Qualitative Behavioural Assessment of bonobo emotional expressivity across observer groups and zoo housing environments.

Human evaluation of animal emotional expressivity can inform animal welfare. Qualitative Behavioural Assessment (QBA) has been applied to domesticated and some non-domesticated animals, but its use in primates is limited despite their emotional expressivity. We aimed to develop and apply a QBA for bonobos (Pan paniscus) through two consecutive studies. We applied Free Choice Profiling (FCP) and the Fixed List methodology, respectively, in Study 1 and 2, and invited students and bonobo experts to rate video clips of zoo-living bonobos of different sexes and age classes, and before and after moving to a new enclosure. In Study 1, students described dimension 1 as ranging from 'quiet/calm' to 'angry/active' and dimension 2 from 'sad/anxious' to 'happy/loving'. Experts described dimension 1 ranging from 'quiet/relaxed' to 'nervous/alert' and dimension 2 from 'nervous/bored' to 'playful/happy'. Using a fixed list of descriptors, informed by findings from Study 1, students in Study 2 described dimension 1 as ranging from 'quiet/calm' to 'agitated/frustrated', and dimension 2 from 'sad/stressed' to 'happy/positively engaged'. Experts described dimension 1 as ranging from 'quiet/calm' to 'active/excited', and dimension 2 from 'sad/bored' to 'happy/positively engaged'. Students scored adults as more 'calm/quiet' and experts scored subadults as more 'happy/positively engaged'. Additionally, experts in Study 2 rated bonobos as more 'active/excited' in their new enclosure. Reliability was moderate to good for the dimensions. Additionally, animal-directed empathy of observers influenced QBA scores. This is the first time, FCP has been successfully used as a method to study primate emotional expressivity. Our findings show the promise of employing QBA in primate studies and in industry, with validation of additional metrics to enable its use for welfare-monitoring purposes.

Visually assessed body condition shows high heritability in a pedigreed great ape population.

Body condition, a measure for relative fat mass, is associated with primate health, fitness, and overall welfare. Body condition is often influenced by dietary factors, age, and/or sex, but several body condition measures (body weight, weight-to-height ratios, and so on) also show high heritability across primate species, indicating a role of genetic effects. Although different measures for body condition exist, many require direct handling of animals, which is invasive, time-consuming, and expensive, making them impractical in wild and captive settings. Therefore, noninvasive visual body condition score (BCS) systems were developed for various animal species, including macaques and chimpanzees, to visually assess relative fat mass. Here we evaluate the utility of a visual BCS system in bonobos by assessing (1) inter-rater reliability, (2) links with body mass, a traditional hands-on measure of condition, and (3) the factors driving individual variation in BCS. We adapted the chimpanzee BCS system to rate 76 bonobos in 11 European zoos (92% of the adult population). Inter-rater reliability was high (s* = 0.948), BCSs were positively associated with body mass (ß = 0.075) and not predicted by diet, sex, or age, nor were they associated with a higher abundance of obesity-related diseases. Instead, BCSs showed high levels of heritability (h2 = 0.637), indicating that a majority of body condition variation in bonobos is attributable to genetic similarity of the individuals. This is in line with reported h2 -values for traditional body condition measures in primates and provides support for the reliability of visual BCS systems in great apes. The results of this study emphasize an often unanticipated role of genetics in determining primate body fat and health that has implications for the management of captive primates. Application of this tool in wild populations would aid to unravel environmental from genetic drivers of body condition variation in primates.

Multi-group analysis of grooming network position in a highly social primate.

Individual variation in complex social behavioral traits, like primate grooming, can be influenced by the characteristics of the individual and those of its social group. To better grasp this complexity, social network analysis can be used to quantify direct and indirect grooming relationships. However, multi-group social network studies remain rare, despite their importance to disentangle individual from group-level trait effects on grooming strategies. We applied social network analysis to grooming data of 22 groups of zoo-housed bonobos and investigated the impact of three individual (sex, age, and rearing-history) and two group-level traits (group size and sex ratio) on five social network measures (out-strength, in-strength, disparity, affinity, and eigenvector centrality). Our results showed age-effects on all investigated measures: for females, all measures except for affinity showed quadratic relationships with age, while in males, the effects of age were more variable depending on the network measure. Bonobos with atypical rearing histories showed lower out-strength and eigenvector centrality, while in-strength was only impacted by rearing history in males. Group size showed a negative association with disparity and eigenvector centrality, while sex ratio did not influence any of the investigated measures. Standardization for group size did not impact the effects of sex and age, indicating the robustness of these findings. Our study provides comprehensive insights into the complexity of grooming behavior in zoo-housed bonobos, and underlines the importance of multi-group analyses for the generalizability of social network analysis results for species as a whole.

Evaluating Self-Directed Behaviours and Their Association with Emotional Arousal across Two Cognitive Tasks in Bonobos (Pan paniscus).

Self-directed behaviours (SDBs) are widely used as markers of emotional arousal in primates, and are commonly linked to negative arousal, or are used as indicators of stress or poor welfare. However, recent studies suggest that not all SDBs have the same function. Moreover, lateralisation in the production of these behaviours has been suggested to be associated with emotional processing. Hence, a better understanding of the production and the asymmetry of these displacement behaviours is needed in a wider range of species in order to confirm their reliability as indicators of emotional arousal. In the current study, we experimentally evaluated the production and asymmetry of SDBs in zoo-housed bonobos during two cognitive touchscreen tasks. Overall, nose wipes were most commonly observed, followed by gentle self-scratches, and rough self-scratches. The rates of nose wipes and rough self-scratches increased with incorrect responses, suggesting that these behaviours indicate arousal and possibly frustration. Rough self-scratching was additionally more directed towards the left hemispace after incorrect responses. In contrast, gentle self-scratching increased after correct responses in one study, possibly linking it with positive arousal. We also tested if left-handed bonobos showed greater behavioural reactivity towards incorrect responses, but found no evidence to confirm this hypothesis. Our results shed light on potential different mechanisms behind separate SDBs. We therefore provide nuance to the use of SDBs as indicator of emotional arousal in bonobos.

Self-interest precludes prosocial juice provisioning in a free choice group experiment in bonobos.

Previous studies on prosociality in bonobos have reported contrasting results, which might partly be explained by differences in experimental contexts. In this study, we implement a free choice group experiment in which bonobos can provide fruit juice to their group members at a low cost for themselves. Four out of five bonobos passed a training phase and understood the setup and provisioned fruit juice in a total of 17 dyads. We show that even in this egalitarian group with a shallow hierarchy, the majority of pushing was done by the alpha female, who monopolized the setup and provided most juice to two adult females, her closest social partners. Nonetheless, the bonobos in this study pushed less frequently than the chimpanzees in the original juice-paradigm study, suggesting that bonobos might be less likely than chimpanzees to provide benefits to group members. Moreover, in half of the pushing acts, subjects obtained juice for themselves, suggesting that juice provisioning was partly driven by self-regarding behavior. Our study indicates that a more nuanced view on the prosocial food provisioning nature of bonobos is warranted but based on this case study, we suggest that the observed sex differences in providing food to friends corresponds with the socio-ecological sex difference in cooperative interactions in wild and zoo-housed bonobos.

Adult bonobos show no prosociality in both prosocial choice task and group service paradigm.

Previous studies reported contrasting conclusions concerning bonobo prosociality, which are likely due to differences in the experimental design, the social dynamics among subjects and characteristics of the subjects themselves. Two hypotheses have been proposed to explain the occurrence of prosociality in animals: the cooperative breeding hypothesis and the self-domestication hypothesis. While the former predicts low levels of prosociality in bonobos because they are non-cooperative breeders, the latter predicts high levels of prosociality because self-domestication has been proposed to select for high levels of tolerance in this species. Here, we presented a group of thirteen bonobos with two platform food-provisioning tasks: the prosocial choice task (PCT) and the group service paradigm (GSP). The latter has so far never been applied to bonobos. To allow for free choice of participation and partner, we implemented both tasks in a group setting. Like in previous PCT studies, bonobos did not choose the prosocial option more often when a group member could benefit vs not benefit. In the GSP, where food provisioning is costly, only subadult bonobos showed a limited amount of food provisioning, which was much lower than what was previously reported for chimpanzees. In both experiments, adult subjects were highly motivated to obtain rewards for themselves, suggesting that bonobos behaved indifferently to the gains of group members. We suggest that previous positive food-provisioning prosociality results in bonobos are mainly driven by the behaviour of subadult subjects. The lack of prosociality in this study corresponds to the hypothesis that proactive food provisioning co-occurs with cooperative breeding and suggests that proactive prosociality might not be part of the self-domestication syndrome in bonobos.

Social and nonsocial stimuli alter the performance of bonobos during a pictorial emotional Stroop task.

The emotional Stroop task is a paradigm commonly applied in human studies to investigate how emotionally laden stimuli interfere with cognitive processes. Recent modifications of this task have enabled researchers to study similar Stroop effects in zoo-housed primates. Across three experiments using a pictorial emotional Stroop task, we investigated if the attention of bonobos was influenced by social (facial expressions during play, conflict, and neutral events) and nonsocial stimuli (a preferred food item, predator, and flower). Four bonobos successfully learned to complete the task on a touchscreen. First, we tested the bonobos on a standard color-interference Stroop task and found that they made more errors in color-congruent trials. Second, we included facial expressions of unknown conspecifics and found that it took the bonobos longer to select targets with play facial expressions compared to neutral expressions. Last, we included objects and found that the negative, positive and neutral objects altered performance. Our findings show that the cognitive processes of bonobos are influenced by both relevant social and nonsocial stimuli. Specifically, play faces interfered with the bonobos' attention suggesting that these facial expressions form a salient stimulus within bonobo society. Nonsocial stimuli also altered accuracy and reaction times during the task which may be explained by their evolutionary relevance. Our results help us to better understand the (socio-)emotional competencies of bonobos and how they respond to external stimuli. Future studies can further examine how a wider range of biologically relevant stimuli interfere with attentional processes in bonobos.

Respiratory Disease Risk of Zoo-Housed Bonobos Is Associated with Sex and Betweenness Centrality in the Proximity Network.

Infectious diseases can be considered a threat to animal welfare and are commonly spread through both direct and indirect social interactions with conspecifics. This is especially true for species with complex social lives, like primates. While several studies have investigated the impact of sociality on disease risk in primates, only a handful have focused on respiratory disease, despite it being a major cause of morbidity and mortality in both wild and captive populations and thus an important threat to primate welfare. Therefore, we examined the role of social-network position on the occurrence of respiratory disease symptoms during one winter season in a relatively large group of 20 zoo-housed bonobos with managed fission-fusion dynamics. We found that within the proximity network, symptoms were more likely to occur in individuals with higher betweenness centrality, which are individuals that form bridges between different parts of the network. Symptoms were also more likely to occur in males than in females, independent of their social-network position. Taken together, these results highlight a combined role of close proximity and sex in increased risk of attracting respiratory disease, two factors that can be taken into account for further welfare management of the species.

Zoo Visitor Attitudes Are More Influenced by Animal Behaviour than Environmental Enrichment Appearance.

Decisions on environmental enrichment programmes are sometimes based on the assumption that non-natural or artificial looking items negatively affect visitor experiences. In this study, we developed a questionnaire to assess zoo visitor attitudes towards enrichment appearance in an outdoor walk-through enclosure for ring-tailed lemurs (Lemur catta). Naturalistic and artificial looking enrichment items were alternately provided in the enclosure. A total of 371 visitors filled out the questionnaire: 174 in the naturalistic and 197 in the artificial conditions. Both researchers and visitors conducted behavioural observations of the lemurs. Our results suggest that the appearance of the items did not have an effect on visitor attitudes and that visitors recognised both naturalistic and artificial items as enriching for the animals. Moreover, the behaviour and visibility of the lemurs had a greater effect on the visitors' attitudes. We suggest that during the design of enrichment items, less concern should be placed on the appearance of the items and more on their effect on animal behaviour. Ultimately, this would improve both animal welfare in captivity and the visitor experience.

Time-lag of urinary and salivary cortisol response after a psychological stressor in bonobos (Pan paniscus).

Cortisol is often measured as a marker for stress. Therefore, a profound validation of the time-lag between the stressor and the increase and peak in cortisol levels is needed. No study measured both the urinary and salivary cortisol time-lag after a psychological stressor. In this study, we used a frequent sampling study design to (1) describe the urinary and salivary cortisol pattern during a control day; and (2) characterize the induced excretion pattern of urinary and salivary cortisol after a psychological stressor in six zoo-housed bonobos. Liquid chromatography-tandem mass spectrometry was used to analyze 71 urine and 162 saliva samples collected on a control and a test day. We found that the time-lag between the stressor and the maximal cortisol concentration was similar in urine and saliva (160 min after the stressor). However, salivary cortisol after the stressor did show a faster and steeper increase than urinary cortisol. We also show inter-individual variation in the baseline and stress levels of cortisol, which should be considered in future cortisol studies. Our research highlights the importance of validation studies to confirm relevant sampling windows for cortisol sampling in order to obtain biologically meaningful results.

Low relationship quality predicts scratch contagion during tense situations in orangutans (Pongo pygmaeus).

Primates show various forms of behavioral contagion that are stronger between kin and friends. As a result, behavioral contagion is thought to promote group coordination, social cohesion, and possibly state matching. Aside from contagious yawning, little is known about the contagious effect of other behaviors. Scratching is commonly observed during arousal and as such may play a role within group dynamics. While the Bornean orangutan (Pongo pygmaeus) is commonly considered the least social great ape, orangutans do engage in social interactions. Therefore, their social organization makes them a suitable case for studying the social function of behavioral contagion. Through behavioral observations of captive orangutans, we recorded all yawn and scratch events together with the corresponding behavior of all bystander group-members. As yawning was rarely observed, no conclusions could be drawn regarding this behavior. Scratching was contagious and occurred within 90 s after the triggering scratch. Specifically, orangutans showed increased scratch contagion when they had seen a weakly bonded individual scratch during tense contexts. When the orangutan had not seen the triggering scratch, the contagiousness of scratching was not affected by context or relationship quality. Our results indicate that behavioral contagion is not simply higher between individuals with stronger social relationships, but that the contagiousness of behaviors may vary based on the context and on social factors. We discuss these findings in light of an adaptive function that may reduce aggression.