A comparative study of the variety and complexity of object manipulation in captive chimpanzees (Pan troglodytes) and bonobos (Pan paniscus)

Four types of specific objects: wooden spoons, metal bowls, plastic boxes, and cotton towels were introduced in a similar setting to two captive groups of different species in the genusPan, the bonobo and the chimpanzee. In total, 582 unique manipulation forms were distinguished by a set of variables: types of objects, motor patterns, body-parts used, the number of objects manipulated, and types of orienting manipulation. In sum, chimpanzees and bonobos were not so different in the variety and the complexity of object manipulation forms. However, comparison of the two species revealed significant differences as follows: (1) chimpanzees preferred to use only one hand during manipulation of both single- and multiple-objects, whereas in the case of multiple-objects bonobos used both hands significantly more often; (2) chimpanzees performed more orienting manipulations in single-object manipulations than did bonobos, whereas the reverse was the case in multiple-object manipulations; and (3) chimpanzees' object manipulations were overall more substrate-oriented than were bonobos'. The factors producing these differences are discussed in relation to positional behaviors and habitual tool use in the two species.     

Evaluation of a chimpanzee enrichment enclosure

A large, three-part playground for captive chimpanzees was constructed and evaluated in terms of area use and behavior changes. Comparative behavioral samples were obtained on 38 subjects in the existing indoor-outdoor run and in the enclosure. The chimpanzees used the inside run, connective chute, concrete slab, and grass areas most. Activity and environmental manipulation increased in the enclosure while abnormal and self-directed behaviors decreased.     

Successful feeding enrichment for captive chimpanzees

An analysis of a feeding enrichment program for captive chimpanzees was completed to determine the effects of that program on the incidence of agonistic and abnormal behaviors by using 41 adult chimpanzees in six social groups. Four feeding enrichment procedures were implemented simultaneously in the experimental phase of this ABA design study. The procedures were planned to elicit time-consuming, noncompetitive feeding, theorizing a consequent reduction in agonism and detrimental abnormal behaviors typically occurring in captive chimpanzees. The 270 hours of data were collected over a 6-month period. A multivariate analysis of variance result supported the hypothesis, as the barrage of feeding enrichment techniques significantly reduced agonism and abnormal behaviors. This study's significance lies in its application of the scientific method to improving the husbandry of captive primates.     

Frequency of removal movements during social versus self-grooming among wild chimpanzees

Grooming was observed in 11 wild chimpanzees (Pan troglodytes schweinfurthii) in Mahale, Tanzania, and the number of removal and stroke movements and grooming duration were recorded. Removal movements were more frequent during social grooming than during self-grooming. Chimpanzees used one or both hands for grooming, and grooming using both hands was more efficient for removing small objects. Due to physical constraints, self-grooming of the arms was almost always done using only one hand. The removal movement frequency during arm grooming was lower when self-grooming than when grooming another. They were more likely to use both hands during grooming another than during self-grooming, and fewer physical constraints during social grooming enabled a higher level of hygienic grooming.     

Advanced age influences chimpanzee behavior in small social groups

Management strategies for captive chimpanzees (Pan troglodytes) must begin to take into account the increasing age of the captive chimpanzee population. This study represents a baseline assessment of the relationship between advancing age and behavior among male and female chimpanzees living in pairs and trios in indoor/outdoor runs. Data collected on 14 old individuals (30–44 years old) and 20 younger adult individuals (11–22 years old) totaled 240 hours. Levels of agonistic and affiliative social behavior, non‐social activity, abnormal behaviors, and behavioral indicators of anxiety were evaluated. In the same captive setting, the behavior of old chimpanzees was significantly different from younger chimpanzees. Old chimpanzees showed less aggression and moved about their enclosures less. Old females behaved submissively more often than younger adult females; the reverse was found among males. However, affiliative social behavior occurred at similar levels in old and younger adult chimpanzees, implying continued need for social housing with advancing age. The effect of enrichment devices may differ for aged female chimpanzees, given their submissiveness and the lower levels of object manipulation found in aged subjects. These results suggest that aging in chimpanzees may be accompanied by altered patterns of social interaction, requiring careful attention to the compatibility of social partners. Zoo Biol 19:111–119, 2000. © 2000 Wiley‐Liss, Inc.     

Assessing the effects of cognitive experiments on the welfare of captive chimpanzees (Pan troglodytes) by direct comparison of activity budget between wild and captive chimpanzees

We investigated the effects of cognitive experiments by direct comparison of activity budgets between wild and captive chimpanzees. One goal of captive management is to ensure that the activity budgets of captive animals are as similar as possible to those of their wild counterparts. However, such similarity has rarely been achieved. We compared the activity budget among three groups of chimpanzees: wild chimpanzees in Bossou (Guinea, n = 10), and captive chimpanzees who participated in cognitive experiments (experimental chimpanzees, n = 6) or did not participate in the experiments (nonexperimental chimpanzees, n = 6) at the Primate Research Institute (Japan). The experimental chimpanzees voluntarily participated in computer‐controlled cognitive tasks and small pieces of fruits were provided as rewards. The data from captivity were obtained on the experimental days (weekdays) and nonexperimental days (weekends). In both study sites, we followed each chimpanzee from about 7 a.m. until the time when chimpanzees started to rest in the evening. The behaviors were recorded every 1 min. The results showed that on weekdays, feeding time and resting time of the experimental chimpanzees were almost the same as those of wild chimpanzees. However, for the nonexperimental chimpanzees, feeding time was significantly shorter and resting time was longer than those of the wild chimpanzees. In contrast, no difference was found in feeding time or resting time of the two groups of captive chimpanzees on weekends. The results suggested that the cognitive experiments worked as an efficient method for food‐based enrichment. Am. J. Primatol. 73:1231–1238, 2011. © 2011 Wiley Periodicals, Inc.     

Responses to a snake model in captive crab-eating macaques (Macaca fascicularis) and captive tufted capuchins (Cebus apella)

The responses to a model snake in captive crab-eating macaques (Macaca fascicularis) and captive tufted capuchins (Cebus apella) were investigated. In both species the amount of fear behavior was higher in the presence of the model than during baseline conditions. Unlike the macaques, in the capuchins the frequency of these behaviors decreased across trials. In the two species the amount of explorative and manipulative behaviors and the use of space were also different. Unlike macaques, all capuchins manipulated the objects available in the testing room, and three subjects contacted the apparatus by using objects. Macaques did not show significant preferences for any particular part of the testing room. In both conditions, capuchins used the floor more than macaques did. Further, capuchins increased the use of the floor across experimental trials. Latency to reach the floor was higher in macaques than in capuchins. When on the floor, capuchins spent most of the time close to the snake apparatus. It is proposed that the behavioral differences between capuchins and macaques in the responses to a potential predator indicate that capuchins have a greater propensity to explore and to contact the novel stimulus directly, or by means of objects, than macaques do. These tendencies may lead to the exploitation of novel features in the environment.     

Environmental enrichment to address behavioral differences between wild and captive black-and-white ruffed lemurs (Varecia variegata)

I compared the behaviors of wild Varecia variegata living in a Malagasy rain forest with those of caged groups living in zoos in the United Kingdom in order to design environmental enrichment to encourage more natural behaviors. Comparisons were made between wild and captive animals in terms of activity budgets (instantaneously sampled at 1-min intervals) and social and solitary behaviors, which were continuously recorded for focal individuals. I followed the same sampling protocol during behavioral enrichment experiments, with additional monitoring of the amount and type of food consumed, and with more detailed observations of feeding behavior. No significant differences were found in resting or moving between wild and captive V. variegata. However, captive V. variegata spent more time on self-grooming and social behaviors, and less time feeding than wild V. variegata. There was also a lack of manual manipulation of food items. Behavioral enrichment experiments were carried out in which whole rather than chopped fruit was provided and presented in a more naturalistic manner. With this method of dietary presentation, manual manipulation of dietary items increased. Time spent feeding also increased significantly. Captive conservation breeding programs should not be wholly concerned with maintaining a diverse gene pool-they should also be concerned with conserving species-typical behaviors, especially if they are to produce behaviorally intact captive animals that can be reintroduced to the wild with minimal training, financial resources, and loss of individuals.     

Abnormal behaviors,with a special focus on rocking,and reproductive competence in a large sample of captive chimpanzees (Pan troglodytes)

Chimpanzees (Pan troglodytes) are endangered in the wild and may no longer be imported into the United States. Of those animals presently in captivity, candidates for breeding programs must be identified to insure a self-sustaining captive population. Some have suggested that poor reproductive performance might be linked to the performance of abnormal behaviors. In Study 1, three institutions housing breeding colonies of chimpanzees (86 males, 103 females) surveyed their animals for abnormal behaviors, copulatory performance, and, for females, maternal competence. In neither sex was there a positive association between absence of copulation and the presence of any of 18 forms of abnormal behavior. No one abnormal behavior was positively associated with inadequate maternal performance. Contrary to expectations, in both sexes (significantly for females), copulators exhibited more forms of abnormal behaviors than did noncopulators. In contrast, good mothers did show slightly fewer different forms of abnormal behaviors than did inadequate mothers. No specific combination of abnormal behaviors was associated with lack of copulatory performance in either sex or with inadequacy of maternal behavior. Significant sex differences occurred only in 2 of the 18 abnormal behaviors (coprophagy and self-clinging), both with females showing the higher prevalence. In Study 2, the rate of rocking in 5 male and 14 female chimpanzees at the Primate Foundation of Arizona was found to be relatively high among some reproductively competent subjects. Some rocking had forms and contexts indicative of aggressive displays. We conclude that chimpanzees should not be disregarded as potential breeders or as candidates for resocialization and breeding programs solely because they exhibit abnormal behaviors. Anyone involved in assessing well-being needs to be aware of individual differences among animals in the stimuli that may elicit rocking behavior. If they are strangers, they may elicit display rocking which does not indicate a lack of well-being. © 1992 Wiley-Liss, Inc.     

Coyote Investigative Behavior Following Removal of Novel Stimuli

ABSTRACT Because coyotes (Canis latrans) show an aversion to novel objects, we examined the effects of the presence and removal of repellent and attractive stimuli on coyote behavior. We found a greater proportion of captive coyotes investigated 10-cm-tall cones (0.95) compared to 90-cm-tall cones (0.68) and control sites (0.81), and spent longer periods (P < 0.001 in all instances) investigating small cones (x̄ = 465 sec), compared to large cones (x̄ = 212 sec) and control sites (x̄ = 45 sec). However, investigation times at sites following removal of large cones were 1.6 and 2.3 times greater than investigation times at sites following removal of small cones and the control, respectively. Results from pen studies were supported by a field study. Wild coyotes in south Texas visited 43% of small cones but did not visit large cones. Following removal of cones, visits to small cone stations decreased to 29%, whereas coyotes visited 43% of large cone stations. Thus, we observed a direct relationship between aversion toward large novel objects and subsequent attraction to sites following their removal among both captive and wild coyotes. Based upon our results, we suggest that placing large novel objects over traps that are set and removing such objects after a few days, with the subsequent addition of an olfactory attractant, may increase exploratory behavior and capture of coyotes.     

Behavioral budgets of captive sea otter mother–pup pairs during pup development

Instantaneous sampling of eight behavior categories for a captive mother sea otter (Enhydra lutris) and her four pups was conducted continuously during the first three months following each pup's birth. Initially, pup-grooming and rest occupied the largest proportion of the mother's time. Despite a steady decline in the amount of time the mother spent pup-grooming, the mother continued to groom the pup a substantial amount of time three months after the pup's birth. The proportion of time the mother spent resting, self-grooming, or swimming did not change significantly over the study period, suggesting that these behaviors are important to the mother's self-maintenance. The newborn pups' behaviors were initially limited to rest, active, and nursing, with large proportions of time spent resting and nursing. A significant increase in self-grooming occurred regularly by week 2, followed by increases in swimming (week 3), diving (week 6), and feeding (week 7). Three months after birth, the pups' behavior budgets were similar to their mother, with the exception that pups self-groomed substantially less than their mother self-groomed. The lower proportion of pup self-grooming may be due to the continued close proximity to their mother in captivity, which afforded extended association, and allowed the mother to continue to perform this complex behavior for the pup. © 1993 Wiley-Liss, Inc.     

Transfer and Acclimatization Effects on the Behavior of Two Species of African Great Ape (<Emphasis Type="BoldItalic">Pan troglodytes</Emphasis> and <Emphasis Type="BoldItalic">Gorilla gorilla gorilla</Emphasis>) Moved to a Novel and Naturalistic Zoo Environment

Studying the effects of moving animals to new enclosures is of value to both captive managers and to scientists interested in the complex interplay between environment and behavior. Great apes represent some of the greatest challenges in this regard. Given the cognitive sophistication of these species and the substantial investments in new primate facilities, these investigations are particularly important. Using post-occupancy evaluation (POE) methodology, we compared behavior exhibited by chimpanzees (Pan troglodytes) and gorillas (Gorilla gorilla gorilla) in indoor hardscape-type exhibits to behavior of the same individuals in new naturalistic enclosures with outdoor access. In the new facility, chimpanzees showed decreases in the frequency of abnormal behaviors and visual monitoring of humans (attention behaviors) whereas gorillas exhibited reduced agonism as well as decreased attention behaviors. Both gorillas and chimpanzees demonstrated higher rates of inactivity after transfer to the new facility. All subjects in addition demonstrated transitory changes in behavior after the move to the new facility (higher rates of scratching in yr 1 than in subsequent years), indicating a period of acclimatization. Seasonal effects on feeding behavior and activity levels (both species were more active in the winter) were evident as well. The results indicate that behavioral adjustment to a new facility is an extended process for both species and that seasonal effects should be considered in longitudinal analyses of acclimatization. Behavioral patterns supported the benefits of naturalistic, functional exhibit spaces and the utility of post-occupancy evaluations in assessing captive animal welfare.     

Response to novel food in infant chimpanzees: Do infants refer to mothers before ingesting food on their own?

We investigated infant response toward novel food in captive chimpanzees under the condition in which they can explore such items freely together with their mother. Infants first approached novel foods rather than familiar ones when presented simultaneously. However, they did not ingest novel food immediately, but always sniff-licked it first. Infants tended to pay attention to their mothers before mouthing or ingesting novel foods themselves, but never did so with familiar ones. In response to the infant's activity, mother chimpanzees were tolerant rather than actively interfering. Those results imply that chimpanzee infants respond to novel foods in a neophobic way and refer to their mother for some kind of cue before attempting to ingest them.     

Chimpanzee (Pan troglodytes) responses to caregiver use of chimpanzee behaviors

The relationships between captive primates and their caregivers are critical ones and can affect animal welfare. Friendly relationships can improve quality of life; adversely, agonistic relationships can decrease quality of life. Caregivers in and of themselves should not be stressful to their charges, instead the caregivers' behaviors and the nature of their interactions with captive primates is likely the basis for the stress. One method to promote positive relationships in the captive environment is for caregivers to employ species‐specific behaviors in their interactions with their charges. This study tested the effect of caregivers' use of these behaviors with chimpanzees at The Zoo Northwest Florida in Gulf Breeze. The chimpanzee participants were three males. Data collection occurred during typical interactions between the human participants and the chimpanzees. Some days the caregiver presented chimpanzee behaviors and vocalizations (CB—Chimpanzee Behavior Condition) in the data collection interactions with the chimpanzees. On other days the caregiver presented human behaviors and used speech (HB—Human Behavior Condition) in the interactions with the chimpanzees. The interactions were videotaped. Data coders recorded the behavioral contexts for each chimpanzee as they occurred on the videotape and the time that each context began. Overall they engaged in significantly more friendly behaviors such as play in CB than in HB. They were significantly less interactive in HB than CB. Caregivers should understand and employ species‐specific interactions with chimpanzees to promote friendly interactions and animal welfare. Zoo Biol 27:345–359, 2008. © 2008 Wiley‐Liss, Inc.     

Responses to novel foods in captive chimpanzees

Hesitancy to eat novel foods hampers the immediate enlargement of the diet but serves to limit the risk of ingesting toxic foods. Neophobia has been systematically investigated in only a few primate species, in which it appears to be affected by social influences. Surprisingly, little is known about neophobia in chimpanzees. We studied the response of eight adult captive chimpanzees to 16 foods (foods commonly eaten by humans and never tasted before by chimpanzees). Each novel food was presented twice to the chimpanzee by a familiar or an unfamiliar human. Between the two trials the human ate the food face to face with the chimpanzee (demonstration). Results showed that some foods were almost unanimously accepted, whereas others were not. Moreover, there were marked interindividual differences in food acceptance and consumption; chimpanzees ranged from being almost completely neophobic to accepting almost all foods. Familiarity with the human and the human's demonstration did not affect responses to the foods. The humans' predictions concerning the chimpanzees' acceptance of the different foods were rather good; furthermore, in seven cases out of eight the humans' preferences did not correlate with their predictions on the chimpanzees' preferences. The finding that most captive chimpanzees are initially cautious toward novel foods supports the little information there is regarding this subject in wild chimpanzees. However, the lack of influence of the humans' familiarity and demonstration on the response to food by the chimpanzees calls for more naturalistic studies, in which social influences are provided by group members. Since novel stimuli provide sensory stimulation and elicit exploration and social interest, occasional presentation of novel foods could be a promising and cheap device for feeding enrichment. Zoo Biol 21:539–548, 2002. © 2002 Wiley‐Liss, Inc.     

How Abnormal Is the Behaviour of Captive,Zoo-Living Chimpanzees?

BACKGROUND: Many captive chimpanzees (Pan troglodytes) show a variety of serious behavioural abnormalities, some of which have been considered as possible signs of compromised mental health. The provision of environmental enrichments aimed at reducing the performance of abnormal behaviours is increasing the norm, with the housing of individuals in (semi-)natural social groups thought to be the most successful of these. Only a few quantitative studies of abnormal behaviour have been conducted, however, particularly for the captive population held in zoological collections. Consequently, a clear picture of the level of abnormal behaviour in zoo-living chimpanzees is lacking. METHODS: We present preliminary findings from a detailed observational study of the behaviour of 40 socially-housed zoo-living chimpanzees from six collections in the United States of America and the United Kingdom. We determined the prevalence, diversity, frequency, and duration of abnormal behaviour from 1200 hours of continuous behavioural data collected by focal animal sampling. RESULTS, CONCLUSION AND SIGNIFICANCE: Our overall finding was that abnormal behaviour was present in all sampled individuals across six independent groups of zoo-living chimpanzees, despite the differences between these groups in size, composition, housing, etc. We found substantial variation between individuals in the frequency and duration of abnormal behaviour, but all individuals engaged in at least some abnormal behaviour and variation across individuals could not be explained by sex, age, rearing history or background (defined as prior housing conditions). Our data support a conclusion that, while most behaviour of zoo-living chimpanzees is 'normal' in that it is typical of their wild counterparts, abnormal behaviour is endemic in this population despite enrichment efforts. We suggest there is an urgent need to understand how the chimpanzee mind copes with captivity, an issue with both scientific and welfare implications.     

Uprooted trees facilitate the psychological well-being of captive chimpanzees

After the introduction of uprooted trees to their environment, the behavior of 28 socially housed, laboratory chimpanzees (Pan troglodytes) was studied for five months. Subjects used the tree during 41.9% of the data points collected during the first day trees were introduced. Thereafter, the mean for tree use dropped to 3.5% and remained fairly consistent. Immature subjects used the trees significantly more than did adult subjects, as measured by the Mann-Whitney U-test. No sex difference was detected. The trees elicited a variety of species-appropriate behaviors. Increasing the similarity between the behavior of captive and wild chimpanzees can be viewed as promoting the psychological well-being of the captive animals.     

Baboons, chimpanzees, and tools

Wild chimpanzees make and use tools with far greater frequency and variety than wild baboons. Sampling differences; differences in the sensory, motor, or cognitive capacities for skilled tool use; or environmental differences are not responsible. Fortuitous discovery of novel forms of tool behavior probably occurs as rarely among chimpanzees as among baboons. However, research on wild and captive chimpanzees reveals that the discovery is transmitted quickly among chimpanzee groups by observation learning, and thus becomes well-established in the group's behavioral repertoire. In contrast, study of captive baboons reveals that they acquire little information about tool behavior by observation. With little observation learning the behavior is not likely to be acquired by other group members since repeated independent discovery is improbable. Thus chimpanzees' more proficient tool behavior is due mainly to their greater capacity for observation learning. This suggests that the advent of hominid tool traditions was accompanied by a capacity for facile observation learning and thus, perhaps, by language ability.     

Effects of selected behavioral enrichment devices on behavior of Western Lowland Gorillas (Gorilla gorilla gorilla)

Environmental complexity plays an integral role in the activity and psychological well-being of primates. The experiment described in this article evaluates the effects of nonintrusive, inexpensive, and easily managed behavioral enrichment devices on the behavior of a group of captive Western lowland gorillas. Devices used included cardboard boxes containing food items, paper bags containing food items, burlap rags, and willow and maple browse. The enrichment devices increased foraging, social play, and solitary play behaviors. Sedentary behaviors decreased. Rags, bags, browse, and boxes did not statistically decrease the incidence of regurgitation/reingestation or coprophagy. Depending on the type of enrichment item used, the effects on agonism and manipulation of enrichment item were variable. To make informed management decisions about the psychological well-being of captive animals, it is important to objectively quantify and examine the influences on their behavior.     

Conflict management by hamadryas baboons (Papio hamadryas hamadryas) during crowding: a tension-reduction strategy

Primates change a variety of behavioral responses during short-term exposure to crowding. Under crowded conditions, rates of aggression, submissive behavior, and affiliative behavior may increase or decrease. Different patterns of change among these three categories of response have been interpreted as various coping "strategies" for managing the increased risk of conflict under crowded conditions. Grooming is of particular interest because this behavior is known to have a calming influence on the recipient and could be used to manage conflict under tense situations. A captive group of nine hamadryas baboons (Papio hamadryas hamadryas) composed of two harems was observed under short-term crowding to determine whether this species adopts conflict-management strategies similar to those described in other primates. The aggression, submission, affiliation, and displacement activities of the six adults in the group (two males and four females) were recorded, and behaviors in their small indoor quarters was compared with baseline behaviors in the outdoor section of their enclosure, which had over 10 times more space. Repeated-measures analysis of variance (ANOVA) was used to compare behavioral rates during crowding with baseline rates recorded immediately after crowding and during matched controls collected at the same time of day as the crowding sessions. Aggression and submission rates did not change significantly across conditions. Huddling together and proximity increased during crowding, and females increased grooming of their harem male during crowding. Displacement activities (e.g., pacing and self-grooming) increased during crowding, but scratching, an indicator of anxiety in primates, did not. The pattern of behavior exhibited by this group conforms to an active "tension-reduction" strategy in which animals successfully reduce the higher risk of aggression during crowding.