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.

A 25-Year Retrospective Review of Mortality in Chimpanzees (Pan troglodytes) in Accredited U.S. Zoos from a Management and Welfare Perspective.

Understanding causes of death allows adjustment of health management strategies for animals in managed care. From 224 documented chimpanzee deaths occurring from 1995 to 2019 in 42 accredited U.S. zoos, post-mortem records and necropsy reports were analyzed for the primary cause of death, which were available for 214 individuals. In total, 37 cases of stillbirth and neonatal deaths were assessed (16.5%); however, the focus was otherwise placed on the remaining 177 cases in which the death occurred in individuals aged greater than 1 month. There were no sex-related differences in etiology; however, age variation in the cause of death was statistically significant (p < 0.001). Elderly (35 years and older) chimpanzees tended to die of intrinsic, often degenerative, etiologies, whereas infants, juveniles, and adolescents (less than 15 years) were more likely to be involved in fatal trauma. Overall, there were 27 deaths (15.3% of all post-neonatal deaths) related to trauma and 13 of these were directly or indirectly related to conspecific aggression. Understanding causes of mortality and the interrelation with management can benefit managed populations of chimpanzees.

Familiarity mediates apes' attentional biases toward human faces.

In zoos, primates experience markedly different interactions with familiar humans, such as the zookeepers who care for them, compared with those with unfamiliar humans, such as the large volume of zoo visitors to whom they are regularly exposed. While the behaviour of zoo-housed primates in the presence of unfamiliar, and to a lesser extent familiar, humans has received considerable attention, if and how they spontaneously distinguish familiar from unfamiliar people, and the cognitive mechanisms underlying the relationships they form with familiar and unfamiliar humans, remain poorly understood. Using a dot-probe paradigm, we assessed whether primates (chimpanzees and gorillas) show an attentional bias toward the faces of familiar humans, with whom the apes presumably had a positive relationship. Contrary to our predictions, all subjects showed a significant attentional bias toward unfamiliar people's faces compared with familiar people's faces when the faces showed a neutral expression, both with and without a surgical face mask on, but no significant attentional bias when the faces showed a surprised expression. These results demonstrate that apes can spontaneously categorize humans based on familiarity and we argue that the attentional biases the apes showed for unfamiliar human faces reflect a novelty effect.

Younger generations are more interested than older generations in having non-domesticated animals as pets.

The trade and private ownership of non-domesticated animals has detrimental effects on individual animals and their wild populations. Therefore, there is a need to understand the conditions that motivate and dissuade interest in non-domesticated pet ownership. Past research has demonstrated that the way in which non-domesticated animals are portrayed in images influences the public's perception that they are suitable as pets. We conducted an online survey of people residing in the United States to investigate how viewing images that could be realistically captured in the zoo and broader tourism industries impact the degree to which people report interest in having that animal as a pet. We focused on two species, reticulated pythons (Malayopython reticulatus) and two-toed sloths (Choloepus hoffmanni), and presented each species in six different visual contexts. After viewing an image, respondents reported interest in pet ownership on a four-point Likert scale. Each species was studied separately in a between-subjects design and results were analyzed using ordinal logistic regression models. Thirty-nine percent of respondents reported interest in sloth pet ownership, and 21% reported interest in python pet ownership. However, contrary to our hypotheses, we found that viewing these species in different visual contexts did not significantly affect survey respondents' reported interest in having either species as a pet. Generation was a significant predictor of interest in both sloth and python pet ownership, with younger generations reporting more interest in having these species as pets. Male respondents reported more interest in python pet ownership, whereas there were no significant differences between genders regarding interest in sloth ownership. We consider how modern media exposure to animals in unnatural contexts may relate to the generational effect and discuss priorities for future research to better understand the development of individual interests in non-domesticated pet ownership.

The relationship between personality, season, and wounding receipt in zoo-housed Japanese macaques (Macaca fuscata): A multi-institutional study.

It is important to those managing Japanese macaques (Macaca fuscata) in captive settings to understand predictors of wounding. While studies have demonstrated that season (breeding or nonbreeding) and sex predict rates of wounding received by zoo-housed Japanese macaques, we investigated whether individual differences in personality ratings also might explain some of the observed interindividual variance in wounding. Such patterns were previously observed in rhesus macaques (M. mulatta), such that individuals rated higher on Anxiety and Confidence received greater wounding. Here, we collected wounding data over 24 months on 48 Japanese macaques from eight AZA-accredited zoos. Each macaque was also rated by keepers using a 26-item personality questionnaire. Principle components analysis of these ratings revealed four personality components: Openness, Friendliness, Dominance, and Anxiety/Reactivity. The model with the best fit revealed an interaction effect between season (breeding vs. nonbreeding) and the personality component Friendliness, such that individuals rated higher on Friendliness incurred fewer wounds in the nonbreeding season. The second-best model revealed both a main effect of the season as well as an interaction effect between season and Openness, such that macaques rated higher in Openness received more wounds in the nonbreeding season than those rated lower in Openness. Thus, as with rhesus macaques, personality mediated wounding receipt rate in Japanese macaques, although different personality components explained interindividual variance in wounding for these two species. These differences likely reflect species differences in behavior and personality structure, as well as the influence of differing management practices, highlighting the importance of species-specific approaches for captive primate care and welfare. This study provides further support for understanding primate personality to create individualized strategies for their care.

An evaluation of thermal imaging as a welfare monitoring tool for captive chimpanzees.

Among the growing list of novel tools with which to assess animal welfare is the use of thermal (infrared) imaging. The technology has already been utilized to identify emotional arousal in several nonhuman primate species, though most of these approaches have necessitated the use of relatively controlled settings. Here, we were interested to determine the feasibility of such techniques in a sanctuary setting in which chimpanzees were unrestrained and able to move freely around their enclosures. Furthermore, we sought to evaluate how such thermal images could be paired with corresponding long-term behavioral data and contribute to a multifactorial welfare monitoring system. Over a 6-month period, we simultaneously collected both behavioral and thermographic data on 29 chimpanzees living in four social groups. While we took a thermal image with every behavioral data point, we found that only a small proportion (6.38%) of the thermal images we captured were of sufficient quality to analyze. Most of these usable thermal images (55%) corresponded with a behavioral observation scored as "inactive," and thus other, less frequent behaviors are not so well represented in our final data set. From our data set, we were able to determine that nasal temperatures were relatively lower when chimpanzees were categorized in active behaviors compared to inactive behaviors, providing some validity measures to our approach. While there are other potential applications for thermal imaging in the behavioral management of chimpanzees, managers should consider the practical limitations of developing long-term welfare monitoring programs that rely on thermographic data.

Comparative survival analyses among captive chimpanzees (Pan troglodytes) in America and Japan.

Detailed, long-term datasets on the life histories of long-lived species such as great apes are necessary to understand their survival patterns but are relatively rare. Such information requires prolonged and consistent record-keeping over many generations, so for chimpanzees (Pan troglodytes), this equates to many decades of input. As life history variables can be altered by differences in environmental influences (whether natural or artificial), there is substantial value to being able to compare across populations. Here, we present the first comparative analysis of life history data for two ex situ chimpanzee populations residing in North America (1975-2020; n = 730) and Japan (1980-2020; n = 660). Overall, survival patterns were similar between regions, and the median life expectancy from birth is estimated at 35.7 (95% CI = [32.4-40.0]) years for females and 30.1 (27.3-34.3) years for males across both populations. Females who survive to their first birthday are estimated to survive 42.4 (40.0-46.3) years and males 35.5 (32.6-38.0) years. We found that birth type (wild-born or captive-born) did not influence survival patterns in either population, but there were differential effects of sex on longevity. In the America population, males had higher mortality rates than females, whereas in the Japan population we found no differences between the sexes. First year mortality did not differ between populations for males (18-20%), but for females it was lower in America (15%) compared to Japan (25%). Survival patterns of chimpanzees in the present study will be useful for future investigation into potential causes of regional differences and cross-species comparisons.

A Comparative Perspective on Three Primate Species' Responses to a Pictorial Emotional Stroop Task.

The Stroop effect describes interference in cognitive processing due to competing cognitive demands. Presenting emotionally laden stimuli creates similar Stroop-like effects that result from participants' attention being drawn to distractor stimuli. Here, we adapted the methods of a pictorial Stroop study for use with chimpanzees (N = 6), gorillas (N = 7), and Japanese macaques (N = 6). We tested all subjects via touchscreens following the same protocol. Ten of the 19 subjects passed pre-test training. Subjects who reached criterion were then tested on a standard color-interference Stroop test, which revealed differential accuracy in the primates' responses across conditions. Next, to test for an emotional Stroop effect, we presented subjects with photographs that were either positively valenced (a preferred food) or negatively valenced (snakes). In the emotional Stroop task, as predicted, the primates were less accurate in trials which presented emotionally laden stimuli as compared to control trials, but there were differences in the apes' and monkeys' response patterns. Furthermore, for both Stroop tests, while we found that subjects' accuracy rates were reduced by test stimuli, in contrast to previous research, we found no difference across trial types in the subjects' response latencies across conditions.

Evolution of water conservation in humans.

To sustain life, humans and other terrestrial animals must maintain a tight balance of water gain and water loss each day.1-3 However, the evolution of human water balance physiology is poorly understood due to the absence of comparative measures from other hominoids. While humans drink daily to maintain water balance, rainforest-living great apes typically obtain adequate water from their food and can go days or weeks without drinking4-6. Here, we compare isotope-depletion measures of water turnover (L/d) in zoo- and rainforest-sanctuary-housed apes (chimpanzees, bonobos, gorillas, and orangutans) with 5 diverse human populations, including a hunter-gatherer community in a semi-arid savannah. Across the entire sample, water turnover was strongly related to total energy expenditure (TEE, kcal/d), physical activity, climate (ambient temperature and humidity), and fat free mass. In analyses controlling for those factors, water turnover was 30% to 50% lower in humans than in other apes despite humans' greater sweating capacity. Water turnover in zoo and sanctuary apes was similar to estimated turnover in wild populations, as was the ratio of water intake to dietary energy intake (∼2.8 mL/kcal). However, zoo and sanctuary apes ingested a greater ratio of water to dry matter of food, which might contribute to digestive problems in captivity. Compared to apes, humans appear to target a lower ratio of water/energy intake (∼1.5 mL/kcal). Water stress due to changes in climate, diet, and behavior apparently led to previously unknown water conservation adaptations in hominin physiology.

Do zoo visitors induce attentional bias effects in primates completing cognitive tasks?

While previous research has focused on the impact of visitors on zoo-housed animals' behavior, here, we evaluated the impact of visitors on the performance of four zoo-housed Japanese macaques (Macaca fuscata) in a cognitive task. The macaques completed a touchscreen-based match-to-sample task in glass-sided booths at the perimeter of their enclosure, adjacent to a visitor viewing area. The task was novel to all macaques at the start of this study but over the 6-month testing period the macaques showed increased accuracy on the task, suggestive of learning. We recorded the number of visitors within the viewing area roughly every 12 trials each macaque completed. We categorized visitor counts as small (0-20), medium (21-40), and large (41-60) crowds and we considered the macaques' response latencies and accuracy by crowd size and study period (first 3 months versus second 3 months). If visitor presence negatively influenced performance, we predicted that macaques' accuracy would decrease but response times would increase with crowd size. We found effects of crowd size and study period on the macaques' accuracy. In the first period, the macaques performed at chance and accuracy did not differ across crowd categories. In the second period, the macaques' accuracy improved as compared to the first period, but their accuracy was mediated by crowd size: the macaques were significantly more accurate in the presence of small crowds than medium or large crowds. The macaques' response latencies also varied by study period and crowd size, but we found no evidence of a response-slowing effect.

Same Space, Different Species: The Influence of Exhibit Design on the Expression of Zoo-Housed Apes' Species-Typical Retiring Behaviors.

Wild chimpanzees frequently make arboreal nests, while wild lowland gorillas typically nest on the ground. We aimed to understand whether zoo-housed apes' use of elevated spaces for retiring similarly differed between species and across exhibits. Using a pre-planned exhibit switch at Lincoln Park Zoo (Chicago, USA), we compared where (elevated or terrestrial) two groups of apes (Pan troglodytes and Gorilla gorilla gorilla) performed retiring behaviors (inactive, sleeping, and nest-building behaviors). We studied a group of six chimpanzees and a group of four gorillas in two exhibits of similar size and configuration for two three-month periods (between 3 and 5 p.m.) before and after the groups switched exhibits. We predicted that chimpanzees would be more likely to retire in elevated locations compared to gorillas, irrespective of the exhibit. We found a significant effect of exhibit on where the apes retired but no effect of species, such that both species were more likely to retire in elevated locations in one exhibit but not the other. This suggests that the specific characteristics of the exhibits (e.g., number of visual barriers) influenced the expression of the apes' retiring behaviors. These findings offer further insight in how exhibit design can influence the expression of natural behaviors in these species.

A review of research in primate sanctuaries.

While non-human primate studies have long been conducted in laboratories, and more recently at zoological parks, sanctuaries are increasingly considered a viable setting for research. Accredited sanctuaries in non-range countries house thousands of primates formerly used as subjects of medical research, trained performers or personal pets. In range countries, however, sanctuaries typically house orphaned primates confiscated from illegal poaching and the bushmeat and pet trafficking trades. Although the primary mission of these sanctuaries is to rescue and rehabilitate residents, many of these organizations are increasingly willing to participate in non-invasive research. Notably, from a scientific standpoint, most sanctuaries provide potential advantages over traditional settings, such as large, naturalistic physical and social environments which may result in more relevant models of primates' free-ranging wild counterparts than other captive settings. As a result, an impressive scope of research in the fields of primate behaviour, cognition, veterinary science, genetics and physiology have been studied in sanctuaries. In this review, we examine the range and form of research that has been conducted at accredited sanctuaries around the world. We also describe the potential challenges of sanctuary-based work and the considerations that external researchers may face when deciding to collaborate with primate sanctuaries on their research projects.

Food Cleaning by Japanese Macaques: Innate, Innovative or Cultural?

Japanese macaques (Macaca fuscata) display a number of cultural behaviours including food washing, stone handling and certain grooming techniques. These are deemed cultural behaviours because it is presumed that they are socially learned and, importantly, that social learning is essential for their emergence. Recently, however, research has revealed that culturally naïve primates can re-innovate presumed cultural behaviours. These behaviours are said to fall within that species' "zone of latent solutions" (ZLS). A notable cultural behaviour of Japanese macaques is food washing, first reported by Japanese researchers studying wild Japanese macaques in the 1950s. To test whether culturally naïve Japanese macaques would spontaneously wash food and also, therefore, whether food-washing behaviour is within their ZLS, we presented 12 zoo-housed macaques with sweet potato covered in sand near a pool in their exhibit. Over 11 days we recorded the macaques' behaviour. While 11 of the 12 macaques ate the potato pieces, none washed them. However, 4 macaques cleaned their food, brushing off the sand using their hand or rubbing the potato against their body or another food item, using three distinct techniques. We found no change over time in the rate at which monkeys cleaned or consumed potato, but there was a significant positive correlation between the number of potato pieces a monkey ate and the number of cleaning behaviours performed. We conclude that, minimally, food-cleaning behaviour is within macaques' ZLS.

Sex and season predict wounds in zoo-housed Japanese macaques (Macaca fuscata): A multi-institutional study.

Japanese macaque societies are characterized by frequent intragroup conflict both in free-ranging and zoo-housed conditions. In zoos, understanding the factors that contribute to wounding is of interest because this knowledge can aid in proactive husbandry and management planning that can minimize the negative impacts wounding can have on individual welfare. This study sought to determine whether the variables sex, season and age predicted wounding rates. Data were collected for 24 months on 119 Japanese macaques living in 10 zoos, and we analyzed the contribution of variables using generalized linear mixed models. A total of 1,007 wounds were reported, and the best model included the interaction between sex and season. Follow-up analyses revealed that females incurred more wounds than males, and this sex difference was more pronounced during the breeding compared to the nonbreeding season. On average, individuals received 4.67 (±SEM: 0.55) wounds per year and 77.31% of the population incurred at least one wound in the study period. The majority of wounds were superficial and did not require veterinary intervention. Wound locations were not randomly distributed across body regions and were most often reported on the face. Finally, macaques living in larger social groups experienced more wounds, on average. This study represents the first quantification of wounding in this species and may provide insight to help inform husbandry and management strategies in zoos.

Reducing the primate pet trade: Actions for primatologists.

This commentary emerged from a panel presentation at the International Primatological Society Congress in Nairobi, Kenya, 2018. The goal was to provide regional updates on the status of primate removal from habitat countries, especially for the pet trade, and develop guidelines that could help primatologists address this critical problem. The trade in live primates includes those used as pets, in entertainment, and as subjects of biomedical experimentation, but here we focus on those primates destined for the pet trade. Such transactions are a hugely lucrative business, impacting hundreds of thousands of individuals annually and affecting the survival of wild populations. Being intimately familiar with primate social behavior, life history and biology, primatologists, whether they work with captive or wild primates, are in a unique position to understand the nature of the trade and attempt to counter its effects. In addition to updating the status of the primate pet trade, we provide recommendations that may help primatologists formulate a plan to deal, locally and regionally, with illegal trafficking in live primates. General guidelines include increasing awareness of local customs, policies and laws; developing collaborative research opportunities for local people; engaging in training/informational opportunities; and instructing on how to take action when encountering illegally-trafficked primates.

The effect of captivity on the primate gut microbiome varies with host dietary niche.

Despite careful attention to animal nutrition and wellbeing, gastrointestinal distress remains relatively common in captive non-human primates (NHPs), particularly dietary specialists such as folivores. These patterns may be a result of marked dietary differences between captive and wild settings and associated impacts on the gut microbiome. However, given that most existing studies target NHP dietary specialists, it is unclear if captive environments have distinct impacts on the gut microbiome of NHPs with different dietary niches. To begin to examine this question, we used 16S ribosomal RNA gene amplicon sequences to compare the gut microbiomes of five NHP genera categorized either as folivores (Alouatta, Colobus) or non-folivores (Cercopithecus, Gorilla, Pan) sampled both in captivity and in the wild. Though captivity affected the gut microbiomes of all NHPs in this study, the effects were largest in folivorous NHPs. Shifts in gut microbial diversity and in the relative abundances of fiber-degrading microbial taxa suggest that these findings are driven by marked dietary shifts for folivorous NHPs in captive settings. We propose that zoos and other captive care institutions consider including more natural browse in folivorous NHP diets and regularly bank fecal samples to further explore the relationship between NHP diet, the gut microbiome, and health outcomes.

Establishing an infrastructure for collaboration in primate cognition research.

Inferring the evolutionary history of cognitive abilities requires large and diverse samples. However, such samples are often beyond the reach of individual researchers or institutions, and studies are often limited to small numbers of species. Consequently, methodological and site-specific-differences across studies can limit comparisons between species. Here we introduce the ManyPrimates project, which addresses these challenges by providing a large-scale collaborative framework for comparative studies in primate cognition. To demonstrate the viability of the project we conducted a case study of short-term memory. In this initial study, we were able to include 176 individuals from 12 primate species housed at 11 sites across Africa, Asia, North America and Europe. All subjects were tested in a delayed-response task using consistent methodology across sites. Individuals could access food rewards by remembering the position of the hidden reward after a 0, 15, or 30-second delay. Overall, individuals performed better with shorter delays, as predicted by previous studies. Phylogenetic analysis revealed a strong phylogenetic signal for short-term memory. Although, with only 12 species, the validity of this analysis is limited, our initial results demonstrate the feasibility of a large, collaborative open-science project. We present the ManyPrimates project as an exciting opportunity to address open questions in primate cognition and behaviour with large, diverse datasets.

The Social Rank of Zoo-Housed Japanese Macaques is a Predictor of Visitor-Directed Aggression.

The effect that visitors have on the behavior and welfare of animals is a widely-studied topic in zoo animal welfare. Typically, these studies focus on how the presence or activity levels of visitors affect animals. However, for many species, and particularly primates, social factors, such as social rank, can also have a large impact on behavior. Here, we considered the influence of both the role of visitors (crowd size and activity levels) and rank on the occurrence of visitor-directed aggression by zoo-housed Japanese macaques (Macaca fuscata, N = 12). We conducted 52 weeks of observation (443.8 hours) of macaques living in a large outdoor habitat and recorded 1574 events of visitor-directed behavior, 94.2% of which was characterized as aggressive. We calculated rank using the Elo-rating method. GLMM comparisons indicate that rank was a significant predictor of visitor-directed aggression, with lower-ranked individuals displaying more frequent aggression towards visitors. Additionally, visitor-directed aggression differed by crowd activity levels, but not crowd size. These results support our prediction that rank is associated with differences in visitor-directed aggression, and we interpret this pattern as lower-ranking macaques redirecting aggression toward zoo visitors as safe targets. This work emphasizes how factors emanating from the zoo environment can combine with social dynamics to influence primate response to human presence in the zoo setting.

Systemic response of coated-platelet and peripheral blood inflammatory cell indices after aneurysmal subarachnoid hemorrhage and long-term clinical outcome.

PURPOSE: Post-hemorrhage period after aneurysmal subarachnoid hemorrhage (aSAH) has several systemic manifestations including prothrombotic and pro-inflammatory states. Inter-relationship between these states using established/routine laboratory biomarkers and its long-term effect on clinical outcome is not well-defined. MATERIALS AND METHODS: Retrospective analysis of prospective cohort of 44 aSAH patients. Trend of procoagulant biomarkers [coated-platelets, mean platelet volume to platelet count (MPV:PLT)] and peripheral inflammatory biomarkers [platelet-lymphocyte ratio (PLR), neutrophil-platelet ratio (NLR)] were analyzed using regression analysis. Occurrence of delayed cerebral ischemia (DCI), modified Rankin score (mRS) of 3-6 and Montreal cognitive assessment (MoCA) of <26 at 1-year defined adverse clinical outcome. RESULTS: Patients with worse mRS and MoCA score had higher rise in coated-platelet compared to those with better scores [20.4 (IQR: 15.6, 32.9) vs. 10.95 (IQR: 6.1, 18.9), p = 0.003] and [16.9 (IQR: 13.4, 28.1) vs. 10.95 (IQR: 6.35, 18.65), p = 0.02] respectively. NLR and PLR trends showed significant initial decline followed by a gradual rise in NLR among those without DCI as compared to persistent low levels in those developing DCI (0.13 units/day vs. -0.07 units/day, p = 0.06). CONCLUSIONS: Coated-platelet rise after aSAH is associated with adverse long-term clinical outcome. NLR and PLR trends show an early immune-depressed state after aSAH.