effects of predictable versus unpredictable feeding schedules on chimpanzee behavior

ELSEVIER

APPLIED ANIMAL BEHAVIOUR

SCIENCE

Applied Animal Behaviour Science 44 ( 1995) 65-74

Effects of predictable versus unpredictable feeding schedules on chimpanzee behavior

Mollie A. Bloomsmith *, Susan P. Lambeth Department of Veterinary Sciences, The University of Texas M.D. Anderson Cancer Center, Science Park,

Bastrop. TX 78602, USA

Accepted 3 I January 1995

Abstract

One factor not often studied in the design of feeding enrichment programs is the timetable according to which enrichments are offered. This study was performed to lend a quantitative basis to primate colony management decisions concerning feeding schedules. The objective was to determine whether feeding fresh produce meals on a predictable schedule was preferable to doing so on an unpredictable schedule from the perspective of promoting psychological well-being of chimpanzees. The subjects were 30 adult or adolescent chimpanzees (Pun rroglodytes) living in four different social groups. Feeding practices were changed to a more unpredictable schedule for two of these groups, 5 or 6 months prior to the initiation of data collection; feeding of the other two groups continued on a more predictable schedule. The predictable meal was always fed within a 30 min period and the unpredictable meal was fed within a 150 min period. Observational data were collected during prefeeding and baseline periods. A mixed model multivariate analysis of variance for repeated measures revealed that inactivity was more prevalent in the prefeeding period for the chimpanzees fed on the predictable schedule than in the other study phases, and abnormal behavior showed a similar trend. These findings indicate that feeding on a more unpredictable schedule may lead to increased species-appropriate behavior. The scheduling of animal care routines deserves closer attention from those conducting research on improving care and well-being of captive primates.

Keywords: Well-being; Behavioral management; Feeding enrichment; Abnormal behavior

1. Introduction

Much of the environmental enrichment research on nonhuman primates is focused on delivery of food and foraging opportunities. In general, feeding enrichment is effective in

* Corresponding author: Tel. (512) 321-3991; Fax. (512) 332-5208

0168-1591/95/$09.50 0 1995 Elsevier Science B.V. All rights reserved SSDIO168-1591(95)00570-6

66 M.A. Bloomsmith, S. P. Lambeth /Applied Animal Behuviour Science 44 (1995) 65-74

increasing species-typical patterns of foraging and in maintaining behavioral changes over repeated exposures (Chamove et al., 1982; Bloomstrand et al., 1986; Bloomsmith et al., 1988; Maki et al., 1989; Brent and Eichberg, 1991; Byrne and Suomi, 1991; Bayne et al., 1991; Bayne et al., 1992). However, one aspect that might be important in the design of feeding enrichment programs-the timing of the feeding opportunities-has received little study. Some stereotypies among zoo-housed carnivores were associated with regular schedules of feeding (Carlstead, 1995). At one zoo, stereotypic behavior by Fran9ois’ langurs was only recorded during pre-feeding hours (Krishnamurthy, 1994). Some stereotypies among sows increase after meals are provided (Terlouw et al., 1993). Evidence of “food- anticipatory activity” has been found in many species, including rodents, bees, fish, birds, rabbits, and mammalian carnivores, and in one primate species (Suimiri sciureus) (see Mistlberger, 1994, for a review) when they are presented with a restricted number of meals on a predictable schedule, The diversity of fruit fed to chimpanzees did not affect levels of prefeeding agonistic activity in one study (Howell et al., 1993). The question of whether captive animals should be fed on fixed or variable schedules is not new. In a large chimpanzee colony, high levels of aggression were documented prior to and during the predictable delivery of two meals per day, although this analysis was based on little quantitative data (Wilson and Wilson, 1968). The issue of predictability in the delivery of meals to nonhuman primates has been discussed as a possible problem. Fritz and Fritz ( 1979) utilize a variable feeding schedule intended to prevent the development of undesirable behavior in their primate colony. Only one published report (Wasserman and Cruikshank, 1983) has exper- imentally assessed this, comparing prefeeding and postfeeding behavior in a group of seven captive hamadryas baboons. Wasserman and Cruikshank found that aggressive behavior among the baboons took place more often in the 3 h period prior to the meal fed on a predictable schedule than in the 3 h postfeeding period. The authors mentioned that aggression peaked just before the main meal of the day, but they did not support the statement statistically.

There are three bodies of literature addressing predictability that may be relevant to a discussion of the effects of meal schedules on primate behavior. First, unpredictability has been implicated as an important factor in the development of experimental neuroses. Exper- imental neuroses are behavioral disturbances in laboratory animals that emerge in place of previously learned behavior, are uncharacteristic of an animal’s ordinary behavior, and usually include some signs of excessive autonomic arousal. Mineka and Kihlstrom ( 1978) concluded in their literature review that in the cases of experimental neurosis they studied, environmental events of vital importance to the organism became unpredictable, uncontrollable, or both/ (p. 257), and that it is important for the organism that certain events (e.g., acquisition of food, escape from pain) occur in a predictable and/or controllable manner/ (p. 260). These findings indicate that unpredictable events might be detrimental to animal well-being because they elicit behavioral disturbances.

The second collection of literature is by Rosenblum and his colleagues and deals with how foraging demands affect nonhuman primate behavior (Rosenblum and Sunderland, 1982; Rosenblum and Paully, 1984; Rosenblum and Smiley, 1984; Andrews and Rosen- blum, 1991, 1993). In one study, experimenters varied foraging demand levels between low and high without giving any external cues to the bonnet macaque (Macacu rudiufu) subjects; thus, the changes in foraging demand were unpredictable to the subjects. The

M.A. Bloomsmith, S.P. Lambeth /Applied Animal Behaviour Science 44 (1995) 65-74 6-I

monkeys exposed to fluctuating levels of foraging demand manifested a variety of behaviors indicative of social disturbance, including increased agonism, less social grooming, and less secure attachment to infants than subjects under conditions of consistently low or high foraging demand (Rosenblum and Paully, 1984; Andrews and Rosenblum, 1991, 1993). Because all of these behavioral changes could be considered detrimental to primate well- being, Rosenblum’s studies support the hypothesis that an unpredictable feeding schedule may be harmful to primate well-being.

The third area of investigation related to that of predictability is control over environmental stimuli. Predictability and control of events are, of course, related because an event that can be controlled can also be predicted. When animals have control over the presentation of events in their environment, benefits to the animals have been demonstrated. Nonhuman primates with control have been shown to demonstrate reduced levels of cortisol, social aggression (Hanson et al., 1976), and fear of threatening stimuli, as well as less severe reactions to separations from peers (Mineka et al., 1986)) and improved performance on video-generated tasks (Washburn et al., 1991) when compared with those without control. The role of environmental control in improving primate well-being has not been thoroughly studied, although it is often mentioned as being critical to enhancing well-being (Markowitz, 1979; Novak and Drewsen, 1989; Snowdon and Savage, 1989).

The current study was undertaken to provide a source of quantitative data to colony management decisions about feeding schedules. Our objective was to determine whether a predictable or a more variable schedule of feeding fresh produce meals was preferable in terms of promoting the psychological well-being of chimpanzees. To infer the psychological state of an animal by observable behavior is problematic. This and other studies consider changes in behavior that move toward the species-typical model of the free-ranging coun- terpart as evidence of improvements in well-being (Line, 1987; Novak and Suomi, 1988; Bloomsmith et al., 1988; Schapiro and Bloomsmith, 1994).

2. Methods

2. I. Subjects and housing

The subjects were 30 adult or adolescent chimpanzees (Pan troglodytes) living within four different social groups at The University of Texas M.D. Anderson Cancer Center’s Science Park chimpanzee breeding facility in Bastrop, Texas. Each group had a similar composition with seven or eight subjects 8 years old or older. Each group included two or three adult or adolescent males, and four to six adult or adolescent females. Chimpanzees less than 4 years old were not included as subjects. Two groups (a total of 16 animals) were fed according to the predictable schedule and two groups (a total of 14 animals) were fed on the more unpredictable schedule.

Each group lived in an enriched, outdoor yard (22 m in diameter) containing grass as a ground cover, climbing structures, and movable objects; from each yard an indoor area was accessible (for further description see Riddle et al., 1982). During the study, all of the chimpanzees were given a variety of indestructible and destructible objects,‘several stocked

68 M.A. Bloomsmith, S.P. Lambeth /Applied Animal Behaviour Science 44 (1995) 65-74

feeding devices, small food scattered in the grass, browse, and a variety of fresh produce as part of a daily enrichment program.

2.2. Feeding procedures

The chimpanzees were fed four meals of fresh produce daily by care givers who stood on the roof level of the chimpanzee enclosures. Individual portions of fresh produce were tossed down to each group member from a height of about 6 m; the distribution was intended to minimize competition. To get to the roof level of the enclosures, the care givers left the building where the meal was prepared, climbed a nearby set of stairs, and walked across the roof adjoining all of the outdoor corrals. The groups were fed separately rather than simultaneously. As soon as a care giver came out of the building carrying the produce, he was visible to some of the chimpanzees in the colony who routinely responded with loud food vocalizations. In this way, all chimpanzees in the colony were notified of the feeding of each meal whether they were the intended recipients or not. For the purposes of this study, the moment the care giver first appeared on the roof carrying the produce was considered the beginning of the meal.

Before this study, the four produce meals were fed on a fairly strict schedule: at about 08:00, ll:OO, 13:00, and 16:00 h daily. Because this had been the routine practice, all chimpanzees in this study had been fed on this predictable schedule for about 7 years. The first and third meals of each day included produce that varied from day to day and with seasonal availability (e.g. corn on the cob, kiwifruit, celery, apples, onions). The second and fourth meals were fed mainly as nutritional supplements and were the same types of produce each day (cabbage, carrots, oranges, potatoes). In our study, behavior associated with only the first meal of the day was examined.

Six months prior to the initiation of data collection for this study, we changed the feeding practices for the two groups of chimpanzees we intended to feed on the more unpredictable schedule. This more variable schedule was implemented for all four produce meals daily. During the study, the mean time at which the meal began for the predictably fed groups was 08:16 h with a standard deviation of 10.0 min. This meal was always fed within a 30 min period during the course of this study. The mean time at which the meal began for the unpredictably fed groups was 09:08 h with a standard deviation of 57.2 min. This meal was always fed within a 150 min period.

2.3. Data collection procedures

Observational data were collected at two times: ( 1) the prefeeding period consisted of the 30 min directly preceding the beginning of the meal (as previously defined) ; (2) the baseline period was a 30 min period beginning sometime between 0!9:30 and 10:00 h. This baseline period was chosen because it best matched general morning activity levels in the colony and it did not conflict with time directly preceding one of the other three scheduled daily produce meals.

Two chimpanzee groups served as controls and were fed on the predictable schedule as described; and the other two groups were fed on the more unpredictable schedule as described. The four groups were each observed for 25 periods each of 30 min during the

M.A. Bloomsmith, S. P. Lambeth /Applied Animal Behaviour Science 44 (1995) 65-74 69

Table 1 Operational definitions for behaviors analyzed

Behavior category Definition

Abnormal Coprophagy, urophagy, feces manipulation, hair pulling, head shaking, bizarre posturing, regurgitating, rocking, self-slapping,and other idiosyncratic stereotypies (after Walsh et at., 1982)

Agonistic Attacking, hitting, tugging, biting, throwing, threatening, warning barking, brusque rushing, crouching, bobbing, presenting, fleeing, avoiding, bared- teeth screaming, pant-grunting, and hand/wrist extending (after Goodatl, 1968; Van Hoof, 1974; Bygott, 1979; Dewaat and Hoekstra, 1980)

Inactive

Self-directed

Tension-related

Sitting or standing still, hanging, lying down, or sleeping

Self-grooming, self-inspecting, and masturbating

Swaying (standing and shifting weight from side to side), displaying (nonvocal or vocal behavioral sequence incorporating drumming, repeated swaying, exaggerated, and often bipedal locomotion), pacing (repeated slow locomotion in a regular pattern lasting at least 10 s), scratching, and yawning

baseline and during the prefeeding conditions of the study. A total of 100 h was spent in data collection. Observers were clearly visible to the subjects, but collected data throughout the day for other studies as well, so it is unlikely that their presence was a cue for an upcoming meal.

Group scan sampling data (Altmann, 1974) were collected during the 30 min observation periods using a 30 s intersample interval. Thirty-one behaviors were recorded, of which 23 were collapsed into the following five behavioral categories for analysis: abnormal behavior, agonistic behavior, inactivity, self-directed behavior, and tension-related behavior. Table 1 provides operational definitions of these terms. At the same time behavior was recorded for each chimpanzee, information regarding the animal’s proximity to group mates was also recorded. If the subject was within 1 m of another adult or adolescent chimpanzee at the instant of the recording, a positive proximity score was noted.

2.4. Data summary and analysis

Scan sampling data points from the 25 observation sessions in each condition (baseline and prefeeding) of the study were collapsed for each subject over each of the five behavioral categories. A mean was calculated for each subject. This summary procedure yielded a single mean score for each subject for each behavior during each phase of the study, and this score was an estimate of the time the subject spent engaged in the particular behavior. These data were used for statistical analysis. Proximity scores were calculated similarly.

A 2( X 5 X 2) mixed model, multivariate analysis of variance (MANOVA) for repeated measures was applied to the summarized category scores. Predictability was used as a between subjects grouping factor. The five behavioral categories and the two conditions of the study were used as repeated measures and were analyzed as within subjects trial factors.

An analysis of variance (ANOVA) for repeated measures was conducted on the summarized proximity data to discover how much time each chimpanzee spent close to a group


Table 2 Percentage of subjects’ time spent in activities analyzed

Behavior category

Feeding schedule

Predictable

Baseline Prefeeding

Unpredictable

Baseline Prefeeding

Abnormal 0.4 1.0 0.1 0.2 Agonistic 0.1 0.1 0.1 0.3 Inactive 21.0 35.1 25.2 26.9 Self-directed 4.8 6.3 7.9 8.3 Tension-related 1.0 2.2 1.7 2.4 Proximity 10.4 10.5 10.9 11.5

member in the two conditions of the study. The feeding schedule was used as a grouping variable.

3. Results

The overall MANOVA was significant (F= 69.4, d.f. = 4,25, P < 0.001) . The main focus of the study was on the three-way, within-subjects interaction between meal predictability, study condition, and behavior, and was statistically revealed (F=6.2, d.f. =4,112; P<O.OOl). Planned univariate contrasts on this interaction indicated that the change in inactivity (I;= 8.0, d.f. = 1,28; P < 0.01) was statistically significant, and changes in abnormal behavior (F = 2.5; d.f. = 1,28; P = 0.1) indicated a trend in the same direction. Recorded levels for both of these behaviors were highest in the prefeeding period for the chimpanzees fed on a predictable schedule. Table 2 shows the levels of behavior recorded by group and study condition. Because the incidence of abnormal behavior in these chimpanzees was low (mean, 0.3% time, overall), the conventional probability level to determine significance was relaxed, and this finding is discussed as a trend in the data. Coprophagy and feces manipulation made up 94% of the abnormal behavior recorded.

The ANOVA indicated that the percentage of time the chimpanzees spent in proximity to other group members was not differentially affected by the predictability of their meals (F=0.09; d.f.= 1,28; P=O.77) (Table 2).

4. Discussion

Our findings show that meals fed to chimpanzees on a more unpredictable schedule may alter behavior in a species-typical direction, and by that criterion, promote well-being. However, the only behavior category that showed this readily was inactivity; abnormal behavior showed a trend in the same direction. The effect on abnormal behavior was somewhat weak so the study should be replicated with other chimpanzees who exhibit abnormal behavior more frequently. Abnormal behavior in this study consisted mostly of

M.A. Bloomsmith, S.P. L.ambeth /Applied Animal Behaviour Science 44 (1995) 65-74 71

coprophagy and feces manipulation which are fairly common among captive apes (Walsh et al., 1982; Capitanio, 1986) and may be related to boredom and stimulus-poor living conditions (Capitanio, 1986). In this study, coprophagy might also be elicited by hunger prior to a predictably timed meal.

The level of inactivity also rose prior to the feeding of meals at predictable times. Because many animal species have been shown to develop patterns of food-anticipatory activity involving increased arousal and activity prior to being fed meals on predictable schedules (Mistlberger, 1994), it is surprising that the opposite response was seen in chimpanzees. It seemed that the subjects were “waiting” for the meal to be fed. Increased inactivity of the animals is undesirable from a behavioral management perspective because captive primates are often inactive for greater portions of time than are their wild counterparts. Obesity is fairly common among captive apes (Brent, 1995), and offering meals at fixed times may contribute to weight problems in primates by eliciting inactive periods.

It is possible that the behavioral effects demonstrated in this study might have been more pronounced if the regular feeding of biscuits and the use of supplementary feeding enrichment devices were also fed on a schedule (i.e. predictable or unpredictable) similar to that on which the meals of fresh produce were offered.

The results of this study did not indicate major social disturbances related to the timing of meal presentation. This is in contrast to earlier findings indicating anticipatory increases in agonistic behavior within groups fed on predictable schedules (Wilson and Wilson, 1968; Wasserman and Cruikshank, 1983). One other study linked predictable timing of meal presentation with abnormal behavior. Carlstead ( 1995) found that a regular schedule for feeding zoo carnivores (bears, pumas and leopards) was associated with peak levels of some stereotypical behavior, although not all stereotypical behavior was associated with feeding. These findings should be considered in zoos that schedule meals for animals at consistent times of day to facilitate public viewing and education. Such a practice may create an undesirable situation in which the visitors are more likely to be watching the animals at times when the animals are inactive or behaving abnormally.

As described in the Methods section, some of the chimpanzees in the colony could see the food before it was distributed and responded with food vocalizations. Between this announcement of the meal and actually receiving it, the chimpanzees “celebrated”, which was described by DeWaal (1992) as including embracing, kissing, and other physical contact. DeWaal ( 1992) reported that when chimpanzees were fed immediately after their first sight of the food such that the celebration period was circumvented, there was more agonistic behavior during the meal. In this study, behavior during the period of time when the arrival of food was imminent was not analyzed, but even the subjects fed on the unpredictable schedule celebrated. That opportunity may have been important in their positive response to an unpredictable delivery of food.

Our results differ from some of the literature that relates predictable events to more positive behavioral outcomes than unpredictable events, particularly when behavioral measures are examined (Weinberg and Levine, 1980). We found no evidence that a predictable schedule of meals was preferable to promote well-being. While a variety of studies have supported the conclusion that predictable stressors are less noxious than unpredictable stressors, these studies relate to the delivery of aversive events (e.g. electric shock) rather than positive or appetitive events as studied here (Mineka and Kihlstrom, 1978; Jordan et

12 M.A. Bloomsmith, S.P. L.umbeth/Applied Animal Behoviour Science 44 (1995) 65-74

al., 1984; Mineka and Hendersen, 1985). In the current study, the delivery of meals was changed from being uncontrollable by the animals, although predictable, to uncontrollable and unpredictable. So these chimpanzees experienced the loss of a predictable event while they were consistently unable to control the delivery of meals. Our study shows that behavioral disturbance was not caused by the loss of predictability of an appetitive event.

When animals have control over the presentation of events in their environment, a variety of behavioral benefits have been demonstrated (Hanson et al., 1976; Mineka and Hendersen, 1985; Mineka et al., 1986). Other studies have shown that if there is no element of control for the subjects, then predictability can be more stressful than unpredictability (for discussion see Jordan et al., 1984). Loss of control has been shown to produce more profound disturbances than are evident in animals who never experienced the control (Hanson et al., 1976). Separations of mother and infant squirrel monkeys (Suimiri sciureus) were studied to investigate whether predictability influenced the stress shown by the monkeys in response to separation. Infants’ responses to repeated separations of either fixed (predictable) intervals or variable (unpredictable) intervals were compared. The infants showed more disturbed behavior after separations of predictable duration. Jordan et al. ( 1984) suggest that the predictable duration of the separation was more stressful because the infant subjects lacked control over the timing of the reunions with their mothers.

Jordan’s ( 1984) result and the results of the current study may be explained by recog- nizing the value of the upcoming event to the animal. Perhaps, when the upcoming event is positive in nature, such as a mother-infant reunion or the delivery of a meal, predictability in the absence of control is more aversive than unpredictability in the absence of control. If this hypothesis is correct, it would suggest that the unpredictable delivery of desirable events that are uncontrollable by the animals should be incorporated into the design of animal care routines. However, there may be conditions in which unpredictability may be more stressful for captive animals. The degree of foraging demand required under the high demand Rosenblum paradigm was much greater than that in the current study; our subjects had food (monkey biscuits) freely available much of the time. Perhaps under the level of foraging demand in the Rosenblum studies, unpredictability leads to undesirable behavioral consequences. The scheduling of animal care routines to determine conditions under which predictable and unpredictable schedules should be implemented, whether they are positive routines (e.g. feeding) or more negative events, warrant further study.

5. Conclusions

( 1) Offering meals to captive chimpanzees on a schedule that is variable and, therefore, more unpredictable may lead to reduced abnormal behavior and inactivity.

(2) Further study of the predictable nature of animal care routines is needed.

Acknowledgments

The authors thank Pat Alford, Tom Beck, Kyle Burks, Gail Laule, Caroyl Maliniemi, Adam Stone, and Bob Thurston for their contributions to this project. Animals are main-

M.A. Bloomsmith, S.P. Lambeth /Applied Animal Behaviour Science 44 (1995) 65-74 73

tained in facilities approved by the American Association for Accreditation of Laboratory Animal Care and in accordance with current United States Department of Agriculture, Department of Health and Human Services, and National Institutes of Health regulations and standards. The research project described was financially supported by the National Institutes of Health/National Center for Research Resources grants ROl-RR03578 and U42- RR03589.

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