Hierarchical organization of rhesus macaque behavior

Primatologists, psychologists and neuroscientists have long hypothesized that primate behavior is highly structured. However, fully delineating that structure has been impossible due to the difficulties of precision behavioral tracking. Here we analyzed a dataset consisting of continuous measures of the 3D position of fifteen body landmarks from two male rhesus macaques (Macaca mulatta) performing three different tasks in a large unrestrained environment over many hours. Using an unsupervised embedding approach on the tracked joints, we identified commonly repeated pose patterns, which we call postures. We found that macaques' behavior is characterized by 49 distinct identifiable postures, lasting an average of 0.6 seconds each. We found evidence that behavior is hierarchically organized, in that transitions between poses tend to occur within larger modules, which correspond to intuitively identifiably actions; these actions are in turn organized hierarchically. Our behavioral decomposition allows us to identify universal (cross-individual and cross-task) and unique (specific to each individual and task) principles of behavior. These results demonstrate the hierarchical nature of primate behavior and provide a method for the automated "ethogramming" of primate behavior.

Noninvasive Technologies for Primate Conservation in the 21st Century

Observing and quantifying primate behavior in the wild is challenging. Human presence affects primate behavior and habituation of new, especially terrestrial, individuals is a time-intensive process that carries with it ethical and health concerns, especially during the recent pandemic when primates are at even greater risk than usual. As a result, wildlife researchers, including primatologists, have increasingly turned to new technologies to answer questions and provide important data related to primate conservation. Tools and methods should be chosen carefully to maximize and improve the data that will be used to answer the research questions. We review here the role of four indirect methods—camera traps, acoustic monitoring, drones, and portable field labs—and improvements in machine learning that offer rapid, reliable means of combing through large datasets that these methods generate. We describe key applications and limitations of each tool in primate conservation, and where we anticipate primate conservation technology moving forward in the coming years.

Gaze-Related Activity in Primate Frontal Cortex Predicts and Mitigates Spatial Uncertainty

A remarkable feature of primate behavior is the ability to predict future events based on past experience and current sensory cues. To understand how the brain plans movements in the presence of unstable cues, we recorded gaze-related activity in the frontal cortex of two monkeys engaged in a quasi-predictable cue-conflict task. Animals were trained to look toward remembered visual targets in the presence of a landmark that shifted with fixed amplitude but randomized direction. As simulated by a probabilistic model based on known physiology/behavior, gaze end points assumed a circular distribution around the target, mirroring the possible directions of the landmark shift. This predictive strategy was reflected in frontal cortex activity (especially supplementary eye fields), which anticipated future gaze distributions before the actual landmark shift. In general, these results implicate prefrontal cortex in the predictive integration of environmental cues and their learned statistical properties to mitigate spatial uncertainty.

Behavioral Implications of the Complete Absence of Guests on a Zoo-Housed Gorilla Troop

Research conducted on the effects that zoo visitors have on primate behavior has yielded inconsistent patterns. This study aims to contribute to the growing body of literature regarding visitor effects on zoo-housed primate’s activity budgets, with the purpose of quantifying the behavioral variability under two conditions: guest presence and guest absence. Due to the COVID-19 pandemic, many zoos were closed to the public for varying lengths of time. The Buffalo Zoo was closed to guests for an 18-week period including the summer of 2020, which allowed us to effectively control for zoo guest presence. This case report compares data on the zoo’s gorilla troop from the same time period in 2019. We found inconsistent results, similar to prior studies conducted with zoo-housed gorilla troops. Most gorillas were observed foraging less and exhibiting more inactivity in 2020, whereas the adult male silverback showed the opposite pattern. Abnormal or undesirable behaviors were performed less frequently when guests were absent however, these differences were not significant. We encourage others to compare behavior patterns during the pandemic shutdown to add to our knowledge base of visitor effects. We suggest that researchers do not try and generalize their individual and troop results to the entire population of gorillas in managed care, as both intrinsic and extrinsic factors contribute to individual differences in behavioral response.

Social Network Analysis of a Chimpanzee (Pan troglodytes) Group in Captivity Following the Integration of a New Adult Member

Management of primates in captivity often presents the challenge of introducing new individuals into a group, and research investigating the stability of the social network in the medium term after the introduction can help inform management decisions. We investigated the behavior of a group of chimpanzees (Pan troglodytes) housed at Chester Zoo, UK over 12 months (divided into three periods of 4 months) following the introduction of a new adult female. We recorded grooming, proximity, other affiliative behaviors, and agonistic behaviors and used social network analysis to investigate the stability, reciprocity, and structure of the group, to examine the effect of rearing history on grooming network position and the role of sex in agonistic behavior. Both the grooming and agonistic networks correlated across all three periods, while affiliative networks correlated only between periods 2 and 3. Males had significantly higher out-degree centrality in agonistic behaviors than females, indicating that they carried out agonistic behaviors more often than females. There was no significant difference in centrality between hand-reared and mother-reared chimpanzees. Overall, the group structure was stable and cohesive during the first year after the introduction of the new female, suggesting that this change did not destabilize the group. Our findings highlight the utility of social network analysis in the study of primate sociality in captivity, and how it can be used to better understand primate behavior following the integration of new individuals.

Comparing Methods for Assessing Chimpanzee (Pan troglodytes schweinfurthii) Party Size: Observations, Camera Traps, and Bed Counts from a Savanna–Woodland Mosaic in the Issa Valley, Tanzania

Studying animal grouping behavior is important for understanding the causes and consequences of sociality and has implications for conservation. Chimpanzee (Pan troglodytes) party size is often assessed by counting individuals or extracted indirectly from camera trap footage or the number of nests. Little is known, however, about consistency across methods for estimating party size. We collected party size data for wild chimpanzees in the Issa valley, western Tanzania, using direct observations, camera traps, and nest counts over six years (2012–2018). We compared mean monthly party size estimates calculated using each method and found that estimates derived from direct observations were weakly positively correlated with those derived from camera traps. Estimates from nest counts were not significantly correlated with either direct observations or camera traps. Overall observed party size was significantly larger than that estimated from both camera traps and nest counts. In both the dry and wet seasons, observed party size was significantly larger than camera trap party size, but not significantly larger than nest party size. Finally, overall party size and wet season party size estimated from camera traps were significantly smaller than nest party size, but this was not the case in the dry season. Our results reveal how data collection methods influence party size estimates in unhabituated chimpanzees and have implications for comparative analysis within and across primate communities. Specifically, future work must consider how estimates were calculated before we can reliably investigate environmental influences on primate behavior.

Intranasal oxytocin selectively modulates the behavior of rhesus monkeys in an expression matching task

Although the neuropeptide oxytocin (OT) is thought to regulate prosocial behavior in mammals, there is considerable debate as to how intranasal OT influences primate behavior. The aim of this study was to determine whether intranasal OT has a general anxiolytic effect on the performance of rhesus monkeys tasked with matching face stimuli, or a more selective effect on their behavior towards aversive facial expressions. To this end, we developed an innovative delayed match-to-sample task where the exact same trials could be used to assess either a monkey’s ability to match facial expressions or facial identities. If OT has a general affect on behavior, then performance in both tasks should be altered by the administration of OT. We tested four male rhesus monkeys (Macaca mulatta) in both the expression and identity task after the intranasal administration of either OT or saline in a within-subjects design. We found that OT inhalation selectively reduced a selection bias against negatively valenced expressions. Based on the same visual input, performance in the identity task was also unaffected by OT. This dissociation provides evidence that intranasal OT affects primate behavior under very particular circumstances, rather than acting as a general anxiolytic, in a highly translatable nonhuman model, the rhesus monkey.