Intolerant baboons avoid observer proximity, creating biased inter-individual association patterns
All research methods included in this study were performed in accordance with the relevant guidelines and regulations, under ZA/LP/81996 research permit, with ethical approval from the Animal Welfare Ethical Review Board (AWERB) at Durham University. The authors confirm the study was carried out in compliance with ARRIVE guidelines.All inter-individual association data was collected between June 2018 and June 2019 on a wild habituated group of Afro-montane chacma baboons in the western Soutpansberg Mountains, South Africa (central coordinates S29.44031°, E23.02217°) (for study site description see2). The study group was habituated circa 2005 and was the focus of intermittent research attention until 2014. The study area experienced long-term anthropogenic activities (local farming, forestry, and residences) prior to 2005, as such, consistent interactions with humans have been ongoing with this population for some time. From 2007 onwards numerous researchers were able to collect expansive datasets on the study group (e.g. Refs.17,18), indicating that habituation was at a typical level found elsewhere (also validated by AA and RH, who had researched chacma baboons elsewhere). From 2014 the group received full day (dawn until dusk) follows 3–4 days a week, with occasional gaps of up to 5 weeks in duration. These gaps did not appear to effect habituation levels, likely due to the presence of other researchers at the field site who always tried to act benignly when encountering the habituated group. The follow schedule was designed so that the study group retained as much of their natural interactions with predators as possible by ensuring the baboons spent significant time without observers who may influence the frequency and nature of predator–prey interactions19.The study site was located in a private nature reserve and the study group was not hunted during observation gaps or engaged in any conflict with humans, other than occasionally being scared (chasing, yelling, throwing stones etc.) from a small plantation by local workers, usually resulting in alarm barks and fleeing responses. However, the study group appeared adept at recognising the differences between researchers and these threats20. The majority of the study group’s home-range typically overlapped with the core area of the Lajuma Research Centre, and as a result, interactions with staff living in the area, unfamiliar researchers, and tourists were frequent. However, the baboons had not engaged in ‘raiding’ residences, threatening humans, or any other potentially negative symptom of habituation before the end of this study.Sampling methodology for proximity associations30-s focal sampling was used to collect proximity associations between all group members (excluding infants). All data was collected between June and December 2018 and January and June 2019; the majority of 2018s data was collected during the wet season, whilst most of 2019s data was collected during the dry season. To account for time of day, each day was split into four time-periods that were seasonally adjusted ensuring each period accounted for 25% of the current day length. A randomly ordered list of individuals was produced for each day, the first individual identified from the top 15 (approx. 20% of group size) individuals on the list was sampled immediately. Individuals could only be sampled once per time period per day, and a maximum of twice total per day. All individuals received at least 14 focal observations per time period (56 total) across the study period (see below for how we handled uneven sampling for some individuals). A video camera was used by AA (the only observer to collect this data) to record all focal observations (Panasonic HC-W580 Camcorder). At the end of the 30-s focal observation the identities of all neighbouring conspecifics within 5 m, 2.5 m, 1 m, and touching the focal animal were recorded (audibly by AA). We chose the end of the focal observation to record this data as this was most likely to reflect the conditions during the focal, i.e., the observer had been in proximity for at least 30 s.Neighbour information was extracted from video footage and entered manually by AA and AW. Data was split into separate years to reflect an observation gap of several weeks and to understand whether there was consistency in the hypothesized effects through time and to reflect underlying differences in environmental conditions during the two study periods; during the dry season fruits and seeds are scarce and day lengths are several hours shorter than in the wet season such that day journey lengths are often shorter in the dry season and animals are much more sedentary which could impact inter-individual spacings. In 2018 each individual was sampled between 28 and 30 times; 28 focals were randomly selected from each individual to make sampling even. For 2019 there were between 25 and 27 focals per individual; 25 samples of each individual were randomly selected. Observations were undertaken at a range of distances. For both years the median end observer distance was 4.5 m; data was thus split into close focal observations of less than or equal to 4.5 m (2018: n = 918, 2019: n = 809), and observations greater than 4.5 m (2018: n = 902 2019: n = 816). See supporting information Table S1 for summary statistics of the observation distances of each individual.We did not make any attempt to record our focal data evenly across the various habitats at our field site (see Supporting information text S1 for complete habitat descriptions) as our previous research indicated there was little difference in general spatial cohesion/inter-individual proximity patterns across these habitats (see Supporting information text S2 and Table S2). As a result, we considered it unlikely that there were fundamental differences in inter-individual association patterns across habitats, or that observers struggled to reliably detect or identify neighbours in dense habitats. We do acknowledge, however, that there will always be an element of bias with such methods, as observations were avoided, aborted, or excluded if visual obstructions (e.g., cliffs, rocks, walls, buildings, very dense vegetation etc.) prohibited accurate assessments; the observations used in the current study are from occasions when these factors were not an issue.During this study the group contained between 85 and 92 individuals. Age-sex class was defined according to secondary sexual characteristics (e.g., testes descending/enlarging, sexual swelling, canine eruption) and changes in pelage throughout juvenile development (see Supporting information text S3 for full descriptions). All 65 non-infant individuals that were present during 2017 (when displacement tolerances were calculated) and still remaining in the group by the end of 2019 were used in this study (4 individuals from the prior FID study were no longer present). There were a high number of births between 2018 and 2019, but none were independent by the time either of our sampling periods begun in 2018 or 2019. There was no immigration of foreign individuals, but two individuals disappeared, both during the 2018 focal sampling period. As a result, we had a very consistent pool of individuals to sample from during this study. We removed all data associated with the two individuals who disappeared as their occurrences as neighbours would have been poorly sampled (due to missing more than half the study) relative to the rest of the group which would have led to statistical biases21.Flight initiation distance procedureIndividual displacement tolerance estimates were previously quantified in our previous research2 using a flight initiation distance (FID) procedure22 that was completed between October 2017 and April 2018, prior and independent to the commencement of proximity association focal sampling in June 2018. Individual baboons were approached by an observer, and the distance at which the animal displaced away from the observer measured (see Supporting information Table S2 for summary statistics). This procedure was repeated 24 times for each individual baboon, with approaches spread evenly across two observers differing in familiarity. At the beginning of each approach we also recorded several behavioural, social, and environmental factors that could have hypothetically influenced an individual’s FID2 including whether the animal was engaged (e.g., digging or grooming) or not engaged (e.g., resting, chewing food, being groomed), habitat type (open/closed: see Supporting text S1), whether the animal was on the ground or sat on a low branch or rock within 50 cm of the ground, the number of conspecifics within 5 m of the focal animal, and whether there had been any external events within the preceding 5 min (e.g., alarm calls, aggressions, encountering another group or predator). During the approach, we also recorded the visual orientation distance (the distance at which the focal animal directed its line of vision towards the head of the approaching observer) and whether one of the focal animal’s neighbours had displaced/fled before the focal animal. Although all but neighbour flee first and external events showed some importance for predicting looking (see Table S4), FID was found to be distinct amongst individuals and repeatable within each individual, evidence that displacement tolerance may be an individual level trait2. Full details of methods, statistical analysis, and results (including comparison to the original model) for this updated model are in Supporting information text S4, with model summary results for the previous and updated models in Tables S3 and S4.The notion of an observer approaching a habituated primate may be considered atypical or likely to result in habituation/sensitization effects or agonistic behaviours being directed towards the approaching observers. However, our previous study2 showed that almost all approaches resulted in the animal passively relocating (98.85%), a very benign response identical to the behaviours of subordinate baboons displacing away from dominant conspecifics. This suggests that in this group, observers may be considered equivalent to a high-level social threat2. Throughout observation periods on habituated animals, observers are likely to approach or displace animals either incidentally or accidentally multiple times throughout the day, especially during lengthy focal observations. As such, the approach methodology is unlikely to represent a stimulus outside of the norm for our study animals. This may explain why displacement responses were so passive and why there was no evidence of habituation or sensitization effects across the group or individually through a range of temporal periods2 or after life-threatening events20. As a result, our situation was possible without risk of causing stress or anxiety in the study subjects, eliciting agonistic behaviours towards observers, or interfering with their prior habituation levels.Statistical analysisInfluence of tolerance and observer distance on inter-individual association patternsQuantifying displacement toleranceTo quantify displacement tolerance towards observers we extracted the individual conditional modes from the updated FID model using the ranef function in brms. Conditional modes are often referred to as Best Linear Unbiased Predictors (BLUPs) and are the difference between the predicted mean population-level response for a given set of treatments (i.e., population-level effects) and the predicted responses for each individual, and therefore infer the extent to which each individual differs from the population mean. The conditional modes and their associated standard deviations can be found in supporting information Table S5.To validate that the conditional modes from the updated model were both representative of the individual’s flight responses and in line with the estimates produced from our previous study2 we performed additional tests. Firstly, we performed a Pearson’s correlation between the conditional modes from the updated model and the conditional modes from the previous article. Individual tolerance estimates were consistent (r(63) = 0.915, p More
