Cortisol metabolites vary with environmental conditions, predation risk, and human shields in a wild primate, Cercopithecus albogularis.

Environmental challenges are often associated with physiological changes in wildlife that allow animals to maintain homeostasis. Among these, scarcity in resources, and risks from predators, competitors, and humans can all result in psychological and physiological stress. Yet, for habituated species, it is not clear whether this relationship with humans still holds to a lesser degree or is outweighed by the benefits of human presence - such as serving as a buffer from competitors or predators. We investigated how human presence and environmental challenges such as resource availability, weather, predation, and competition may be associated with variation in fecal cortisol metabolite levels (FCMs) in a group of samango monkeys (Cercopithecus albogularis) in the Soutpansberg Mountains, South Africa. FCMs can often broadly track environmental challenges and perturbations. Initially, we employed an exploratory analysis comparing candidate models representing biological hypotheses and found that those incorporating information on human presence had less weight than models for food availability, thermoregulation, and water scarcity. When we examined a subset of the data that included information on intergroup competition and predator alarm calls, we found that FCMs were higher on the day following potential predator encounters but not competitive interactions. As observer numbers increased, responses to predators flattened, indicating that the presence of several humans might deter predators and/or affect samangos' perception of danger - yet we could not distinguish between these possibilities. Together, these results suggest that ecological perturbations track with FCMs in this study population and challenge long-held assumptions that human presence has negligible effects on habituated study animals.

Anthropogenic influences on primate antipredator behavior and implications for research and conservation.

Predation risk affects prey species' behavior, even in the absence of a direct threat, but human-induced environmental change may disturb ecologically significant predator-prey interactions. Here, we propose various ways in which knowledge of antipredator tactics, behavioral risk effects, and primate-predator interactions could assist in identifying human-caused disruption to natural systems. Using behavior to evaluate primate responses to the ongoing environmental change should be a potentially effective way to make species conservation more predictive by identifying issues before a more dramatic population declines. A key challenge here is that studies of predation on primates often use data collected via direct observations of habituated animals and human presence can deter carnivores and influence subjects' perception of risk. Hence, we also review various indirect data collection methods to evaluate their effectiveness in identifying where environmental change threatens wild species, while also minimizing observer bias.

What have we been looking at? A call for consistency in studies of primate vigilance.

Vigilance functions to detect threats. In primates, these threats emerge from both predators and conspecifics, but a host of other social, demographic, and ecological factors have been shown to influence primate vigilance patterns. The primate vigilance literature is thus characterized by considerable variation in findings, with inconsistent or contradictory results reported not only across different species but also within species and populations across studies. Some of this variation could emerge from fundamental differences in the methods employed, making comparisons across species and groups challenging. Furthermore, identifying consistent behavioral markers for the state of vigilance appears to have proved challenging in primates, leading to a range of definitions being developed. Deviation at this level leads directly into concomitant variation at the level of sampling methodologies. As a result, the primate vigilance literature currently presents a diverse series of approaches to exploring subtly different behaviors and phenomena. This review calls for a greater consistency in studying vigilance, with the aim of encouraging future research to follow similar principles leading to more comparable results. Identifying whether an animal is in a vigilant state is challenging for most field researchers; identifying and recording a more general behavior of "looking" should though be more achievable. Experimental approaches could then be employed to understand the compatibility "looking" has with predator detection (and other threats) in individual study systems. The outcome of this approach will allow researchers to understand the key determinants of looking in their study groups and explore threat detection probabilities given an individual or group's relative level of looking.

Temporal activity and detection rates of chilla (Lycalopex griseus) in Tierra del Fuego, Argentina.

Designing mitigation strategies for invasive species requires a clear understanding of their ecology and behaviour. Chilla (or grey fox; Lycalopex griseus) were introduced to Isla Grande de Tierra del Fuego (Tierra del Fuego Island) in 1951 to control European rabbit (Oryctolagus cuniculus) populations. Although this management strategy was unsuccessful, the chilla spread across the island and are now considered invasive. Despite this, there is a lack of research concerning their ecology and behavioural patterns, particularly on the Argentinian side of the island. We assessed the detection rates and temporal activity patterns of chillas using camera traps in the Argentinian region of Tierra del Fuego Island. Chilla had average detection rates of 61.7 (SD ± 33.3, range = 13.5-105.7) per 100 trap nights. Although analysis by clock time suggested cathemeral activity patterns, when analysed by sun time the chillas exhibited distinct nocturnal activity patterns. These findings offer the first information on the detection rates of chilla on the Argentinian side of Tierra del Fuego Island and reveal new insights into their temporal activity patterns, providing an important basis for future research that may aid the development of more effective management and conservation strategies.

Intolerant baboons avoid observer proximity, creating biased inter-individual association patterns.

Social network analysis is an increasingly popular tool for behavioural ecologists exploring the social organisation of animal populations. Such analyses require data on inter-individual association patterns, which in wild populations are often collected using direct observations of habituated animals. This assumes observers have no influence on animal behaviour; however, our previous work showed that individuals in a habituated group of chacma baboons (Papio ursinus griseipes) displayed consistent and individually distinct responses to observer approaches. We explored the implications of our previous findings by measuring the inter-individual association patterns of the same group of chacma baboons at different observer distances. We found a strong positive association between individual tolerance levels (towards observers) and how often an animal appeared as a neighbour to focal animals when observers were nearer, and a neutral relationship between the same variables when the observer was further away. Additionally, association matrices constructed from different observation distances were not comparable within any proximity buffer, and neither were the individual network metrics generated from these matrices. This appears to be the first empirical evidence that observer presence and behaviour can influence the association patterns of habituated animals and thus have potentially significant impacts on measured social networks.

Consistency in the flight and visual orientation distances of habituated chacma baboons after an observed leopard predation. Do flight initiation distance methods always measure perceived predation risk?

Flight initiation distance (FID) procedures are used to assess the risk perception animals have for threats (e.g., natural predators, hunters), but it is unclear whether these assessments remain meaningful if animals have habituated to certain human stimuli (e.g., researchers, tourists). Our previous work showed that habituated baboons displayed individually distinct and consistent responses to human approaches, a tolerance trait, but it is unknown if the trait is resilient to life-threatening scenarios. If it were consistent, it would imply FIDs might measure specific human threat perception only and not generalize to other threats such as predators when animals have experienced habituation processes. We used FID procedures to compare baseline responses to the visual orientation distance, FID, and individual tolerance estimates assessed after a leopard predation on an adult male baboon (group member). All variables were consistent despite the predation event, suggesting tolerance to observers was largely unaffected by the predation and FID procedures are unlikely to be generalizable to other threats when habituation has occurred. FID approaches could be an important tool for assessing how humans influence animal behavior across a range of contexts, but careful planning is required to understand the type of stimuli presented.

Habituation is not neutral or equal: Individual differences in tolerance suggest an overlooked personality trait.

In behavioral studies, observer effects can be substantial, even for habituated animals, but few studies account for potential observer-related phenomenon empirically. We used wild, habituated chacma baboons to explore two key assumptions of behavioral ecology (i) that observers become a "neutral" stimulus and (ii) that habituation is "equal" across group members. Using flight initiation distance (FID) methods within a personality paradigm, the behavioral responses of baboons suggested that observers were not perceived as neutral but instead viewed as a high-ranking social threat. Habituation was also not equal across group members, with repeatable individual differences more important than contextual factors (e.g., habitat) in determining the distance at which baboons visually oriented or displaced from observers. A strong correlation between individual visual tolerance and displacement tolerance (i.e., convergent validity) indicated a personality trait. We offer several suggestions for how to account for these factors and minimize potential bias in future studies.

Influence of food availability, plant productivity, and indigenous forest use on ranging behavior of the endangered samango monkey (Cercopithecus albogularis schwarzi), in the Soutpansberg Mountains, South Africa.

Understanding the determinants of ranging patterns in species susceptible to habitat fragmentation is fundamental for assessing their long-term adaptability to an increasingly human-dominated landscape. The aim of this study was to determine and compare the influence of ground-based food availability, remotely sensed plant productivity, and indigenous forest use on the ranging patterns of the endangered samango monkey (Cercopithecus albogularis schwarzi). We collected monthly ranging data on two habituated samango monkey groups, from February 2012 to December 2016, from our field site in the Soutpansberg Mountains, South Africa. We used linear mixed models to explore how food availability, plant productivity, and indigenous forest use influenced monthly ranging patterns, while controlling for group size, number of sample days and day length. We found that as more areas of high plant productivity (derived from remotely sensed EVI) were incorporated into the ranging area, both total and core monthly ranging areas decreased. In addition, both total ranging area and mean monthly daily path length decreased as more indigenous forest was incorporated into the ranging area. However, we found no effect of either ground-based food availability or remotely sensed plant productivity on ranging patterns. Our findings demonstrate the behavioral flexibility in samango monkey ranging, as samangos can utilize matrix habitat during periods of low productivity but are ultimately dependent on access to indigenous forest patches. In addition, we highlight the potential of using remotely sensed areas of high plant productivity to predict ranging patterns in a small ranging, forest-dwelling guenon, over ground-based estimates of food availability.