Sarah-Jane Vick

Learning and limits of use of eye gaze by capuchin monkeys (Cebus apella) in an object-choice task.

The ability of 3 capuchin monkeys (Cebus apella) to use experimenter-given cues to solve an object-choice task was assessed. The monkeys learned to use explicit gestural and postural cues and then progressed to using eye-gaze-only cues to solve the task, that is, to choose the baited 1 of 2 objects and thus obtain a food reward. Increasing cue-stimulus distance and introducing movement of the eyes impeded the establishment of effective eye-gaze reading. One monkey showed positive but imperfect transfer of use of eye gaze when a novel experimenter presented the cue. When head and eye orientation cues were presented simultaneously and in conflict, the monkeys showed greater responsiveness to head orientation cues. The results show that capuchin monkeys can learn to use eye gaze as a discriminative cue, but there was no-evidence for any underlying awareness of eye gaze as a cue to direction of attention.

Brief communication: MaqFACS: A muscle-based facial movement coding system for the rhesus macaque.

Over 125 years ago, Charles Darwin (1872) suggested that the only way to fully understand the form and function of human facial expression was to make comparisons with other species. Nevertheless, it has been only recently that facial expressions in humans and related primate species have been compared using systematic, anatomically based techniques. Through this approach, large-scale evolutionary and phylogenetic analyses of facial expressions, including their homology, can now be addressed. Here, the development of a muscular-based system for measuring facial movement in rhesus macaques (Macaca mulatta) is described based on the well-known FACS (Facial Action Coding System) and ChimpFACS. These systems describe facial movement according to the action of the underlying facial musculature, which is highly conserved across primates. The coding systems are standardized; thus, their use is comparable across laboratories and study populations. In the development of MaqFACS, several species differences in the facial movement repertoire of rhesus macaques were observed in comparison with chimpanzees and humans, particularly with regard to brow movements, puckering of the lips, and ear movements. These differences do not seem to be the result of constraints imposed by morphological differences in the facial structure of these three species. It is more likely that they reflect unique specializations in the communicative repertoire of each species.

Intramuscular Electrical Stimulation of Facial Muscles in Humans and Chimpanzees: Duchenne Revisited and Extended

The pioneering work of Duchenne (1862/1990) was replicated in humans using intramuscular electrical stimulation and extended to another species (Pan troglodytes: chimpanzees) to facilitate comparative facial expression research. Intramuscular electrical stimulation, in contrast to the original surface stimulation, offers the opportunity to activate individual muscles as opposed to groups of muscles. In humans, stimulation resulted in appearance changes in line with Facial Action Coding System (FACS) action units (AUs), and chimpanzee facial musculature displayed functional similarity to human facial musculature. The present results provide objective identification of the muscle substrate of human and chimpanzee facial expressions- data that will be useful in providing a common language to compare the units of human and chimpanzee facial expression.

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

The ability of 4 olive baboons (Papio anubis) to use human gaze cues during a competitive food task was investigated. Three baboons used head orientation as a cue, and 1 individual also used eye direction alone. As the baboons did not receive prior training with gestural cues, their performance suggests that the competitive paradigm may be more appropriate for testing 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 the use of visual orientation cues may not be indicative of visual perspective-taking abilities. Performance was disrupted by the introduction of a screen and objects to conceal food items and by the absence of movement in cues presented.

Cognitive Research in Zoo‐Housed Chimpanzees: Influence of Personality and Impact on Welfare

We monitored chimpanzee welfare during the introduction of on‐exhibit cognitive research training and testing, as measured by behavior and interest in such training, and related individual variation to personality assessments. We observed 11 chimpanzees (six males; five females) over a 16‐month period and compared their behavior across three conditions: (1) Baseline (nontraining/research situations) and (2) an on‐going, off‐exhibit program of Husbandry Training and (3) Research Pod Activities, on‐exhibit, group training for cognitive testing. There was considerable individual variation in their interest levels during research sessions; females and those scoring higher for Openness were present more frequently (including those who actively participated and those who observed others participating), but interest did not vary in relation to rates of self‐directed behaviors (SDBs), rank, or the level of social disruptions within the group (i.e. large‐scale displays or fights). The frequency of SDBs was predicted by the Neuroticism personality factor, but did not differ across baseline and training contexts, indicating that these activities do not negatively impact welfare. We also explored vigilance as an indicator of social uncertainty, but social monitoring did not differ in relation to either social context or rank. Finally, we explored how the specific characteristics of the research context impacted on SDBs; namely, social context, reward contingency, and visual access to keepers. SDBs increased only when visual access to keepers was restricted, suggesting that visual contact reduced uncertainty in novel training contexts. Overall, the introduction of a cognitive research program did not compromise welfare, and the chimpanzees’ repeated interest and willingness to participate suggests that the research was enriching. Am. J. Primatol. 74:828‐840, 2012.

Communicative intentions in wild chimpanzees: persistence and elaboration in gestural signalling

We examine evidence for communicative intent during conspecific interactions in wild chimpanzees (Budongo Forest, Uganda), focusing on persistence in gestural communication. Previous research indicates that great apes have large gestural repertoires and produce gestural communication in a flexible and intentional manner, including the production of gesture sequences. Although there is a lack of consensus on the form and function of sequences, there is some evidence that sequences are produced when signallers fail to receive any response from a recipient. Here, we provide first systematic evidence for communicative persistence in wild chimpanzees. Rather than examining only the presence or absence of a response, we used the most commonly observed response to assign meanings to gestures and examined sequence production in relation to response congruency. Chimpanzees ceased communication if successful, but persevered when unsuccessful. Chimpanzees repeated gestures when a response partially matched their goal but substituted the original gesture when a response was incongruent. Persistence was also mediated by recipient intent to respond, with more sequences produced within competitive than affiliative contexts. Gestures within sequences were homogenous in semantic meaning and signallers continued until the response matched the assigned meaning of the initial gesture. Gestural sequence production was not primarily affective; gesture intensity (in terms of modality) did not increase within sequences. Chimpanzee gestural sequences emerged to achieve specific outcomes; given variability in recipient behaviour following initial gestures, signallers were flexible in their persistence towards these goals.

Usage and comprehension of manual gestures in wild chimpanzees

Flexibility is considered a defining feature of great ape gestural communication. Previous research has suggested that there is a ‘means–ends’ dissociation between gesture type and context, whereby one signal may be used across contexts and several signals used within the same context. Such flexibility in signal production demands contextual comprehension, whereby recipients may perceive the context-free message of a given manual gesture, but also decide how to respond by inferring the signallers goals from the accompanying context. We conducted naturalistic observations of wild East African chimpanzee, Pan troglodytes schweinfurthii, manual gestures, focusing on recipient perspective- during communicative interactions. Our results indicate that chimpanzees recognize the context-free meanings of gestures and they are also able to respond flexibly by inferring the meaning from the combination of gesture and context, including relative rank. When analysed at the level of gesture type, some gestures were tightly associated with dominant responses and outcomes. Chimpanzee manual gestures are primarily used for directing a recipients movement or attention but the motivation underlying these gestural requests is inferred by the recipient from the context.

Chimpanzees modify intentional gestures to coordinate a search for hidden food

Humans routinely communicate to coordinate their activities, persisting and elaborating signals to pursue goals that cannot be accomplished individually. Communicative persistence is associated with complex cognitive skills such as intentionality, because interactants modify their communication in response to anothers understanding of their meaning. Here we show that two language-trained chimpanzees effectively use intentional gestures to coordinate with an experimentally-naïve human to retrieve hidden food, providing some of the most compelling evidence to date for the role of communicative flexibility in successful coordination in nonhumans. Both chimpanzees (named Panzee and Sherman) increase the rate of non-indicative gestures when the experimenter approaches the location of the hidden food. Panzee also elaborates her gestures in relation to the experimenters pointing, which enables her to find food more effectively than Sherman. Communicative persistence facilitates effective communication during behavioural coordination and is likely to have been important in shaping language evolution.

Variation and context of yawns in captive chimpanzees (Pan troglodytes).

Primate yawns are usually categorized according to context (e.g. as a threat, anxious, or rest yawn), but there has been little consideration of whether these yawns are best regarded as a unitary behavior that only differs with respect to the context in which it is observed. This study examined the context and precise morphology of yawns in a group of 11 captive chimpanzees. Focal video sampling was used to describe the morphology and intensity of 124 yawns using ChimpFACS, a system for coding facial movements. Two distinct forms of yawn were identified, a full yawn and a yawn which is modified by additional actions that reduce the mouth aperture. These modified yawns may indicate some degree of voluntary control over facial movement in chimpanzees and, consequently, multiple functions of yawning according to context. To assess context effects, mean activity levels (resting, locomotion, and grooming) and scratching rates were compared one minute before and after each yawn. Locomotion was significantly increased following both types of yawn, whereas scratching rates significantly increased following modified yawns but decreased following full yawns. In terms of individual differences, males did not yawn more than females, although male yawns were of higher intensity, both in the degree of mouth opening and in the amount of associated head movement. These data indicate that yawning is associated with a change in activity levels in chimpanzees, but only modified yawns may be related to increased arousal. Different types of yawn can therefore be differentiated at the morphological level as well as context level. Am. J. Primatol. 72:262–269, 2010.

The repertoire and intentionality of gestural communication in wild chimpanzees

A growing body of evidence suggests that human language may have emerged primarily in the gestural rather than vocal domain, and that studying gestural communication in great apes is crucial to understanding language evolution. Although manual and bodily gestures are considered distinct at a neural level, there has been very limited consideration of potential differences at a behavioural level. In this study, we conducted naturalistic observations of adult wild East African chimpanzees (Pan troglodytes schweinfurthii) in order to establish a repertoire of gestures, and examine intentionality of gesture production, use and comprehension, comparing across manual and bodily gestures. At the population level, 120 distinct gesture types were identified, consisting of 65 manual gestures and 55 bodily gestures. Both bodily and manual gestures were used intentionally and effectively to attain specific goals, by signallers who were sensitive to recipient attention. However, manual gestures differed from bodily gestures in terms of communicative persistence, indicating a qualitatively different form of behavioural flexibility in achieving goals. Both repertoire size and frequency of manual gesturing were more affiliative than bodily gestures, while bodily gestures were more antagonistic. These results indicate that manual gestures may have played a significant role in the emergence of increased flexibility in great ape communication and social bonding.