meal (e.g. from 1 to 300 bar presses) does not change meal frequency (Collier et al. 1972; Hirsch & Collier 1974). By bar-pressing more rapidly for each 'bite',

31,

2

however, animals minimized meal duration which otherwise would have lengthened as more bar presses were interpolated between successive pellets. When the operant requirement was imposed on each brief, fixed-duration operation of the feeder within a meal (instead of each small, fixed-sized pellet), similar findings were obtained: meal frequency and meal size were unaffected but rate of responding within a meal increased as hopper duration decreased (Collier & Kaufman 1977). A distinction between foraging and consumption costs has also been reported for drinking (Marwine & Collier 1979) with similar results. In prior studies of avian feeding, both Clifton (1979b) and Duncan et al. (1970) varied the operant requirement for each brief, fixed-duration operation of the feeder, i.e. consumption cost. As expected, neither observed a change in meal size or meal frequency under such conditions and so their definition of a meal remained the same as that used in unconstrained feeding. Because neither measured consumption rate, the effects of increasing consumption cost on within-meal behaviour could not be seen. In the present experiment we sought to eliminate the necessity of arbitrary meal criteria through exploring the effect of foraging cost on feeding patterns of an avian species. In doing so, we asked whether previous descriptions of avian feeding patterns are artifacts of the testing situation or whether they represent a true difference in the feeding behaviour of avians and mammals.

Methods Animals Eight male broiler chickens (Gallus gallus) were obtained at one day of age and tested in two replications of four chickens each. Apparatus Chickens were individually housed in 37.5 x 52.5 • 40.0 cm cages (Wahmann CL316/A) mounted two abreast. A hardware-cloth partition separating each pair of cages permitted visual and auditory contact between adjacent subjects. This form of social housing obviated some of the effects of isolated rearing in young chicks (Kaufman & R o v e e 1975). Each cage was equipped with front-mounted food and water hoppers (Wahmann LC-287/S). The feeder mounting was modified so that a motor-operated door covered the 9.0 • 9.0 cm entrance to the feeder. A photocell, mounted across and just inside the feeder opening, monitored feeding

KAUFMAN & COLLIER: FEEDING BY CHICKENS activity. A response key (Grason-Stadler E8670A), requiring 0.5 N of force to operate, was mounted centrally in the front of the cage between the food and water hoppers. The height of the keys was adjusted as the chickens grew. Procedure We housed chicks in pairs for the first 10 days posthatch with free access to food and water. We then placed them into individual cages and, five days later, trained them to key-peck for access to food. Free-access feeding patterns were obtained from four of the chicks during the five days of individual housing prior to training. During the experiment, food procurement was contingent upon completion of a key-peck requirement. When the required number o f pecks had been emitted, the door that blocked the feeder entrance moved aside and allowed access to the food for a self-terminated meal. Food remained accessible as long as the chick continued to feed and until 10 consecutive minutes elapsed without a feeder re-entry (monitored by the photocell), at which time the feeder door closed. Access to food for another meal could be obtained only if the chick again completed the key-peck requirement. Meal duration was defined as the time from the opening of the feeder door to the time of the last photocell break. During the initial free-access phase, we observed frequent, short bursts of feeding typical of that described by other investigators (Duncan et al. 1970; Slater 1974; Zeigler 1976; Clifton 1979a; Squibb & Collier 1979). Intra- and interindividual variab!lity was high regardless of the particular meal criterion we used. When we introduced the requirement of a single key-peck to open the feeder door, feeding behaviour clustered into identifiable, discrete bouts, and a 10-min meal criterion resulted in a reliable meal count with low intra- and inter-individual variability. This will be elaborated below. Although the key-peck requirement for access to food was systematically increased as the experiment increased (1, 10, 20, 40, 80, 160, 320, 640, 1280, 2560 and 5120 key-pecks), for a given subject it was never increased above the value at which that animal's mean meal frequency fell below one meal every two days. Upon completion of the ascending series of procurement costs, four animals were retested at some or all of five randomly-ordered values (20, 80, 320, 1280 and/ or 2560 key-pecks) in order to ascerta.in the stability of behaviour at a given procurement cost. Each key-peck requirement remained in

399

effect for a minimum of 7 days and until we obtained at least four consecutive days of stable meal patterns. Thus the duration of the total experimental period differed for each bird but lasted approximately 30-90 days. By the end of the experiment, chickens were 100-115 days old. Chicks were housed on a 12:12 L:D schedule at a temperature of 22-26 C and a humidity of approximately 50 %. Daily maintenance occurred in the hour immediately following light onset. During this time body weight and food and water intake were measured. Spilled food was collected and weighed. Food and water hoppers were then refilled to their original levels. Throughout the study, chicks were fed commercial chick starter (F.C.A. of New Jersey). Results Data analyses were based on the last four consecutive days of each key-peck requirement schedule. Because there were no significant differences between replications, data from the two replications were combined. The effect of increasing procurement cost on meal frequency is shown in Fig. 1. Daily meal frequency was a decreasing function of procurement cost. When only one key-peck was required to open the feeder door, chicks initiated approximately 15 meals per day (approximately one meal every 48 min). As the procurement cost increased, chicks reduced meal frequency until, at the highest procurement costs, they ate less than one meal per day. The initiation of less than one meal per day first occurred at key-peck requirements of 640 ( N = 1), 1280 ( N = 1) 2560 (N = 5), and 5120 ( N - 1). As procurement cost increased and meal frequency decreased, meal size increased in a compensatory manner for all chicks (Fig. 1). Chicks that were retested at randomly-ordered procurement costs initiated meals with the same frequency and of the same size as had originally been associated with those particular procurement costs when they had been serially ordered. The success of the strategy of reducing meal frequency (and increasing meal size) in terms of maintaining a relatively constant total cost of feeding is shown in Fig. 2. The upper and lower lines indicate the cost (number of key-pecks) to a chick had it continued to consume 15 meals/day, or had it consumed only one meal/day, as the procurement cost (number of key-pecks) increased. The average actual cost falls between these two bounds except at those procurement costs associated with less than one meal/day.

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Fig. 1. Mean (over 4 days) daily meal frequency and food intake per meal as a function of cost for eight chickens. Each line represents an individual subject. The filled circles in the left portion of tbe figure represent the performance of the four chickens for which free-access data were obtained. Open circles represent the performance of four chickens during the retest series.

Consumption rate (grams of food eaten per minute of meal time; Fig. 3) also increased for every chick as procurement cost increased. This ability of birds to adjust their rate of eating has seldom been reported and is the source of many disparate results in amount-of-reward studies with birds (Hirsch & Collier 1974). Consumption rates during retesting at selected procurement costs did not differ from rates at corresponding costs during the original ascending series, eliminating age- and growth-related factors (e.g. beak size) as the basis for the increase in rate of food intake during the original test series. The preceding changes in feeding patterns enabled chicks to obtain an average total daily food intake sufficient to maintain a high growth rate (Fig. 3). Although freely-feeding controls

Fig. 2. Effort (key-pecks) expended per day by eight chickens as a function of procurement cost per meal. Symbols ( 9 indicate actual mean performance. Solid

lines indicate costs that would have been incurred had the animals maintained the meal frequency associated with a single key-peck requirement (approximately 15 meals per day) across all conditions (upper line) or taken only one meal per day across all conditions (lower line). were not run during the first 40 days of the study, growth curves of chicks in the present study actually surpassed the standard curve of singlyhoused male chickens from the same supplier. Moreover, chicks were healthy, vigorous, and did not differ in size from chickens of the same age used in numerous other experiments in our laboratory over the years. Throughout the course of the experiment, chicks retained their characteristic diurnal pattern of feeding. Finally, the running rate of key-pecking, defined as the rate o f responding over the time interval between the first and last key-peck of a given procurement requirement, also increased as a function of procurement cost (Fig. 3). Analyses of free-access feeding data collected from four chicks yielded no significant correlations between meal duration and either preprandial (range = 0.000-0.126) or postprandial (range = 0.009-0.104) interval. Similar analyses over meal patterns of chicks at procurement costs of 1, 10, 20 and 40 key-pecks, when meals were less frequent and larger, also yielded no significant values (see Table I). When the procurement cost was 80 key-pecks, two chicks showed significant correlations and two did not. These data are consistent with Richter's (1927)

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Fig. 3. Means (over 4 days) of consumption rate, total food intake per day, body weight, and rate of keypecking (procurement rate) as a function of procurement cost. Vertical bars represent standard errors of the mean. third observation that meals are distributed randomly within the phase of the photoperiod that the animal is active. Discussion Contrary to previous reports, chickens eat in discrete meals. In this respect, their pattern does not differ from that of most mammalian species. This pattern emerged following the introduction of a small and seemingly insignificant foraging cost (one peck) that reduced the frequency of feeder entries. An enriched environment with opportunities for alternative activities would also be likely to reduce entries. The domestic chicken has undergone intense artificial selection for rapid growth, high egg production, and high

FEEDING

BY

401

CHICKENS

feed efficiency. As a result, the rate of food consumption by chickens is high, and their efficiency of conversion of food stuff to protein exceeds that of any other domesticated animal. Even so, the present results show that chickens feed in discrete meals with a frequency that appears to be independent of their growth demands. Moreover, chickens deploy the same strategy of reducing meal frequency while increasing meal size in response to increases in the cost o f access to food as many animals, both wild and domesticated, that occupy widely different niches. When meals are infrequent and large, the usual assumption is that there are substantial fluctuations in the circulating metabolites associated with this pattern. If meals are initiated and terminated in response to these fluctuations (LeMagnen 1981), then the prandial correlations should be large. In the present study, such large correlations would be particularly expected when meals were less frequent. The correlations, however, do not support this hypothesis. An alternative hypothesis is that the internal milieu is defended by means of storage, both internal (e.g. adipose tissue) and external (e.g. the gut). The avian crop, which plays only a minor role in digestion, is an important external storage device (Bolton 1965; Hazelwood 1972; Ziseiler & Farner 1972). Following a single 2-h meal per day, the amount of food in the chicken crop declines throughout the 22-h postfeeding interval but the amount of food in other portions of the digestive tract remains fairly constant (Shannon & McNab, cited in Richardson 1970). Enlargement of the digestive tract, Table I. Prandial Correlations Premeal interval vs meal duration Subject No. 1 2 3 4

FR1

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0.000 0.129 0.001 0.085

0.055 0.305 0.006 0.000

0.002 0.257 0.040 0.003

0.102 0.012 0.002 0.391

Meal duration vs postmeal interval Subject No. 1 2 3 4 *P < 0.05.

FR1

F R 10

FR20

FR40

FR80

0.117 0.226 0.020 0.003

0.007 0.001 0.062 0.055

0.005 0.076 0.002 0.000

0.015 0.114 0.215 0.096

0.683* 0.609* 0.194 0.032

402

ANIMAL

BEHAVIOUR,

especially of the crop, has been observed in chicks with only brief daily periods of food access (Lepkovsky et al. 1960; Feigenbaum et al. 1962; Leveille & Hanson 1965). Conversely, cropectomized chickens with continuous access to food grow as well as unoperated and shamoperated controls (Fisher & Weiss 1956; Griminger et al. 1969), but they do not respond well when food access is restricted (Lepkovsky et al. 1960; Griminger et al. 1969). In the present study a shift to a pattern of infrequent, large meals as a result of the increasing cost of procurement did not depress growth, even when chickens ate as infrequently as once every two days. This suggests that food stored in the crop buffers the effects of variable resources and lengthy intermeal intervals and permits the chicken and other physiologicaIly similar species to survive periods of food scarcity or environmental stringency (Hazelwood 1972; Wilson t975; Wolf & Hainsworth 1977). Mechanisms that serve a similar cost-reducing function have also evolved in other species, e.g. the large, acid stomach of the carnivore and the large rumen or caecum of some herbivores. Two ways of reducing the time cost associated with feeding were available in this experiment, and the chickens used both. The time spent procuring a meal was reduced by increases in the rate of key-pecking, and the total time spent eating was reduced by increases in the rate of eating once the meal was procured. These behaviours may reflect the social nature of the chicken. Changes in feeding rate have been associated with changes in food availability in field observations of socially-feeding nondomesticated animals (Geist 1971; Kruuk 1972). Geist (1974) suggested that socially-feeding conspecifics compete for scarce food resources by eating as rapidly as possible. This is seen as a more efficient and evolutionarily successful means of competing than fighting. The present results add to the picture of the chicken as a generalist omnivore. Like the rat, the chicken is capable of adapting to a wide variety of climates, food sources, abundance, and availability (Rovee-Collier et al. 1982). Here we have shown that the structure of the environment is a major determinant of the pattern of feeding: chickens will eat either frequent, small meals or infrequent, large meals depending upon the cost of procuring them. These results, along with others (Collier 1980; Collier & Rovee-Collier 1981), suggest that the regulation of food intake by its metabolic Consequences must be viewed as

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a long-term rather than a short-term process. Meal patterns do not reflect momentary fluctuations in the internal environment; rather, they appear to be a behavioural device that animals adjust to exploit the available resources in their current habitat efficiently.

Acknowledgments This research was supported by Grant HD-10588 from the National Insiitutes of Health and a Biomedical Research Support Grant from Rutgers University to the second author. The manuscript was prepared while the first author was a National Research Council Associate at the Walter Reed Army Institute of Research, Washington, D.C. Portions of these data were presented at the meeting of the Eastern Psychological Association, Washington, D.C., March 1978. We thank C. Royce-Collier for comments and editorial assistance.

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J. R. Krebs & N. B. Davies), pp. 377-410. Sunderland, MA: Sinauer Associates. McParland, D. J. 1971. Feedback Mechanisms in Animal Behaviour. London : Academic Press. McFarland, D. J. 1977. Decision making in animals. Nature, Lond., 269, 15-21. Novin, D., Wyrwicka, W. & Bray, G. 1976. Hunger: Basic Mechanisms and Clinical Implications. New York: Raven Press. Panksepp, J. 1973. Reanalysis of feeding patterns in the rat. J. eomp. physiol. Psyehol., 82, 78-94. Panksepp, J. 1978. Analysis of feeding patterns: data reduction and the theoretical implications. In: Hunger Models: Computable Theory of Feeding Control (Ed. by D. A. Booth), pp. 143-166. London: Academic Press. Panksepp, J. 1980. Hypothalamic integration of behavior: rewards, punishments, and related psychological processes. In: Handbook of the HypothaIamus, Vol. 3; Part B: Behavioral Studies of the Hypothalamus (Ed. by P. J. Morgane & J. Panksepp), pp. 289-431. New York: Marcel Dekker. Pyke, G. H., Pultiam, H. R. & Charnov, E. L. 1977. Optimal foraging: a selective review of theories and tests. Q. Rev. BioL, 52. 137-154. Richardson, A. J. 1970. The role of the crop in the feeding behavior of the domestic chicken. Anita. Behav., 18, 633-639. Richter, C. P. 1927. Animal behaviour and internal drives. Q. Rev. Biol., 2, 30'7-342. Richter, C. P. 1947. Biology of drives. J. comp. physiol. PsyehoL, 40, 129-134. Rovee-Collier, C. K., Clapp, B. A. & Collier, G. H. 1982. The economics of food choice in chicks. PhysioL Behav., 28, 1097-1102. Schoener, T. W. 1971. Theory of feeding strategies. Ann. Rev. Ecol. Syst., 2, 369-404. Slater, P. J. B. 1974. The temporal pattern of feeding in the Zebra finch. Anim. Behav., 22, 506-515. Squibb, R. L. & Collier, G. H. 1979. Feeding behavior of chicks under three lighting regimens. Poult. Sci., 58, 641-645. Thomas, D. W. & Mayer, J. 1968. Meal taking and regulation of food intake by normal and hypothalamic hyperphagic rats. J. eomp. physiol. PsychoL, 66, 642-653. Wiepkema, P. R. 1968. Behaviour changes in CBA mice as a result of one goldthioglucose injection. Behaviour, 32, 179-210. Wilson, E. O. 1975. Sociobiology. Cambridge, MA: Harvard University Press. Wolf, L. L. & Hainsworth, F. R. 1977. Temporal patterning of feeding by hummingbirds. Anim. Behav., 25, 976-989. Zeigler, H. P. 1976. Feeding behavior of the pigeon. In: Advances in the Study of Behavior, Vol. 7 (Ed. by J. S. Rosenblatt, R. A. Hinde, E. Shaw & C. Beer), pp. 286-381. New York: Academic Press. Ziseiler, V. S. & Farner, D. S. 1972. Digestion and the digestive system. In: Avian Biology, Vol. 2 (Ed. by D. S. Farner & J. R. King), pp. 343-430. New York: Academic Press.

(Received 18 March 1981 ; revised 24 August 1982; MS. number: a2626)