Chimpanzees (Pan troglodytes) in U.S. Zoos, Sanctuaries, and Research Facilities: A Survey-Based Comparison of Species-Typical Behaviors.

A survey was sent to zoos, research facilities, and sanctuaries which housed chimpanzees. Data collected included information about 1122 chimpanzees' age, sex, social group-size, rearing history, and enclosure. Respondents were also asked to indicate if certain behaviors had been observed in each chimpanzee over the prior two years. Species- typical behaviors (STBs) were queried, including copulation, tool-use, nest-building, and social grooming. Tool-use was reported present for 94.3% of the sample (n = 982), active social grooming for 85.7% (n = 1121), copulation for 68.3% (n = 863) and nest-building for 58.9% (n = 982). Of the subjects for whom we had data regarding all four STBs (n = 860), 45.6% were reported to engage in all four. Logistic regression analyses using forward Wald criteria were conducted to determine the best model for each STB based on the predictors of age, sex, rearing history, group-size, facility-type, and a sex-by-rearing interaction. The best model for copulation (χ2(6) = 124.62, p < 0.001) included rearing, group-size, facility-type, and the sex-by-rearing interaction. Chimpanzees were more likely to copulate if they were mother-reared, in larger groups, living in research facilities, and, if not mother-reared (NOTMR), more likely to copulate if they were female. The best model for tool-use retained the predictors of age category, facility-type, and sex-by-rearing (χ2(5) = 55.78, p < 0.001). Chimpanzees were more likely to use tools if they were adult, living in research facilities, and if NOTMR, were female. The best model for nest-building included facility-type and rearing (χ2(3) = 205.71, p < 0.001). Chimpanzees were more likely to build nests if they were MR and if they were living in zoos or in sanctuaries. The best model for active social grooming retained the predictors of age, sex, rearing, and type of facility (χ2(6) = 102.15, p < 0.001). Chimpanzees were more likely to engage in active social grooming if they were immature, female, mother-reared, and living in zoos. This research provides a basic behavioral profile for many chimpanzees living under human care in the United States and allows us to determine potential methods for improving the welfare of these and future chimpanzees in this population.

Weight management towards physiological and behavioral wellbeing for chimpanzees living under human care.

Across a period of 54 months, several changes were made to the feeding protocols of 32 adult chimpanzees living at the Yerkes National Primate Research Center Field Station. Before implementing any changes in diet, baseline data were collected for 6 months. During Baseline (BS), the chimpanzees received unlimited amounts of primate biscuits twice a day and a limited amount of produce as enrichment. Treatment One (T1) dietary modifications included an increased amount of vegetables, primarily leafy greens, and biscuit feedings scheduled to occur an hour after vegetables were provided to the chimpanzees. T1 lasted for 1 year. At the end of T1, most of the chimpanzees had gained weight. Treatment Two (T2) occurred over the span of 3 years, during which all the chimpanzees were switched from unlimited, group-distributed primate biscuits to individually prescribed amounts of biscuits, fed in\dividually, and increased daily feedings of leafy greens. By the end of T2, 10 of 15 chimpanzees who were overweight or obese at the start of the project were within range of ideal body condition, and 4 of the remaining 5 were improved. All the chimpanzees who started the project within ideal range were still within ideal range. Significantly more time was invested in eating, foraging, and processing food during T2 (p < .05), more appropriately replicating the natural time budget for a chimpanzee. There were not any increases in abnormal, stress-related, or agonistic behaviors as a function of dietary modifications. Inactivity, however, was significantly higher (p < .05) during the later protocol, and locomotion was concurrently lower (p < .05).

Survey of Behavioral Indices of Welfare in Research Chimpanzees (Pan troglodytes) in the United States.

Chimpanzees demand specialized housing and care and the highest degree of attention to animal welfare. The current project used a survey method to collate information on chimpanzee housing and behavioral indices of welfare across all 6 of the chimpanzee research facilities in the United States. Data were compiled on 701 chimpanzees ranging from 2 to 62 y old (mean age, 26.0 y). All chimpanzees except for one were socially housed; the median group size was 7 animals, and group sizes ranged from 1 to 14. All of the subjects had access to outdoor spaces each day. Daily access to a natural substrate in the chimpanzee's enclosure was available for 63.8% of the subjects. Overall, 94.1% of the chimpanzees used tools to acquire food, 48.1% built nests, 75.8% copulated, and 83.3% initiated grooming bouts. The following atypical behaviors were reported most often: rocking (13.0%), coprophagy (10.0%), and stereotyped behaviors other than rocking (9.4%). There was widespread evi- dence of positive animal training techniques, with nearly all (97.7%) subjects reported to generally voluntarily cooperate with shifting in their enclosure, and 72.2% were reported to present for an injection of anesthetic. We include some comparison between these findings and data describing zoo-housed chimpanzees. In addition, we discuss survey findings in reference to recommendations made by the NIH Working Group on the Use of Chimpanzees in NIH-supported Research. The current survey assessed a larger sample of chimpanzees living under human care than has been published previously. This broad analysis can help to guide future improvements in behavioral management to address behavioral problems or deficits.

Effects of sex and early rearing condition on adult behavior, health, and well-being in captive chimpanzees (Pan troglodytes).

Scientific evaluation of management strategies for captive species is part of the establishment of best practices for animal welfare. Here we report the effects of sex, rearing, and a sex-by-rearing interaction on adult, captive chimpanzees' (Pan troglodytes) behavior, health, well-being, personality, and orientation towards humans based on multiple methods (observation, animal records, and surveys). Chimpanzees raised in three conditions, mother-reared (MR), standard nursery (ST) and an experimental nursery (RC), were assessed approximately 20 years after their differential rearing experiences concluded. Sex had a significant effect on behavior towards conspecifics (aggression [M > F]; affiliation [F > M]), on abnormal behavior (rocking [M > F]), and on likelihood of incurring at least one injury (between ages 6 and 10 [M > F]). Rearing condition had a significant impact on behavior towards humans (negative solicitation [RC = ST > MR = ST]; neutral behavior [RC > ST > MR], yawning (RC = ST > MR = ST), subjective well-being (MR = ST > RC = ST), and on GI illness frequency (RC > ST = MR). Sex interacted with rearing on aggression towards humans (for males, RC > MR = ST), frequency of upper respiratory infection (URI: for males RC > MR = ST)) and likelihood of at least one URI between the ages of 11 and 15 (RC males > ST males). Our findings support the conclusion that there are long-term effects of both early rearing and sex on captive adult chimpanzee welfare.

Long-term effects of infant attachment organization on adult behavior and health in nursery-reared, captive chimpanzees (Pan troglodytes).

This research traces the long-term effects on health, well-being, personality, and behavior of adult chimpanzees as a function of their attachment to a primary human caregiver assessed when they were 1 year of age. Of the 46 chimpanzees assessed at 1 year of age, we assessed health in 43 individuals, adult behavior in 20 individuals, and adult well-being and personality in 21 individuals. Attachment disorganization was found to be a significant predictor of stereotypic rocking in adult chimpanzees, F(1, 18) = 7.50, p = .013. For those subjects (N = 24) with a full 20 years (birth through age 20 years) of health data available, both rearing experience and disorganized attachment were significant predictors of upper respiratory infection frequency, F(2, 21) = 8.86, p = .002. Chimpanzees with disorganized attachment exhibited average subjective well-being as adults, whereas chimpanzees with organized strategies exhibited higher than average subjective well-being as adults. These results support the findings of human attachment research and are in line with attachment-based predictions for chimpanzees, such that the consequences of an early history of disorganized attachment may be adverse and long lasting.

Technology at the zoo: the influence of a touchscreen computer on orangutans and zoo visitors.

A computer-controlled touchscreen apparatus (hereafter referred to as "touchscreen") in the orangutan exhibit at Zoo Atlanta provides enrichment to the animals and allows cognitive research to take place on exhibit. This study investigated the impact of the touchscreen on orangutan behavior and visibility, as well as its impact on zoo visitors. Despite previous research suggesting that providing a single computer system may negatively affect orangutan behavior, there was not a significant increase in aggression, stereotypic, or distress-related behaviors following the activation of the on-exhibit touchscreen. We also investigated the possibility that zoo visitors may be negatively affected by technology because it deviates from naturalism. However, we did not find a change in stay time or overall experience rating when the computer was turned on. This research was the first to assess visitor attitudes toward technology at the zoo, and we found that visitors report highly positive attitudes about technology for both animals and visitors. If subjects visited the exhibit when the computer was turned on, they more strongly agreed that orangutans benefit from interacting with computerized enrichment. This study is the first investigation of an on-exhibit touchscreen in group-housed apes; our findings of no negative effects on the animals or zoo visitors and positive attitudes toward technology suggest a significant value of this practice.

The use of technology to enhance zoological parks.

Technology can be used in a zoological setting to improve visitor experience, increase research opportunities, and enhance animal welfare. Evaluating the quality of these technological innovations and their use by nonhuman and human counterparts is a critical part of extending the uses of technology to enhance animal welfare and visitor experience at zoological parks. Survey data from a small sample of institutions housing primates suggest that computers, television, radio, and sprinklers are the most prevalent types of technological enrichment currently used. Survey respondents were positive about the technology implemented, stating a desire to increase its use.

Habituation and desensitization as methods for reducing fearful behavior in singly housed rhesus macaques.

Operant conditioning using positive reinforcement techniques has been used extensively in the management of nonhuman primates in both zoological and laboratory settings. This research project was intended to test the usefulness of counter-conditioning techniques in reducing the fear-responses of singly housed male rhesus macaques living in the laboratory environment. A total of 18 male rhesus macaques (Macaca mulatta) were selected for this project and randomly assigned to one of three groups: a desensitization training group, a husbandry training group, or a control group. Behavioral data were collected before and after a 6 weeks training and/or habituation period during which the first two groups received a total of 125 min of positive reinforcement training (and also were assumed to undergo habituation to the environment) and the control group experienced only simple habituation to the environment. Based on a Wilcoxon Matched-Pairs Sign Test, we found that a significant proportion of animals exposed to desensitization training showed a reduction in the rate at which they engaged in cringing toward humans (exact significance=0.016, one-tailed, N-ties=6), cringing in general (exact significance=0.016, one-tailed, N-ties=6), and in stress-related behaviors (exact significance=0.016, one-tailed, N-ties=6). This was not the case for animals exposed to basic husbandry training or animals in the control group. A significant proportion of desensitization-exposed animals also showed a reduction in the duration of time spent cringing toward humans (exact significance=0.016, one-tailed, N-ties=6), but not in cringing behaviors in general or in stress-related behaviors. There were not a significant proportion of animals in either the husbandry training group or the control group that showed a decrease in duration of these behaviors. Results of this study could enhance both laboratory animal welfare and laboratory animal research, and could be a first step in developing techniques for reducing fearful behavior in rhesus monkeys in the laboratory environment.

Systematic investigation of the stability of food preferences in captive orangutans: implications for positive reinforcement training.

Using preference-assessment tests with humans in conjunction with behavioral modification sessions has been a regular component of almost all operant conditioning programs with mentally challenged humans. This has been very effective in improving the efficiency of behavioral training in these settings and could be similarly effective in zoological and research environments. This study investigated the preferences of 9 captive orangutans for different food items. The study used a pairwise presentation to record each nonhuman animal's preferences for 5 different foods on 6 different occasions over the course of 6 months. Results of a Friedman's 2-way ANOVA indicated that the orangutans showed a clear overall preference for apple. However, there was significant variability among different orangutans in preference ranking for the 5 foods, as shown by a Kendall's tau. In addition, there was variability in preference rankings across time for each orangutan. Because the orangutans' preferences change over time and vary according to individual, regular assessments should identify items to be used as rewards in behavioral husbandry training or as part of feeding enrichment strategies.