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.

Metabolic acceleration and the evolution of human brain size and life history.

Humans are distinguished from the other living apes in having larger brains and an unusual life history that combines high reproductive output with slow childhood growth and exceptional longevity. This suite of derived traits suggests major changes in energy expenditure and allocation in the human lineage, but direct measures of human and ape metabolism are needed to compare evolved energy strategies among hominoids. Here we used doubly labelled water measurements of total energy expenditure (TEE; kcal day(-1)) in humans, chimpanzees, bonobos, gorillas and orangutans to test the hypothesis that the human lineage has experienced an acceleration in metabolic rate, providing energy for larger brains and faster reproduction without sacrificing maintenance and longevity. In multivariate regressions including body size and physical activity, human TEE exceeded that of chimpanzees and bonobos, gorillas and orangutans by approximately 400, 635 and 820 kcal day(-1), respectively, readily accommodating the cost of humans' greater brain size and reproductive output. Much of the increase in TEE is attributable to humans' greater basal metabolic rate (kcal day(-1)), indicating increased organ metabolic activity. Humans also had the greatest body fat percentage. An increased metabolic rate, along with changes in energy allocation, was crucial in the evolution of human brain size and life history.

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.

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.

Hip extensor mechanics and the evolution of walking and climbing capabilities in humans, apes, and fossil hominins.

The evolutionary emergence of humans' remarkably economical walking gait remains a focus of research and debate, but experimentally validated approaches linking locomotor capability to postcranial anatomy are limited. In this study, we integrated 3D morphometrics of hominoid pelvic shape with experimental measurements of hip kinematics and kinetics during walking and climbing, hamstring activity, and passive range of hip extension in humans, apes, and other primates to assess arboreal-terrestrial trade-offs in ischium morphology among living taxa. We show that hamstring-powered hip extension during habitual walking and climbing in living apes and humans is strongly predicted, and likely constrained, by the relative length and orientation of the ischium. Ape pelves permit greater extensor moments at the hip, enhancing climbing capability, but limit their range of hip extension, resulting in a crouched gait. Human pelves reduce hip extensor moments but permit a greater degree of hip extension, which greatly improves walking economy (i.e., distance traveled/energy consumed). Applying these results to fossil pelves suggests that early hominins differed from both humans and extant apes in having an economical walking gait without sacrificing climbing capability. Ardipithecus was capable of nearly human-like hip extension during bipedal walking, but retained the capacity for powerful, ape-like hip extension during vertical climbing. Hip extension capability was essentially human-like in Australopithecus afarensis and Australopithecus africanus, suggesting an economical walking gait but reduced mechanical advantage for powered hip extension during climbing.

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.

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.

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.

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.

An assessment of touchscreens for testing primate food preferences and valuations.

Typically, animals' food preferences are tested manually, which can be both time-consuming and vulnerable to experimenter biases. Given the utility of ascertaining animals' food preferences for research and husbandry protocols, developing a quick, reliable, and flexible paradigm would be valuable for expediting many research protocols. Therefore, we evaluated the efficacy of using a touchscreen interface to test nonhuman primates' food preferences and valuations, adapting previously validated manual methods. We tested a nonhuman primate subject with four foods (carrot, cucumber, grape, and turnip). Preference testing followed a pairwise forced choice protocol with pairs of food images presented on a touchscreen: The subject was rewarded with whichever food was selected. All six possible pairwise combinations were presented, with 90 trials per pairing. Second, we measured how hard the subject was willing to work to obtain each of the four foods, allowing us to generate demand curves. For this phase, a single image of a food item was presented on the touchscreen that the subject had to select in order to receive the food, and the number of selections required increased following a quarter-log scale, with ten trials per cost level (1, 2, 3, 6, 10, and 18). These methods allowed us to ascertain the subject's relative preferences and valuations of the four foods. The success of this touchscreen protocol for testing the subject's food preferences, from both a practical and a theoretical standpoint, suggests that the protocol should be further validated with other foods with this subject, with other subjects, and with other test items.

A review of zoo-based cognitive research using touchscreen interfaces.

In the past few decades, there has been an increase in the number of zoo-based touchscreen studies of animal cognition around the world. Such studies have contributed to the field of comparative cognition despite the fact research has only been performed at a relatively small number of institutions and with a narrow range of species. Nonetheless, zoo-based touchscreen studies are increasingly recognized as both having the potential to be enriching for captive animals by providing them with opportunities for choice, as well as potentially being a tool with which to measure changes in welfare. Zoo-based touchscreen research on public display also has the potential to impact zoo visitors; encouraging them not only learn more about the cognitive abilities of animals, but also potentially promoting increased respect for these species. Given the lack of a comprehensive review of this scope of specialized research, and the broad potential impacts on animals and programs, here we discuss the history, implementation, and potential outcomes of touchscreen research in zoo settings.

Great ape walking kinematics: Implications for hominoid evolution.

OBJECTIVES: Great apes provide a point of reference for understanding the evolution of locomotion in hominoids and early hominins. We assessed (1) the extent to which great apes use diagonal sequence, diagonal couplet gaits, like other primates, (2) the extent to which gait and posture vary across great apes, and (3) the role of body mass and limb proportions on ape quadrupedal kinematics. METHODS: High-speed digital video of zoo-housed bonobos (Pan paniscus, N = 8), chimpanzees (Pan troglodytes, N = 13), lowland gorillas (Gorilla gorilla, N = 13), and orangutans (Pongo spp. N = 6) walking over-ground at self-selected speeds were used to determine the timing of limb touch-down, take-off, and to measure joint and segment angles at touch-down, midstance, and take-off. RESULTS: The great apes in our study showed broad kinematic and spatiotemporal similarity in quadrupedal walking. Size-adjusted walking speed was the strongest predictor of gait variables. Body mass had a negligible effect on variation in joint and segment angles, but stride frequency did trend higher among larger apes in analyses including size-adjusted speed. In contrast to most other primates, great apes did not favor diagonal sequence footfall patterns, but exhibited variable gait patterns that frequently shifted between diagonal and lateral sequences. CONCLUSION: Similarities in the terrestrial walking kinematics of extant great apes likely reflect their similar post-cranial anatomy and proportions. Our results suggest that the walking kinematics of orthograde, suspensory Miocene ape species were likely similar to living great apes, and highlight the utility of videographic and behavioral data in interpreting primate skeletal morphology.

Stillbirth rates across three ape species in accredited American zoos.

Stillbirths, or births of infants that died in the womb, represent a failure of the materno-feto-placental unit to maintain a suitable fetal environment. Typical studies of nonhuman primate (NHP) stillbirth patterns are primarily descriptive and focus on macaques (genus Macaca). Thus, less is known about other NHP species and rarer still are studies that examine possible biological factors that influence stillbirth rates across taxa. To examine possible contributors to stillbirths in great apes, we analyzed 36 years (1980-2016) of historical data documenting births of zoo-housed chimpanzees (Pan troglodytes, N = 391), western lowland gorillas (Gorilla gorilla gorilla, N = 491), and orangutans (Pongo spp, N = 307) in accredited zoological parks in the United States. The average number of births for each of the 446 mothers was 2.7, resulting in a total of 1,189 births with 143 stillbirths (12%). Stillbirths represented 12% of chimpanzee births, 13% of gorilla births, and 10% of orangutan births. We used generalized linear mixed-effects models to assess possible relationships between stillbirth likelihood and mother origin (wild- versus captive-born), age, and genus. Across taxa, older mothers were more likely to have a stillbirth (p = 0.004). While these results are likely influenced by both biological and management-related factors (e.g., selective captive breeding), they may be useful to population managers in evaluating pregnancy risks for great apes. Captive settings and archival studbook data such as these may provide a unique opportunity to further explore this topic.

A multi-institutional assessment of a short-form personality questionnaire for use with macaques.

There are two commonly-used methods for calculating primates' personality dimensions, behavioral assessments and surveys, which can be used separately or in conjunction. However, these methods have limitations. Behavioral assessments, such as the novel object test or human intruder test, often require subjects to be separated and demand highly-controlled conditions. This is likely not feasible in many zoological institutions. Furthermore, it may be difficult to replicate methods across institutions. While surveys are easier to implement, the most commonly used one - the Hominoid Personality Questionnaire (HPQ) - is long and can be time consuming to complete, especially if multiple individuals need assessing. Therefore, we developed a short-form personality questionnaire for use with macaques. We aimed to retain elements of published scales while creating a tool that would be less time consuming to complete. After creating a novel 26-item scale (28 fewer items than the HPQ), we gathered ratings for 63 Japanese macaques (Macaca fuscata) living in eight zoos accredited by the Association of Zoos and Aquariums. Using principal components analysis, we identified four components to describe the Japanese macaque personality: Openneness, Friendliness, Dominance, and Anxiety/Reactivity. While further testing is required to fully validate this scale, we tested for the convergent validity of our questionnaire by correlating the responses of a subset of the monkeys to a novel object and assessed the face validity of our scale in comparison to previously-published scales.

An evaluation of video cameras for collecting observational data on sanctuary-housed chimpanzees (Pan troglodytes).

Video cameras are increasingly being used to monitor captive animals in zoo, laboratory, and agricultural settings. This technology may also be useful in sanctuaries with large and/or complex enclosures. However, the cost of camera equipment and a lack of formal evaluations regarding the use of cameras in sanctuary settings make it challenging for facilities to decide whether and how to implement this technology. To address this, we evaluated the feasibility of using a video camera system to monitor chimpanzees at Chimp Haven. We viewed a group of resident chimpanzees in a large forested enclosure and compared observations collected in person and with remote video cameras. We found that via camera, the observer viewed fewer chimpanzees in some outdoor locations (GLMM post hoc test: est. = 1.4503, SE = 0.1457, Z = 9.951, p < 0.001) and identified a lower proportion of chimpanzees (GLMM post hoc test: est. = -2.17914, SE = 0.08490, Z = -25.666, p < 0.001) compared to in-person observations. However, the observer could view the 2 ha enclosure 15 times faster by camera compared to in person. In addition to these results, we provide recommendations to animal facilities considering the installation of a video camera system. Despite some limitations of remote monitoring, we posit that there are substantial benefits of using camera systems in sanctuaries to facilitate animal care and observational research.

Primate energy expenditure and life history.

Humans and other primates are distinct among placental mammals in having exceptionally slow rates of growth, reproduction, and aging. Primates' slow life history schedules are generally thought to reflect an evolved strategy of allocating energy away from growth and reproduction and toward somatic investment, particularly to the development and maintenance of large brains. Here we examine an alternative explanation: that primates' slow life histories reflect low total energy expenditure (TEE) (kilocalories per day) relative to other placental mammals. We compared doubly labeled water measurements of TEE among 17 primate species with similar measures for other placental mammals. We found that primates use remarkably little energy each day, expending on average only 50% of the energy expected for a placental mammal of similar mass. Such large differences in TEE are not easily explained by differences in physical activity, and instead appear to reflect systemic metabolic adaptation for low energy expenditures in primates. Indeed, comparisons of wild and captive primate populations indicate similar levels of energy expenditure. Broad interspecific comparisons of growth, reproduction, and maximum life span indicate that primates' slow metabolic rates contribute to their characteristically slow life histories.

Assessment of behavior and space use before and after forelimb amputation in a zoo-housed chimpanzee (Pan troglodytes).

Primates possess great manual dexterity, and their limbs are integral to many aspects of normal functioning (e.g., climbing, feeding). As such, the loss of a limb carries the risk of significant disability and potentially harmful impairment of species-typical functioning. Limb loss is known to occur in some wild primate populations due to entanglement in hunting snares, but can also occur in captive settings due to injury that necessitates therapeutic amputation. In this study, we conducted a detailed evaluation of the behavior, travel, and space use expressed by a female zoo-housed chimpanzee (Pan troglodytes) before and following surgical amputation of her right forelimb. Overall, our results suggest that the injury did not substantively affect her daily activities. She showed no change to her vertical space use, spending equivalent proportions of her time on the ground and high in the enclosure. There was a decrease in the frequency of locomotion on the ground (P = 0.006) but also a significant increase in the overall distance travelled (P = 0.0015) following the removal of the limb. This case study provides evidence that individual chimpanzees are able to successfully adjust to significant anatomical changes when provided adequate environments in which to stay active, and highlights the importance of an effective post-surgical monitoring period-a comprehensive recovery evaluation that includes input from both veterinary and behavioral research staff is likely to provide the most holistic assessment of animal health and long-term wellbeing. Zoo Biol. 36:5-10, 2017. © 2016 Wiley Periodicals, Inc.

Asymmetries in the production of self-directed behavior by chimpanzees and gorillas during a computerized cognitive test.

Self-directed behaviors (SDBs) are a commonly used behavioral indicator of arousal in nonhuman primates. Experimental manipulations, designed to increase arousal and uncertainty, have been used to elicit SDB production in primates. Beyond measuring rates of SDB production, researchers have also recorded their lateralized production by primates, thought to reflect laterality of hemispheric brain control and response to emotion. Although a handful of such studies exist, all have been conducted with chimpanzees. Expanding on this line of inquiry, we tested both chimpanzees (N = 3) and gorillas (N = 3) in a serial learning task presented on a touchscreen interface that incorporated both EASY (two-item list) and HARD (four-item list) versions of the task. Although SDB production by the apes did not differ across the two levels of task complexity, both species produced higher rates of SDB when they made an error, regardless of task difficulty. Furthermore, the apes made more SDB with the left hand-directed to the right side of their body (contralateral SDB) and left side of their body (ipsilateral SDB)-when they made an incorrect response. There was no difference in the rate of SDB produced with the right hand across correct compared to incorrect trials. The apes' responses reflect previous reports that show humans are quicker at selecting negative emotional stimuli when using their left, compared to their right, hand (the reverse is true for positive stimuli). However, previous work has shown that chimpanzees are more likely to produce (contralateral) SDB with their right hand when aroused and so we discuss our results in relation to these findings and consider how they relate to the 'right hemisphere' and 'valence' models of emotional processing in apes.

Atypical early histories predict lower extraversion in captive chimpanzees.

Although much research has been conducted to understand personality development in humans, there remain substantial gaps in our understanding of these processes, particularly in relation to social influences. As such, investigations into personality development in our closest living relative, the chimpanzee, may provide useful insight. We evaluated the impact of early social exposure (to both humans and conspecifics) on personality development by studying 88 chimpanzees, including former pets and entertainers, living in accredited zoos and sanctuaries. During infancy, subjects varied in the amount of time spent with conspecifics compared with humans. Caregivers familiar with the chimpanzees rated them using a modified version of the Hominoid Personality Questionnaire (HPQ) and the ratings were found to have strong inter-rater reliability. We used the published structure of the HPQ to evaluate our results in relation to differences in early life experience. Chimpanzees who as infants spent less time with conspecifics were rated as lower in Extraversion later in life in comparison with chimpanzees who as infants spent more time with conspecifics. These results suggest that a broad range of social influences should be considered when evaluating the impact of early social environment on later personality expression.