The Use of Guanfacine to Mediate Anxiety-related Reactivity and Reduce Associated Agonistic Behavior in Two Pigtail Macaques (Macaca nemestrina).

Guanfacine, an α2 adrenoceptor agonist, has been used to successfully treat self-injurious behavior in nonhuman primates, including macaques (Macaca mulatta) and baboons (Papio anubis). It does so by facilitating a correction to the dopaminergic system that mediates a reduction in impulsivity and reactivity. Given this, we assessed the potential efficacy of guanfacine to treat socially directed agonistic behavior in primates with an apparent reactive behavioral phenotype. We present data from 2 pigtail macaques (Macaca nemestrina): an intact adult male housed in a breeding group, and an experimentally naive adult female living in a research setting with her social partner. Baseline behavioral assessments suggested that both macaques showed extreme responses to external stressors that triggered them to aggress social partners often leading to wounding that required veterinary intervention. Both animals were tracked during the course of 1 y. Once treated regularly with guanfacine, both animals showed significant reduction in their agonistic behavior and the rate at which they wounded other animals. Indeed, in the year since the female has been treated with guanfacine she has never wounded her cagemate. By collecting regular and detailed behavioral observations on the male in the breeding colony, we were able to identify triggers for his aggression and to track the behavioral changes evidenced after guanfacine treatment. These data supported our hypothesis that his aggression reflected extreme reactivity to external stressors, rather than general anxiety. Importantly, we saw only a limited and short-lived reduction in the male's affiliative behavioral rates, and thus guanfacine had no sedative effect, but did successfully reduce his reactivity and resultant agonism and wounding.

In search of animal normativity: a framework for studying social norms in non-human animals.

Social norms - rules governing which behaviours are deemed appropriate or inappropriate within a given community - are typically taken to be uniquely human. Recently, this position has been challenged by a number of philosophers, cognitive scientists, and ethologists, who have suggested that social norms may also be found in certain non-human animal communities. Such claims have elicited considerable scepticism from norm cognition researchers, who doubt that any non-human animals possess the psychological capacities necessary for normative cognition. However, there is little agreement among these researchers about what these psychological prerequisites are. This makes empirical study of animal social norms difficult, since it is not clear what we are looking for and thus what should count as behavioural evidence for the presence (or absence) of social norms in animals. To break this impasse, we offer an approach that moves beyond contested psychological criteria for social norms. This approach is inspired by the animal culture research program, which has made a similar shift away from heavily psychological definitions of 'culture' to become organised around a cluster of more empirically tractable concepts of culture. Here, we propose an analogous set of constructs built around the core notion of a normative regularity, which we define as a socially maintained pattern of behavioural conformity within a community. We suggest methods for studying potential normative regularities in wild and captive primates. We also discuss the broader scientific and philosophical implications of this research program with respect to questions of human uniqueness, animal welfare and conservation.

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.

Behavioral Evaluation of Laboratory-housed Ferrets (Mustela Putorius Furo) in Different Enclosure Sizes.

The domestic ferret (Mustela putorius furo) is a common research model for infectious disease and behavioral studies. Ferrets are social animals that are commonly pair-housed. The United States has no species-specific regulatory standards for housing ferrets. Optimal enclosure dimensions have also not been investigated in this species, and cage sizes reported in the literature vary. Adequate space is an important animal welfare consideration, as smaller cages have been linked to increased incidence of stress- or boredom-related behaviors in some species. Here, we evaluated activity budget and space utilization in 2 different enclosure sizes for pair-housed female ferrets (n = 12). Single cages measured 78.7×78.7×45.7cm; double cages were comprised of 2 single cages connected by a short tunnel measuring 17.8 cm. Three pairs of ferrets were housed in each cage size and continuous video recordings were captured for 2 wk prior to crossover to the other cage size. The overall activity budget was similar between groups, with the predominant behavior being inactivity (89%). Stereotypic behaviors, such as cage biting or escape attempts, were infrequent (<0.1%) in both groups. Ferrets in double cages remained in the same cage as their partner 96% of the time, suggesting that social support is very valuable. Our results suggest that ferrets in both cage sizes experienced satisfactory welfare conditions. Our findings also suggest that while cage size is not the only determinant of conspecific aggression, larger cages may be an effective intervention to ameliorate aggression in certain ferrets based on signalment or behavioral history, with particular utility as a potential alternative to re-pairing or single-housing. This study provides valuable information to guide animal care and use programs regarding appropriate ferret housing.

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.

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.

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.

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.

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.

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 zone of latent solutions and its relevance to understanding ape cultures.

The zone of latent solutions (ZLS) hypothesis provides an alternative approach to explaining cultural patterns in primates and many other animals. According to the ZLS hypothesis, non-human great ape (henceforth: ape) cultures consist largely or solely of latent solutions. The current competing (and predominant) hypothesis for ape culture argues instead that at least some of their behavioural or artefact forms are copied through specific social learning mechanisms ("copying social learning hypothesis") and that their forms may depend on copying (copying-dependent forms). In contrast, the ape ZLS hypothesis does not require these forms to be copied. Instead, it suggests that several (non-form-copying) social learning mechanisms help determine the frequency (but typically not the form) of these behaviours and artefacts within connected individuals. The ZLS hypothesis thus suggests that increases and stabilisations of a particular behaviour's or artefact's frequency can derive from socially-mediated (cued) form reinnovations. Therefore, and while genes and ecology play important roles as well, according to the ape ZLS hypothesis, apes typically acquire the forms of their behaviours and artefacts individually, but are usually socially induced to do so (provided sufficient opportunity, necessity, motivation and timing). The ZLS approach is often criticized-perhaps also because it challenges the current null hypothesis, which instead assumes a requirement of form-copying social learning mechanisms to explain many ape behavioural (and/or artefact) forms. However, as the ZLS hypothesis is a new approach, with less accumulated literature compared to the current null hypothesis, some confusion is to be expected. Here, we clarify the ZLS approach-also in relation to other competing hypotheses-and address misconceptions and objections. We believe that these clarifications will provide researchers with a coherent theoretical approach and an experimental methodology to examine the necessity of form-copying variants of social learning in apes, humans and other species.

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.

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.

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.

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.