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.

Impacts of invasive plants on animal behaviour.

The spread of invasive species is a threat to ecosystems worldwide. However, we know relatively little about how invasive species affect the behaviour of native animals, even though behaviour plays a vital role in the biotic interactions which are key to understanding the causes and impacts of biological invasions. Here, we explore how invasive plants - one of the most pervasive invasive taxa - impact the behaviour of native animals. To promote a mechanistic understanding of these behavioural impacts, we begin by introducing a mechanistic framework which explicitly considers the drivers and ecological consequences of behavioural change, as well as the moderating role of environmental context. We then synthesise the existing literature within this framework. We find that while some behavioural impacts of invasive plants are relatively well-covered in the literature, others are supported by only a handful of studies and should be explored further in the future. We conclude by identifying priority topics for future research, which will benefit from an interdisciplinary approach uniting invasion ecology with the study of animal behaviour and cognition.

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.

Adapting Methodology Used on Captive Subjects for Estimating Gut Passage Time in Wild Monkeys.

Gut passage time of food has consequences for primate digestive strategies, which subsequently affect seed dispersal. Seed dispersal models are critical in understanding plant population and community dynamics through estimation of seed dispersal distances, combining movement data with gut passage times. Thus, developing methods to collect in situ data on gut passage time are of great importance. Here we present a first attempt to develop an in situ study of gut passage time in an arboreal forest guenon, the samango monkey (Cercopithecus albogularis schwarzi) in the Soutpansberg Mountains, South Africa. Cercopithecus spp. consume large proportions of fruit and are important seed dispersers. However, previous studies on gut passage times have been conducted only on captive Cercopithecusspp. subjects, where movement is restricted, and diets are generally dissimilar to those observed in the wild. Using artificial digestive markers, we targeted provisioning of a male and a female samango monkey 4 times over 3 and 4 days, respectively. We followed the focal subjects from dawn until dusk following each feeding event, collecting faecal samples and recording the date and time of deposition and the number of markers found in each faecal sample. We recovered 6.61 ± 4 and 13 ± 9% of markers from the male and the female, respectively, and were able to estimate a gut passage window of 16.63-25.12 h from 3 of the 8 trials. We discuss methodological issues to help future researchers to develop in situ studies on gut passage times.

Topological spatial representation in wild chacma baboons (Papio ursinus).

Many species orient towards specific locations to reach important resources using different cognitive mechanisms. Some of these, such as path integration, are now well understood, but the cognitive orientation mechanisms that underlie movements in non-human primates remain the subject of debate. To investigate whether movements of chacma baboons are more consistent with Euclidean or topological spatial awareness, we investigated whether baboons made repeated use of the same network of pathways and tested three predictions resulting from the hypothesized use of Euclidean and topological spatial awareness. We recorded ranging behaviour of a group of baboons during 234 full days and 137 partial days in the Soutpansberg Mountains, South Africa. Results show that our baboons travelled through a dense network of repeated routes. In navigating this route network, the baboons did not approach travel goals from all directions, but instead approached them from a small number of the same directions, supporting topological spatial awareness. When leaving travel goals, baboons' initial travel direction was significantly different from the direction to the next travel goal, again supporting topological spatial awareness. Although we found that our baboons travelled with similar linearity in the core area as in the periphery of their home range, this did not provide conclusive evidence for the existence of Euclidean spatial awareness, since the baboons could have accumulated a similar knowledge of the periphery as of the core area. Overall, our findings support the hypothesis that our baboons navigate using a topological map.

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.

Red clothing increases perceived dominance, aggression and anger.

The presence and intensity of red coloration correlate with male dominance and testosterone in a variety of animal species, and even artificial red stimuli can influence dominance interactions. In humans, red stimuli are perceived as more threatening and dominant than other colours, and wearing red increases the probability of winning sporting contests. We investigated whether red clothing biases the perception of aggression and dominance outside of competitive settings, and whether red influences decoding of emotional expressions. Participants rated digitally manipulated images of men for aggression and dominance and categorized the emotional state of these stimuli. Men were rated as more aggressive and more dominant when presented in red than when presented in either blue or grey. The effect on perceived aggression was found for male and female raters, but only male raters were sensitive to red as a signal of dominance. In a categorization test, images were significantly more often categorized as 'angry' when presented in the red condition, demonstrating that colour stimuli affect perceptions of emotions. This suggests that the colour red may be a cue used to predict propensity for dominance and aggression in human males.

Biogeographic variation in the diet and behaviour of Cercopithecus mitis.

Primate species are characterised by variation in foraging behaviour and dietary composition across their geographic range. Here we examine how ecological conditions account for variation in the behavioural ecology of a widespread arboreal guenon, Cercopithecus mitis. Although substantial variation existed in time budgets, group size, home range and day journey length, clear biogeographic patterns were not apparent. In contrast, dietary variation was correlated with underlying climatic conditions. Temperature seasonality, which tends to increase with latitude, was significantly positively related to the proportion of fruit in the diet and negatively related to the proportion of animal matter. Both dietary components were 'preferred' foods, with the variability between populations reflecting the availability of different food types across their geographic range. Although we found no significant relationships between climate and the proportion of leaves in the diet, the ability for C. mitis to vary its diet to include a diversity of food types, and to incorporate a significant proportion of leaves when preferred sources are scarce, likely underpins its ability to survive across such a large distribution.

Keystone individuals - linking predator traits to community ecology.

Individual behavioral plasticity enables animals to adjust to different scenarios. Yet, personality traits limit this flexibility, leading to consistent interindividual differences in behavior. These individual behavioral traits have the potential to govern community interactions, although testing this is difficult in complex natural systems. For large predators who often exert strong effects on ecosystem functioning, this behavioral diversity may be especially important and lead to individualized ecosystem roles. We present a framework for quantifying individual behavioral plasticity and personality traits of large wild predators, revealing the extent to which certain natural behaviors are governed by these latent traits. The outcomes will reveal how the innate characteristics of wildlife can scale up to affect community interactions.

Behavioural compatibility, not fear, best predicts the looking patterns of chacma baboons.

Animal vigilance is often investigated under a narrow set of scenarios, but this approach may overestimate its contribution to animal lives. A solution may be to sample all looking behaviours and investigate numerous competing hypotheses in a single analysis. In this study, using a wild group of habituated chacma baboons (Papio ursinus griseipes) as a model system, we implemented a framework for predicting the key drivers of looking by comparing the strength of a full array of biological hypotheses. This included methods for defining individual-specific social threat environments, quantifying individual tolerance to human observers, and incorporating predator resource selection functions. Although we found evidence supporting reactionary and within-group (social) vigilance hypotheses, risk factors did not predict looking with the greatest precision, suggesting vigilance was not a major component of the animals' behavioural patterns generally. Instead, whilst some behaviours constrain opportunities for looking, many shared compatibility with looking, alleviating the pressure to be pre-emptively vigilant for threats. Exploring looking patterns in a thorough multi-hypothesis framework should be feasible across a range of taxa, offering new insights into animal behaviour that could alter our concepts of fear ecology.

Open plains are not a level playing field for hominid consonant-like versus vowel-like calls.

Africa's paleo-climate change represents an "ecological black-box" along the evolutionary timeline of spoken language; a vocal hominid went in and, millions of years later, out came a verbal human. It is unknown whether or how a shift from forested, dense habitats towards drier, open ones affected hominid vocal communication, potentially setting stage for speech evolution. To recreate how arboreal proto-vowels and proto-consonants would have interacted with a new ecology at ground level, we assessed how a series of orangutan voiceless consonant-like and voiced vowel-like calls travelled across the savannah. Vowel-like calls performed poorly in comparison to their counterparts. Only consonant-like calls afforded effective perceptibility beyond 100 m distance without requiring repetition, as is characteristic of loud calling behaviour in nonhuman primates, typically composed by vowel-like calls. Results show that proto-consonants in human ancestors may have enhanced reliability of distance vocal communication across a canopy-to-ground ecotone. The ecological settings and soundscapes experienced by human ancestors may have had a more profound impact on the emergence and shape of spoken language than previously recognized.

Model selection in occupancy models: Inference versus prediction.

Occupancy models are a vital tool for ecologists studying the patterns and drivers of species occurrence, but their use often involves selecting among models with different sets of occupancy and detection covariates. The information-theoretic approach, which employs information criteria such as Akaike's information criterion (AIC) is arguably the most popular approach for model selection in ecology and is often used for selecting occupancy models. However, the information-theoretic approach risks selecting models that produce inaccurate parameter estimates due to a phenomenon called collider bias, a type of confounding that can arise when adding explanatory variables to a model. Using simulations, we investigated the consequences of collider bias (using an illustrative example called M-bias) in the occupancy and detection processes of an occupancy model, and explored the implications for model selection using AIC and a common alternative, the Schwarz criterion (or Bayesian information criterion, BIC). We found that when M-bias was present in the occupancy process, AIC and BIC selected models that inaccurately estimated the effect of the focal occupancy covariate, while simultaneously producing more accurate predictions of the site-level occupancy probability than other models in the candidate set. In contrast, M-bias in the detection process did not impact the focal estimate; all models made accurate inferences, while the site-level predictions of the AIC/BIC-best model were slightly more accurate. Our results show that information criteria can be used to select occupancy covariates if the sole purpose of the model is prediction, but must be treated with more caution if the purpose is to understand how environmental variables affect occupancy. By contrast, detection covariates can usually be selected using information criteria regardless of the model's purpose. These findings illustrate the importance of distinguishing between the tasks of parameter inference and prediction in ecological modeling. Furthermore, our results underline concerns about the use of information criteria to compare different biological hypotheses in observational studies.

Camera traps and guard observations as an alternative to researcher observation for studying anthropogenic foraging.

Foraging by wildlife on anthropogenic foods can have negative impacts on both humans and wildlife. Addressing this issue requires reliable data on the patterns of anthropogenic foraging by wild animals, but while direct observation by researchers can be highly accurate, this method is also costly and labor-intensive, making it impractical in the long-term or over large spatial areas. Camera traps and observations by guards employed to deter animals from fields could be efficient alternative methods of data collection for understanding patterns of foraging by wildlife in crop fields. Here, we investigated how data on crop-foraging by chacma baboons and vervet monkeys collected by camera traps and crop guards predicted data collected by researchers, on a commercial farm in South Africa. We found that data from camera traps and field guard observations predicted crop loss and the frequency of crop-foraging events from researcher observations for crop-foraging by baboons and to a lesser extent for vervets. The effectiveness of cameras at capturing crop-foraging events was dependent on their position on the field edge. We believe that these alternatives to direct observation by researchers represent an efficient and low-cost method for long-term and large-scale monitoring of foraging by wildlife on crops.

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.

Psychology: red enhances human performance in contests.

Red coloration is a sexually selected, testosterone-dependent signal of male quality in a variety of animals, and in some non-human species a male's dominance can be experimentally increased by attaching artificial red stimuli. Here we show that a similar effect can influence the outcome of physical contests in humans--across a range of sports, we find that wearing red is consistently associated with a higher probability of winning. These results indicate not only that sexual selection may have influenced the evolution of human response to colours, but also that the colour of sportswear needs to be taken into account to ensure a level playing field in sport.

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.

Habitat selection of an endangered primate, the samango monkey (Cercopithecus albogularis schwarzi): Integrating scales to prioritize habitat for wildlife management.

AIM: As habitat loss continues to accelerate with global human population growth, identifying landscape characteristics that influence species occurrence is a key conservation priority in order to prevent global biodiversity loss. In South Africa, the arboreal samango monkey (Cercopithecus albogularis sp.) is threatened due to loss and fragmentation of the indigenous forests it inhabits. The aim of this study was to determine the habitat preferences of the samango monkey at different spatial scales, and to identify key conservation areas to inform management plans for this species. LOCATION: This study was carried out in the western Soutpansberg Mountains, which represents the northernmost population of samango monkeys within South Africa, and the only endangered subspecies (C. a. schwarzi). METHODS: We used sequentially collected GPS points from two samango monkey groups followed between 2012 and 2017 to quantify the used and available habitat for this species within the western Soutpansberg Mountains. We developed 2nd-order (selection of ranging area), 3rd-order (selection within range), and 4th-order (feeding site selection) resource selection functions (RSFs) to identify important habitat features at each scale. Through scale integration, we identified three key conservation areas for samango monkeys across Limpopo Province, South Africa. RESULTS: Habitat productivity was the most important landscape variable predicting probability of use at each order of selection, indicating the dependence of these arboreal primates on tall-canopy indigenous forests. Critical habitat across Limpopo was highly fragmented, meaning complete isolation between subpopulations is likely. MAIN CONCLUSIONS: Understanding the habitat characteristics that influence samango monkey distribution across South Africa is crucial for prioritizing critical habitat for this species. Our results indicated that large, contiguous patches of tall-canopy indigenous forest are fundamental to samango monkey persistence. As such, protected area expansion of large forest patches and creation of forest corridors are identified as key conservation interventions for this species.

Seasonal variation in the behavioural ecology of samango monkeys (Cercopithecus albogularis schwarzi) in a southern latitude montane environment.

Samango monkeys (Cercopithecus albogularis schwarzi) in the Soutpansberg Mountains, South Africa, experience a highly seasonal climate, with relatively cold, dry winters. They must show behavioural flexibility to survive these difficult conditions near the southern limit of the species' distribution and maintain the minimum nutritional intake they require. Through environmental monitoring and behavioural observations of a habituated group of samango monkeys, we explored how they adapted to the highly seasonal climate they experienced in the mountains. Our results indicated that the monkeys varied their foraging behaviours to account for changes in climate and daylight availability. The samangos increased their food intake in colder months, specifically leaves, likely due to an increased need for calories during winter to maintain body temperature. Samango monkeys have anatomical and physiological adaptations for digesting leaves, and these are likely important in explaining their ability to adapt to the broad range of climatic conditions they experience.

Insights into short- and long-term crop-foraging strategies in a chacma baboon (Papio ursinus) from GPS and accelerometer data.

Crop-foraging by animals is a leading cause of human-wildlife "conflict" globally, affecting farmers and resulting in the death of many animals in retaliation, including primates. Despite significant research into crop-foraging by primates, relatively little is understood about the behavior and movements of primates in and around crop fields, largely due to the limitations of traditional observational methods. Crop-foraging by primates in large-scale agriculture has also received little attention. We used GPS and accelerometer bio-loggers, along with environmental data, to gain an understanding of the spatial and temporal patterns of activity for a female in a crop-foraging baboon group in and around commercial farms in South Africa over one year. Crop fields were avoided for most of the year, suggesting that fields are perceived as a high-risk habitat. When field visits did occur, this was generally when plant primary productivity was low, suggesting that crops were a "fallback food". All recorded field visits were at or before 15:00. Activity was significantly higher in crop fields than in the landscape in general, evidence that crop-foraging is an energetically costly strategy and that fields are perceived as a risky habitat. In contrast, activity was significantly lower within 100 m of the field edge than in the rest of the landscape, suggesting that baboons wait near the field edge to assess risks before crop-foraging. Together, this understanding of the spatiotemporal dynamics of crop-foraging can help to inform crop protection strategies and reduce conflict between humans and baboons in South Africa.

Assumptions about fence permeability influence density estimates for brown hyaenas across South Africa.

Wildlife population density estimates provide information on the number of individuals in an area and influence conservation management decisions. Thus, accuracy is vital. A dominant feature in many landscapes globally is fencing, yet the implications of fence permeability on density estimation using spatial capture-recapture modelling are seldom considered. We used camera trap data from 15 fenced reserves across South Africa to examine the density of brown hyaenas (Parahyaena brunnea). We estimated density and modelled its relationship with a suite of covariates when fenced reserve boundaries were assumed to be permeable or impermeable to hyaena movements. The best performing models were those that included only the influence of study site on both hyaena density and detection probability, regardless of assumptions of fence permeability. When fences were considered impermeable, densities ranged from 2.55 to 15.06 animals per 100 km2, but when fences were considered permeable, density estimates were on average 9.52 times lower (from 0.17 to 1.59 animals per 100 km2). Fence permeability should therefore be an essential consideration when estimating density, especially since density results can considerably influence wildlife management decisions. In the absence of strong evidence to the contrary, future studies in fenced areas should assume some degree of permeability in order to avoid overestimating population density.