Perception of available space during chimpanzee introductions: Number of accessible areas is more important than enclosure size.

Restricting animals to different areas of their enclosure, for both brief and extended durations, is a key element of animal management practices. With such restrictions, available space decreases and the choices the animals can make are more limited, particularly in relation to social dynamics. When unfamiliar individuals are introduced to each other, group dynamics can be unpredictable and understanding space usage is important to facilitate successful introductions. We studied the behavioral, welfare-related responses of two groups of zoo-housed chimpanzees (n = 22) as they were introduced to each other and experienced a variety of enclosure restrictions and group composition changes. Our analysis of available space while controlling for chimpanzee density, found that arousal-related scratching and yawning decreased as the number of enclosure areas (separate rooms) available increased, whereas only yawning decreased as the amount of available space (m(2)) increased. Allogrooming, rubbing, and regurgitation/reingestion rates remained constant as both the number of enclosure areas and amount of space changed. Enclosure space is important to zoo-housed chimpanzees, but during introductions, a decrease in arousal-related scratching indicates that the number of accessible areas is more important than the total amount of space available, suggesting that it is important to provide modular enclosures that provide choice and flexible usage, to minimize the welfare impact of short- and long-term husbandry needs.

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.

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.

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.

Waiting for more: the performance of domestic dogs (Canis familiaris) on exchange tasks.

Five domestic dogs (Canis familiaris) were tested in a cooperative exchange task with an experimenter, as previously tested in non-human primates. In the first task, the dogs exchanged to maximise payoffs when presented with food items of differing quality. All consistently exchanged lower-value for higher-value rewards, as determined by their individual food preference, and exchanges corresponded significantly with the spontaneous preferences of three dogs. Next, all subjects demonstrated an ability to perform two and three exchanges in succession, to gain both qualitative and quantitatively increased rewards (group mean = 72 and 92% successful triple exchanges, respectively). Finally, the ability to delay gratification over increasing intervals was tested; the dogs kept one food item to exchange later for a larger item. As previously reported in non-human primates, there was considerable individual variation in the tolerance of delays, between 10 s and 10 min for the largest rewards. For those who reached longer time lags (>40 s), the dogs gave up the chance to exchange earlier than expected by each subject's general waiting capacity; the dogs anticipated delay duration and made decisions according to the relative reward values offered. Compared to primates, dogs tolerated relatively long delays for smaller value rewards, suggesting that the socio-ecological history of domestic dogs facilitates their performance on decision-making and delay of gratification tasks.

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.

How do African grey parrots (Psittacus erithacus) perform on a delay of gratification task?

Humans and other animals often find it difficult to choose a delayed reward over an immediate one, even when the delay leads to increased pay-offs. Using a visible incremental reward procedure, we tested the ability of three grey parrots to maintain delay of gratification for an increasingly valuable food pay-off. Up to five sunflower seeds were placed within the parrot's reach, one at a time, at a rate of one seed per second. When the parrot took a seed the trial was ended and the birds consumed the accumulated seeds. Parrots were first tested in daily sessions of ten trials and then with single daily trials. For multiple trial sessions, all three parrots showed some limited improvement across 30 sessions. For single trial sessions, only one parrot showed any increase in seed acquisition across trials. This parrot was also able to consistently obtain two or more seeds per trial (across both multiple and single trial conditions) but was unable to able to wait 5 s to obtain the maximum number of seeds. This parrot was also tested on a slower rate of seed presentation, and this significantly reduced her mean seed acquisition in both multiple and single trial conditions, suggesting that both value of reward available and delay duration impact upon self-control. Further manipulation of both the visibility and proximity of seeds during delay maintenance had little impact upon tolerance of delays for both parrots tested in this condition. This task demanded not just a choice of delayed reward but the maintenance of delayed gratification and was clearly difficult for the parrots to learn; additional training or alternative paradigms are required to better understand the capacity for self-control in this and other species.

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.

Opportunities for refinement in neuroscience: Indicators of wellness and post-operative pain in laboratory macaques.

Being able to assess pain in nonhuman primates undergoing biomedical procedures is important for preventing and alleviating pain, and for developing better guidelines to minimise the impacts of research on welfare in line with the 3Rs principle of Refinement. Nonhuman primates are routinely used biomedical models however it remains challenging to recognise negative states, including pain, in these animals. This study aimed to identify behavioural and facial changes that could be used as pain or general wellness indicators in the rhesus macaque (Macaca mulatta). Thirty-six macaques scheduled for planned neuroscience procedures were opportunistically monitored at four times: Pre-Operative (PreOp), Post-Operative (PostOp) once the effects of anaesthesia had dissipated, Pre-Analgesia (PreAn) on the subsequent morning prior to repeating routine analgesic treatment, and Post-Analgesia (PostAn) following administration of analgesia. Pain states were expected to be absent in PreOp, moderate in PreAn, and mild or absent in PostOp and PostAn when analgesia had been administered. Three potential pain indicators were identified: lip tightening and chewing, which were most likely to occur in PreAn, and running which was least likely in PreAn. Arboreal behaviour indicated general wellness, while half-closed eyes, leaning of the head or body shaking indicated the opposite. Despite considerable individual variation, behaviour and facial expressions could offer important indicators of pain and wellness and should be routinely quantified, and appropriate interventions applied to prevent or alleviate pain, and promote positive welfare.

Perceived differences between chimpanzee (Pan troglodytes) and human (Homo sapiens) facial expressions are related to emotional interpretation.

Human face perception is a finely tuned, specialized process. When comparing faces between species, therefore, it is essential to consider how people make these observational judgments. Comparing facial expressions may be particularly problematic, given that people tend to consider them categorically as emotional signals, which may affect how accurately specific details are processed. The bared-teeth display (BT), observed in most primates, has been proposed as a homologue of the human smile (J. A. R. A. M. van Hooff, 1972). In this study, judgments of similarity between BT displays of chimpanzees (Pan troglodytes) and human smiles varied in relation to perceived emotional valence. When a chimpanzee BT was interpreted as fearful, observers tended to underestimate the magnitude of the relationship between certain features (the extent of lip corner raise) and human smiles. These judgments may reflect the combined effects of categorical emotional perception, configural face processing, and perceptual organization in mental imagery and may demonstrate the advantages of using standardized observational methods in comparative facial expression research.

"You Think You're Helping Them, But They're Helping You Too": Experiences of Scottish Male Young Offenders Participating in a Dog Training Program.

Interaction with animals can be beneficial to humans and animal-assisted interventions (AAIs) are increasingly popular in a range of contexts. Dog training programs (DTPs) are the most popular form of AAI in custodial contexts; prisoners often have multiple needs and DTPs seem to facilitate a diverse range of positive outcomes, including improvements in well-being, behavior, and offending behavior. However, evidence on the efficacy of prison-based DTPs is still limited and these evaluations often lack detail or methodological rigor. We examined the experiences of male young offenders (N = 70) using thematic analysis of semi-structured interviews conducted following completion of a DTP. The themes that emerged indicated a broad range of inter-related experiences and positive outcomes. The most prevalent theme related to their experiences with Dogs (including feelings and attitudes), and there were perceived improvements categorized as: Positive Effects (including mood and well-being), Motivation, Charitable Purpose, Self-Efficacy, Improved Skills, Impulsivity, and Emotional Management. These themes mapped well onto outcomes previously identified in research on DTPs, and to the program's core aims of improving behavior, educational engagement, employability, and well-being. The diversity and nature of these themes indicates that DTPs have considerable potential to engage and benefit those individuals with multiple needs, such as young offenders, and ultimately to achieve positive long-term outcomes with significant social, health, and economic impact.

Facial expression: An under-utilised tool for the assessment of welfare in mammals.

Animal welfare is a key issue for industries that use or impact upon animals. The accurate identification of welfare states is particularly relevant to the field of bioscience, where the 3Rs framework encourages refinement of experimental procedures involving animal models. The assessment and improvement of welfare states in animals depends on reliable and valid measurement tools. Behavioral measures (activity, attention, posture and vocalization) are frequently used because they are immediate and non-invasive, however no single indicator can yield a complete picture of the internal state of an animal. Facial expressions are extensively studied in humans as a measure of psychological and emotional experiences but are infrequently used in animal studies, with the exception of emerging research on pain behavior. In this review, we discuss current evidence for facial representations of underlying affective states, and how communicative or functional expressions can be useful within welfare assessments. Validated tools for measuring facial movement are outlined, and the potential of expressions as honest signals is discussed, alongside other challenges and limitations to facial expression measurement within the context of animal welfare. We conclude that facial expression determination in animals is a useful but underutilized measure that complements existing tools in the assessment of welfare.

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.

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 testing with a similar paradigm in which gaze cues preceded a target identification task [Fagot, J., Deruelle, C., 2002. Perception of pictorial gaze by baboons (Papio papio). J. Exp. Psychol. 28, 298-308]. When tested with either pictorial stimuli or interactants, nonhuman 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.

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.

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.

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 another's understanding of their meaning. Here we show that two language-trained chimpanzees effectively use intentional gestures to coordinate with an experimentally naive 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 experimenter's 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.

Measurement of eye-gaze in chimpanzees (Pan troglodytes).

Gaze cues are used as an index of social cognition in primates, yet the sensitivity to different forms of gaze, and consequently the cues required to test gaze-following abilities remain understudied. Whereas the eye is attributed special signal value in humans, the camouflaged ocular morphology of non-human primates has led to the consensus that head orientation may be a more salient cue. This study presents the first documentation of the surface eye movements of the chimpanzee, Pan troglodytes, in order to determine the behavioral forms of eye-gaze and their saliency as signals, document their functional variation, and address the signal value of the eyes distinct from head orientation. Movements of the eye were identified as Scan (continuous movement), Glance (a single movement <1 sec), or Fixate (no movement). Scans, glances, and fixations were reliably detected by humans during live observation and from video (Cohen's kappa over 0.70) and, therefore, are likely also to be detected by conspecifics. Eye-gaze comprised a nonunitary measure of visual attention, reflecting the attentional task demands of different activities. Specifically, chimpanzees spent significantly more time scanning while feeding and resting, than grooming, F(2,28) = 10.23, P<0.001, and spent significantly more time fixating while grooming, than feeding or resting, F(2,28) = 7.52, P<0.01. Further, eye-gaze was often incongruent with head movement, varying significantly with the form of eye-gaze: incongruence was found during 12-21% of fixations, during 42-49% of scans, and during 70-100% of glances, F(2,16) = 30.17, P<0.001. These findings provide the basis for discrimination of the adaptive significance of gaze-processing abilities with emphasis on sensitivity to eye-gaze distinct from head orientation. If we are to continue exploring gaze-processing abilities in primates, then we need greater consideration of the precise nature of the signals themselves. Here we present evidence for special consideration of the eyes as a salient signal in P. troglodytes.

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 [(1872/1998). The expression of the emotions in man and animals (3rd ed.). New York: Oxford University Press] 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. FACS [Ekman & Friesen (1978). Facial action coding system. CA: Consulting Psychology Press] 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.