Approaches to studying gaze monitoring in nonhuman primates.

This thesis explored the gaze monitoring abilities of monkeys. A review of previous studies indicated that the face is a valuable source of information for nonhuman primates. When viewing faces, nonhuman primates can recognise conspecifics, individuals and emotional expressions. Within the face, the eyes are a particularly salient feature; nonhuman primates are extremely sensitive to the eyes and gaze is an integral component of all primate expressions. However, where another individual is looking potentially allows a primate access to a wealth of information about their environment; another’s visual orientation can indicate important objects or events. It is this informational value of gaze, rather than responses to self-directed gaze, that is the focus of this thesis. Previous research has indicated that nonhuman primates’ responses to gaze are fairly inconsistent across tasks. Therefore, the studies reported here explored monkeys’ responses to gaze within a number of experimental paradigms in order to better evaluate their abilities. Approaches included spontaneous responses to another individual’s visual co-orientation, picture discrimination, object-choice tasks, a competitive task and a computer-based cueing paradigm. The data reported in this thesis are consistent with previous research in this Held. Nonhuman primates spontaneously follow gaze within a simple visual co-orientation paradigm, but they do not readily use gaze as an informational cue within other paradigms, such as the object-choice task. Explanations of this pattern of results are suggested, and mainly focus on the ecological validity of the tasks and general procedural issues. In addition, nonhuman primates do not demonstrate preferential responding to eye gaze, in fact, head orientation seems to be the more salient cue. These findings are not readily accommodated by Baron-Cohen’s (1994) model that proposes that the eyes are the pre-eminent source of information regarding another individuals’ gaze direction. Directions for future research are identified. There is considerable need for further research on a wider range of primate species, and for a consideration o f the ontogeny of behaviours. A more detailed analysis o f the role o f gaze in nonhuman primates’ natural interactions is considered desirable and other paradigms are also suggested

Gaze discrimination learning in olive baboons (Papio anubis)

The ability to discriminate between pairs of photographs according to the portrayed model’s visual attention status was examined in four olive baboons. Two baboons successfully managed to solve the problem, even when attention was demonstrated by eye direction alone. A third showed an ability to discriminate head direction but not eye direction. In order to investigate further their ability to discriminate attention, the two successful baboons and two naïve baboons were presented with a simple object-choice task accompanied by experimenter-given cues. There was no evidence of transfer from the photographic stimuli to a real model; only one baboon showed signs of using the experimenter’s attention to chose between two objects, and only after over 300 trials. These results could suggest that the baboons used simple physical cues rather than a concept of attention to solve the picture discrimination but alternative explanations are also discussed

Eye preferences in capuchin monkeys (Sapajus apella)

This study explored whether capuchin monkey eye preferences differ systematically in response to stimuli of positive and negative valence. The ‘valence hypothesis’ proposes that the right hemisphere is more dominant for negative emotional processing and the left hemisphere is more dominant for positive emotional processing. Visual information from each eye is thought to be transferred faster to and primarily processed by the contralateral cerebral hemisphere. Therefore, it was predicted capuchin monkeys would show greater left eye use for looking at negative stimuli and greater right eye use for looking at positive stimuli. Eleven captive capuchin monkeys were presented with four images of different emotional valence (an egg and capuchin monkey raised eyebrow face were categorised as positive, and a harpy eagle face and capuchin monkey threat face were categorised as negative) and social relevance (consisting of capuchin monkey faces or not), and eye preferences for viewing the stimuli through a monocular viewing hole were recorded. While strong preferences for using either the left or right eye were found for most individuals, there was no consensus at the population level. Furthermore, the direction of looking, number of looks and duration of looks did not differ significantly with the emotional valence of the stimuli. These results are inconsistent with the main hypotheses about the relationship between eye preferences and processing of emotional stimuli. However, the monkeys did show significantly more arousal behaviours (vocalisation, door-touching, self-scratching and hand-rubbing) when viewing the negatively valenced stimuli than the positively valenced stimuli, indicating that the stimuli were emotionally salient. These findings do not provide evidence for a relationship between eye preferences and functional hemispheric specialisations, as often proposed in humans. Additional comparative studies are required to better understand the phylogeny of lateral biases, particularly in relation to emotional valence

Engaging zoo visitors at chimpanzee (Pan troglodytes) exhibits promotes positive attitudes toward chimpanzees and conservation

Understanding how visitor engagement with interpretation impacts on their attitudes to conservation is necessary to develop effective zoo-based conservation education. We examined whether facilitating an emotional connection between a visitor and an individual chimpanzee (Pan troglodytes) was more successful at enhancing attitudes than standard zoo interpretation. Attitudes were assessed post visit using a 12-item questionnaire on predisposition toward nature, attitudes to chimpanzees, and conservation. Visitors at two chimpanzee exhibits were allocated to an emotion enhancement condition (n = 227) or a control condition (n = 203). At one exhibit, visitors were also allocated to an interactive task (location) without emotional enhancement (n = 69). Participants were also recruited to an online control condition (n = 216). Principal component analyses identified two components labeled as Naturalistic, which refers to interest and affection for wildlife and nature, and Humanistic, which refers to interest and affection for individual animals or species with anthropomorphic characteristics. At one exhibit, both Naturalistic and Humanistic attitudes were significantly more positive following the emotion enhancement condition than for the control condition. At the other exhibit, Naturalistic and Humanistic components did not differ between conditions, and there was no overall difference between online and on-site conditions. While emotional enhancement may be effective in promoting pro-conservation attitudes, this is dependent on contextual factors (e.g., exhibit design and interpretation). Attitudes were also influenced by stable visitor characteristics (pet ownership and zoo membership) and are therefore likely to prove difficult to change, at least during a single zoo visit. Visitor and animal characteristics, and the interpretation of the exhibit all shape the visitor experience; understanding these interactions is important in facilitating effective zoo conservation education

Participation in a prison-based training programme is beneficial for rescue dogs

Dogs are often relinquished because of behavioural issues which may be exacerbated in rehoming centres. Prison-based dog training programmes (DTPs) may enhance outcomes for rescue dogs by providing socialisation and training opportunities to improve behaviour, welfare and likelihood of rehoming. We assessed whether dogs benefitted from participation, 1-3 times per week, in a prison-based DTP in which male young offenders learn how to train and care for dogs waiting to be rehomed. Within DTP sessions, there was significant improvement on a range of training tasks (n=42 dogs). Analyses of videos (n=17 dogs) in the kennels and a training barn pre- and post-DTP participation showed improvement in some positive behaviours, but no significant change in other behaviours. Subjective ratings by staff of the dogs’ behaviour were made (n=20 dogs). Desirable behaviours (e.g. playful/friendly) increased, and most undesirable behaviours (e.g. frustrated and noisy) decreased. Participation in the DTP did not mitigate all negative behaviours. However, improvements are consistent with enhanced welfare and likelihood of successful rehoming. Prison-based DTPs can be effective in supporting the work of animal rescue organisations to improve outcomes for dogs, while offering people in custody an opportunity to engage in purposeful activity and provide a community service

Participation in a prison-based training programme is beneficial for rescue dogs

Dogs are often relinquished because of behavioural issues which may be exacerbated in rehoming centres. Prison-based dog training programmes (DTPs) may enhance outcomes for rescue dogs by providing socialisation and training opportunities to improve behaviour, welfare and likelihood of rehoming. We assessed whether dogs benefitted from participation, 1-3 times per week, in a prison-based DTP in which male young offenders learn how to train and care for dogs waiting to be rehomed. Within DTP sessions, there was significant improvement on a range of training tasks (n=42 dogs). Analyses of videos (n=17 dogs) in the kennels and a training barn pre- and post-DTP participation showed improvement in some positive behaviours, but no significant change in other behaviours. Subjective ratings by staff of the dogs’ behaviour were made (n=20 dogs). Desirable behaviours (e.g. playful/friendly) increased, and most undesirable behaviours (e.g. frustrated and noisy) decreased. Participation in the DTP did not mitigate all negative behaviours. However, improvements are consistent with enhanced welfare and likelihood of successful rehoming. Prison-based DTPs can be effective in supporting the work of animal rescue organisations to improve outcomes for dogs, while offering people in custody an opportunity to engage in purposeful activity and provide a community service

Use of human visual attention cues by Olive baboons (Papio anubis) in a competitive task

The ability of four olive baboons (Papio anubis) to use human gaze cues during a competitive task was investigated; the baboons were allowed to remove only the non-fixated one of two simultaneously presented food items. Three baboons successfully learned to exploit the human’s head orientation as a cue to obtain a food item, and one individual also learned to use eye direction alone. As the baboons did not receive prior training with gross gestural cues, their performance suggests that the competitive paradigm may be more conducive to gaze monitoring in nonhuman primates than the standard object-choice paradigm. However, the baboons were insensitive to whether the experimenter could actually perceive the food item and therefore use of visual orientation cues may not be indicative of visual perspective-taking abilities in baboons. Performance was disrupted by the introduction of a screen and objects to conceal the food items, and to a lesser degree by the absence of movement in cues presented

Exploration of potential triggers for self-directed behaviours and regurgitation and reingestion in zoo-housed chimpanzees

The unique challenges faced by animals living in zoos can lead to the production of anxiety-related behaviours. In this study we aimed to understand what specific factors may cause chimpanzees to display these behaviours. In non-human primates, displacement behaviours, such as self-scratching and yawning, are considered markers of anxiety and stress, and Regurgitation and Reingestion (R/R) is considered an abnormal behaviour with negative consequences for physical health. We examined the possible triggers of R/R, scratching, and yawning in a group of zoo-housed chimpanzees and followed this up with an analysis of long-term data to examine further aspects of R/R behaviour. In the first study we conducted focal observations on 18 adult chimpanzees at Edinburgh Zoo, UK, in addition to all occurrence sampling of visitors using flash photography, screaming and banging on the glass in the exhibit. 158 h of data were analysed and Generalised Linear Mixed Models revealed that yawning was significantly more likely if there was a long period of time since the last feed and when there were moderate numbers of visitors in the zoo. There were trends that yawning was more likely to occur if children screamed and that scratching was more likely to occur if visitors used flash photography. R/R occurred most often within 40 min of a feed, but was not affected by the inter-feed interval preceding that feed, positive or negative social interactions, or visitor numbers or behaviour. As there was no obvious daily trigger for R/R, an analysis of long-term data (2009 to 2015) was conducted to investigate if social or dietary factors affected rates of R/R over a larger timescale. It was found that R/R rates in the months before a significant diet change were not different from R/R rates in the months after, but it was found that R/R rates decreased over the five-year period. Lastly, we found no evidence that the introduction of individuals engaging in R/R lead to resident chimpanzees habitually adopting the behaviour, despite considerable opportunities to observe it. These findings have implications for welfare interventions aimed to reduce R/R and/or anxiety behaviours in captive populations and for the translocation of individuals that are known to engage in R/R between groups.Peer reviewe

Pictorial gaze cues do not enhance long tailed macaques’ performance on a computerised object location task

The perception of pictorial gaze cues was examined in long-tailed macaques (Macaca fascicularis). A computerised object location task was used to explore whether the monkeys would show faster response time to locate a target when its appearance was preceded with congruent as opposed to incongruent gaze cues. Despite existing evidence that macaques preferentially attend to the eyes in facial images and also visually orient with depicted gaze cues, the monkeys did not show faster response times on congruent trials either in response to schematic or photographic stimuli. These findings coincide with those reported for baboons tested with a similar paradigm in which gaze cues preceded a target identification task (Fagot and Deruelle 2002). When tested with either pictorial stimuli or interactants, non human primates readily follow gaze but do not seem to use this mechanism to identify a target object; there seems to be some mismatch in performance between attentional changes and manual responses to gaze cues on ostensibly similar tasks

A Cross-species Comparison of Facial Morphology and Movement in Humans and Chimpanzees Using the Facial Action Coding System (FACS)

A comparative perspective has remained central to the study of human facial expressions since Darwin’s (1872) insightful observations on the presence and significance of cross-species continuities and species-unique phenomena. However, cross-species comparisons are often difficult to draw due to methodological limitations. We report the application of a common methodology, the Facial Action Coding System (FACS) to examine facial movement across two species of hominoids, namely humans and chimpanzees. The Facial Action Coding System (FACS: Ekman & Friesen, 1978) has been employed to identify the repertoire of human facial movements. We demonstrate that FACS can be applied to other species, but highlight that any modifications must be based on both underlying anatomy and detailed observational analysis of movements. Here we describe the ChimpFACS and use it to compare the repertoire of facial movement in chimpanzees and humans. While the underlying mimetic musculature shows minimal differences, important differences in facial morphology impact upon the identification and detection of related surface appearance changes across these two species