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.

Learning with lacertids: Studying the link between ecology and cognition within a comparative framework.

Cognition is an essential tool for animals to deal with environmental challenges. Nonetheless, the ecological forces driving the evolution of cognition throughout the animal kingdom remain enigmatic. Large-scale comparative studies on multiple species and cognitive traits have been advanced as the best way to facilitate our understanding of cognitive evolution, but such studies are rare. Here, we tested 13 species of lacertid lizards (Reptilia: Lacertidae) using a battery of cognitive tests measuring inhibitory control, problem-solving, and spatial and reversal learning. Next, we tested the relationship between species' performance and (a) resource availability (temperature and precipitation), habitat complexity (Normalized Difference Vegetation Index), and habitat variability (seasonality) in their natural habitat and (b) their life history (size at hatching and maturity, clutch size, and frequency). Although species differed markedly in their cognitive abilities, such variation was mostly unrelated to their ecology and life history. Yet, species living in more variable environments exhibited lower behavioral flexibility, likely due to energetic constrains in such habitats. Our standardized protocols provide opportunities for collaborative research, allowing increased sample sizes and replication, essential for moving forward in the field of comparative cognition. Follow-up studies could include more detailed measures of habitat structure and look at other potential selective drivers such as predation.

Drivers of Dyadic Cofeeding Tolerance in Pan: A Composite Measure Approach.

This study aimed to construct a composite model of Dyadic Cofeeding Tolerance (DCT) in zoo-housed bonobos and chimpanzees using a validated experimental cofeeding paradigm and to investigate whether components resulting from this model differ between the two species or vary with factors such as sex, age, kinship and social bond strength. Using dimension reduction analysis on five behavioral variables from the experimental paradigm (proximity, aggression, food transfers, negative food behavior, participation), we found a two-factor model: "Tolerant Cofeeding" and "Agonistic Cofeeding". To investigate the role of social bond quality on DCT components alongside species effects, we constructed and validated a novel relationship quality model for bonobos and chimpanzees combined, resulting in two factors: Relationship Value and Incompatibility. Interestingly, bonobos and chimpanzees did not differ in DCT scores, and sex and kinship effects were identical in both species but biased by avoidance of the resource zone by male-male dyads in bonobos. Social bonds impacted DCT similarly in both species, as dyads with high Relationship Value showed more Tolerant Cofeeding, while dyads with higher Relationship Incompatibility showed more Agonistic Cofeeding. We showed that composite DCT models can be constructed that take into account both negative and positive cofeeding behavior. The resulting DCT scores were predicted by sex, kinship and social bonds in a similar fashion in both Pan species, likely reflecting their adaptability to changing socio-ecological environments. This novel operational measure to quantify cofeeding tolerance can now be applied to a wider range of species in captivity and the wild to see how variation in local socio-ecological circumstances influences fitness interdependence and cofeeding tolerance at the dyadic and group levels. This can ultimately lead to a better understanding of how local environments have shaped the evolution of tolerance in humans and other species.

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.