The impact of housing on birth outcomes in breeding macaque groups across multiple research centers.

Demand for nonhuman primates in research has increased over the past several years, while nonhuman primate supply remains a challenge in the United States. Global nonhuman primate supply issues make it increasingly important to maximize domestic colony production. To explore how housing conditions across primate breeding colonies impact infant survival and animal production more broadly, we collected medical records from 7959 rhesus macaques (Macaca mulatta) and 492 pigtail macaques (Macaca nemestrina) across seven breeding facilities and used generalized mixed-effect modeling to determine prenatal and infant survival odds by housing type and group size. Infant survival odds for each housing type and group size varied for prenatal, neonatal, early infant, and late infant age groups. Odds of prenatal survival were lowest in paired indoor housing and small and medium outdoor groups. No housing type performed better than large outdoor groups for neonatal survival. Odds of early infant survival was greatest in indoor and mixed indoor/outdoor housing compared to large outdoor enclosures. Large outdoor housing was associated with higher survival odds for late infant survival compared to small and medium outdoor housing. These results may influence housing choices at macaque breeding facilities hoping to maximize infant success, although there are relative care costs, the promotion of species-typical behaviors, and infrastructure factors to also consider. Our study used an interinstitutional collaboration that allowed for the analysis of more infant macaque medical records than ever before and used the broad variations across the seven national primate research centers to make the results applicable to many other facilities housing macaques.

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.

Primatology in zoos: Studying behavior, cognition, and welfare.

Primatological research in zoos is increasing globally. Such research allows scientists to study primate biology, behavior, and cognition while helping to advance the welfare of captive primates. Moreover, zoos welcome millions of visitors annually, which creates unique opportunities for public engagement with this research. Reflecting the importance of zoos in the field of primatology, the articles in this special issue showcase the range of primatological research currently being conducted in zoos around the world. With this special issue, I have chosen to focus on research examining primate behavior and cognition, addressing both basic and applied questions. The articles included in this special issue also highlight the array of technologies and methods being used to study zoo-housed primates. While zoos house a variety of primate species, potentially enabling the testing of under-studied species or widescale comparative research, great apes are disproportionately represented in current zoo-based research. Thus, while an interest in conducting research with primates in zoos continues to grow, there are still opportunities to increase the breadth and diversity of this study.

Nonhuman primate abnormal behavior: Etiology, assessment, and treatment.

Across captive settings, nonhuman primates may develop an array of abnormal behaviors including stereotypic and self-injurious behavior. Abnormal behavior can indicate a state of poor welfare, since it is often associated with a suboptimal environment. However, this may not always be the case as some behaviors can develop independently of any psychological distress, be triggered in environments known to promote welfare, and be part of an animal's coping mechanism. Furthermore, not all animals develop abnormal behavior, which has led researchers to assess risk factors that differentiate individuals in the display of these behaviors. Intrinsic risk factors that have been identified include the animal's species and genetics, age, sex, temperament, and clinical condition, while environmental risk factors include variables such as the animal's rearing, housing condition, husbandry procedures, and research experiences. To identify specific triggers and at-risk animals, the expression of abnormal behavior in captive nonhuman primates should be routinely addressed in a consistent manner by appropriately trained staff. Which behaviors to assess, what assessment methods to use, which primates to monitor, and the aims of data collection should all be identified before proceeding to an intervention and/or treatment. This article provides guidance for this process, by presenting an overview of known triggers and risk factors that should be considered, steps to design a comprehensive evaluation plan, and strategies that might be used for prevention or treatment. It also outlines the tools and processes for assessing and evaluating behavior in an appendix. This process will lead to a better understanding of abnormal behavior in captive primate colonies and ultimately to improved welfare.

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.

The application of noninvasive, restraint-free eye-tracking methods for use with nonhuman primates.

Over the past 50 years there has been a strong interest in applying eye-tracking techniques to study a myriad of questions related to human and nonhuman primate psychological processes. Eye movements and fixations can provide qualitative and quantitative insights into cognitive processes of nonverbal populations such as nonhuman primates, clarifying the evolutionary, physiological, and representational underpinnings of human cognition. While early attempts at nonhuman primate eye tracking were relatively crude, later, more sophisticated and sensitive techniques required invasive protocols and the use of restraint. In the past decade, technology has advanced to a point where noninvasive eye-tracking techniques, developed for use with human participants, can be applied for use with nonhuman primates in a restraint-free manner. Here we review the corpus of recent studies (N=32) that take such an approach. Despite the growing interest in eye-tracking research, there is still little consensus on "best practices," both in terms of deploying test protocols or reporting methods and results. Therefore, we look to advances made in the field of developmental psychology, as well as our own collective experiences using eye trackers with nonhuman primates, to highlight key elements that researchers should consider when designing noninvasive restraint-free eye-tracking research protocols for use with nonhuman primates. Beyond promoting best practices for research protocols, we also outline an ideal approach for reporting such research and highlight future directions for the field.

Problem solving flexibility across early development.

Cognitive flexibility allows individuals to adapt to novel situations. However, this ability appears to develop slowly over the first few years of life, mediated by task complexity and opacity. We used a physically simple novel task, previously tested with nonhuman primates, to explore the development of flexible problem solving in 2-, 3-, and 4-year-old children from a developmental and comparative perspective. The task goal was to remove barriers (straws) from a clear tube to release a ball. The location of the ball, and therefore the number of straws necessary to retrieve it, varied across two test phases (four of five straws and two of five straws, respectively). In Test Phase 1, all children retrieved the ball in Trial 1 and 83.61% used the most efficient method (removing only straws below the ball). Across Phase 1 trials, 4-year-olds were significantly more efficient than 2-year-olds, and solve latency decreased for all age groups. Test Phase 2 altered the location of the ball, allowing us to explore whether children could flexibly adopt a more efficient solution when their original (now inefficient) solution remained available. In Phase 2, significantly more 4-year-olds than 2-year-olds were efficient; the older children showed greater competency with the task and were more flexible to changing task demands than the younger children. Interestingly, no age group was as flexible in Phase 2 as previously tested nonhuman primates, potentially related to their relatively reduced task exploration in Phase 1. Therefore, this causally clear task revealed changes in cognitive flexibility across both early childhood and species.

User innovation: a novel framework for studying animal innovation within a comparative context.

Much work has been dedicated to defining and describing animal innovation. Despite this, efforts to compare human and animal innovation have been hindered by perceived fundamental differences between how, and why, humans and animals innovate. Furthermore, there is not a useful framework for comparisons across different taxa. Here, we provide an overview of the current understanding of human 'user' innovation, provide some examples of user innovation, and highlight the parallels between animal innovation and user innovation by humans. User innovation, put simply, is the process by which people invent to satisfy their own needs, not necessarily with the aim of distributing their invention, or marketing it for profit. Thus, it is much more closely aligned to the manner in which nonhuman animals innovate. Our intention is that this discussion will help to re-frame how we consider animal innovation and foster more direct comparisons between human and animal innovation, while propagating new avenues for research, both experimental and observational.

Testing the weekend effect hypothesis: Time of day and lunar phase better predict the timing of births in laboratory-housed primates than day of week.

The weekend effect hypothesis proposes that captive primates are more likely to give birth during times of low disturbance and reduced staff activity. The hypothesis specifically predicts that laboratory-housed primates will be more likely to give birth during the weekend than weekdays when staff activity is reduced. To date, support for the weekend effect hypothesis has been mixed and based on studies with relatively few subjects. To further examine the hypothesis, we analyzed the birthing patterns of three genera of laboratory-housed primates: squirrel monkeys (Saimiri species, N = 2,090 births), owl monkeys (Aotus species, N = 479 births), and rhesus macaques (Macaca mulatta, N = 2,047 births). Contrary to predictions derived from the weekend effect hypothesis, the frequencies of births during weekends for all taxa were not significantly different from rates that would be expected by chance. However, while there was no variance across days of the week, all three taxa gave birth at nighttime, when staff was absent. This parallels reports of births in wild and captive monkeys, both diurnal and nocturnal, which are more likely to give birth during the night; plausibly a time when the environmental and social disturbance is lowest and the mother is safest to bond with her newborn infant. As all births occurred at night, we also explored the relationship between the lunar cycle and the timing of births timing. While the diurnal primates (i.e., Saimiri and Macaca) were no more likely to give birth on "bright" nights than "dark" nights, owl monkeys (Aotus) had a much higher frequency of births on bright nights than darker ones, and at rates that deviated from chance. Our data provide a more detailed understanding on how the environment may influence captive monkey births but do not support the oft-cited weekend effect hypothesis.

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.

Chimpanzees demonstrate individual differences in social information use.

Studies of transmission biases in social learning have greatly informed our understanding of how behaviour patterns may diffuse through animal populations, yet within-species inter-individual variation in social information use has received little attention and remains poorly understood. We have addressed this question by examining individual performances across multiple experiments with the same population of primates. We compiled a dataset spanning 16 social learning studies (26 experimental conditions) carried out at the same study site over a 12-year period, incorporating a total of 167 chimpanzees. We applied a binary scoring system to code each participant's performance in each study according to whether they demonstrated evidence of using social information from conspecifics to solve the experimental task or not (Social Information Score-'SIS'). Bayesian binomial mixed effects models were then used to estimate the extent to which individual differences influenced SIS, together with any effects of sex, rearing history, age, prior involvement in research and task type on SIS. An estimate of repeatability found that approximately half of the variance in SIS was accounted for by individual identity, indicating that individual differences play a critical role in the social learning behaviour of chimpanzees. According to the model that best fit the data, females were, depending on their rearing history, 15-24% more likely to use social information to solve experimental tasks than males. However, there was no strong evidence of an effect of age or research experience, and pedigree records indicated that SIS was not a strongly heritable trait. Our study offers a novel, transferable method for the study of individual differences in social learning.

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.

Testing differential use of payoff-biased social learning strategies in children and chimpanzees.

Various non-human animal species have been shown to exhibit behavioural traditions. Importantly, this research has been guided by what we know of human culture, and the question of whether animal cultures may be homologous or analogous to our own culture. In this paper, we assess whether models of human cultural transmission are relevant to understanding biological fundamentals by investigating whether accounts of human payoff-biased social learning are relevant to chimpanzees (Pan troglodytes). We submitted 4- and 5-year-old children (N = 90) and captive chimpanzees (N = 69) to a token-reward exchange task. The results revealed different forms of payoff-biased learning across species and contexts. Specifically, following personal and social exposure to different tokens, children's exchange behaviour was consistent with proportional imitation, where choice is affected by both prior personally acquired and socially demonstrated token-reward information. However, when the socially derived information regarding token value was novel, children's behaviour was consistent with proportional observation; paying attention to socially derived information and ignoring their prior personal experience. By contrast, chimpanzees' token choice was governed by their own prior experience only, with no effect of social demonstration on token choice, conforming to proportional reservation. We also find evidence for individual- and group-level differences in behaviour in both species. Despite the difference in payoff strategies used, both chimpanzees and children adopted beneficial traits when available. However, the strategies of the children are expected to be the most beneficial in promoting flexible behaviour by enabling existing behaviours to be updated or replaced with new and often superior ones.

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.

Chimpanzees, cooking, and a more comparative psychology.

A recent report suggested that chimpanzees demonstrate the cognitive capacities necessary to understand cooking (Warneken & Rosati, 2015). We offered alternative explanations and mechanisms that could account for the behavioral responses of those chimpanzees, and questioned the manner in which the data were used to examine human evolution (Beran, Hopper, de Waal, Sayers, & Brosnan, 2015). Two commentaries suggested either that we were overly critical of the original report's claims and methodology (Rosati & Warneken, 2016), or that, contrary to our statements, early biological thinkers contributed little to questions concerning the evolutionary importance of cooking (Wrangham, 2016). In addition, both commentaries took issue with our treatment of chimpanzee referential models in human evolutionary studies. Our response offers points of continued disagreement as well as points of conciliation. We view Warneken and Rosati's general conclusions as a case of affirming the consequent-a logical conundrum in which, in this case, a demonstration of a partial list of the underlying abilities required for a cognitive trait/suite (understanding of cooking) are suggested as evidence for that ability. And although we strongly concur with both Warneken and Rosati (2015) and Wrangham (2016) that chimpanzee research is invaluable and essential to understanding humanness, it can only achieve its potential via the holistic inclusion of all available evidence-including that from other animals, evolutionary theory, and the fossil and archaeological records.

Chimpanzee food preferences, associative learning, and the origins of cooking.

A recent report suggested that chimpanzees demonstrate the cognitive capacities necessary to understand cooking (Warneken & Rosati, 2015). We offer alternate explanations and mechanisms that could account for the behavioral responses of those chimpanzees, without invoking the understanding of cooking as a process. We discuss broader issues surrounding the use of chimpanzees in modeling hominid behavior and understanding aspects of human evolution.

Behavioral research as physical enrichment for captive chimpanzees.

In this study, we evaluated the potential for a behavioral research study, designed to evaluate chimpanzee decision-making behavior, to also encourage increased activity in a group of zoo-housed chimpanzees. For the behavioral study, the chimpanzees had to carry tokens to different locations such that they always had to travel farther to obtain a more-preferred reward. We recorded the distance travelled by each subject in each of the three phases of the 15-month study. By the final phase, the chimpanzees' rate of travel during test sessions was significantly higher compared to their baseline activity. Importantly, the chimpanzees' increase in locomotion was not dependent on their participation in the study; rate of travel was not correlated with number of tokens exchanged. However, the chimpanzees' activity returned to baseline within 2 hr of the 30-min test sessions. This study emphasizes the role that research can have in providing enrichment, the importance for long-term enrichment plans, and the essential need to evaluate the impact of research on animal participants, just as we evaluate the efficacy of enrichment strategies. Zoo Biol. 35:293-297, 2016. © 2016 Wiley Periodicals, Inc.