More Than Just Kibbles: Keeper Familiarity and Food Can Affect Bonobo Behavior

Animal welfare in captivity is multifaceted, encompassing both internal states (e.g., anxiety) and external factors (e.g., management practices). While environmental factors have traditionally been the focus of research, recent studies highlight the importance of keeper interactions and food provisioning in influencing animal well-being. This is particularly relevant for cognitively and emotionally complex species like great apes. Previous research has shown that keeper-animal relationships can impact fearfulness, and that this interaction can be a form of enrichment. Furthermore, primates show behavioral variability depending on keeper familiarity, the number of keepers, and time spent with keepers. Food quantity and quality also influence welfare; restricted access can trigger negative behaviors. In primates, keeper interaction can affect social behavior; increased keeper presence can correlate with greater affiliation and reduced aggression/anxiety. Food limitations, conversely, can increase food-seeking behaviors and aggression. The type of food can also influence behavior, potentially increasing affiliation or competition. Great apes, particularly, show varying degrees of gestural communication depending on food presence and keeper familiarity. Bonobos, closely related to humans, are typically known for tolerance and peaceful interactions, though aggression can increase around high-quality food. They utilize play and sociosexual interactions in social bonding and tension regulation. Considering these observations, this study aimed to investigate how keeper familiarity and food type influence specific bonobo behaviors, focusing on anxiety, sociosexual interactions, gestures, play, and aggression.

The literature review extensively examines the impact of keeper interactions and food on primate behavior, particularly in great apes. Studies show that positive interactions with keepers can reduce anxiety and increase affiliative behaviors in various primate species, including marmosets, chimpanzees, gorillas, and baboons. Conversely, food scarcity or competition over high-value resources can lead to increased anxiety and aggression. The quality of food can also affect behavior, influencing both social interaction and play. In great apes, gestural communication is frequently employed to obtain desired resources from both conspecifics and humans, with familiarity playing a key role in the success of these requests. Bonobo research emphasizes their generally tolerant nature and the use of sociosexual behavior for tension regulation. Existing literature, however, does not fully elucidate the complex interplay between keeper familiarity and food type on the emotional and social lives of bonobos. The study utilizes these findings to build specific predictions regarding the relationship between bonobo behavior and the variables being studied.

This study involved a three-month observational study of 17 bonobos (various ages and sexes) housed at La Vallée des Singes, France. The group had access to both indoor and outdoor enclosures. Four keepers (two highly familiar and two less familiar) managed the bonobos, providing food four times daily. Data collection occurred daily via video recordings, focusing on periods when the bonobos were outdoors. The all-occurrences sampling method was employed to extract behavioral data, focusing on anxiety (scratching, yawning), sociosexual interactions, play, aggression, and requesting gestures. One coder, who underwent extensive training, performed the video analysis. Two-minute time slots were randomly selected under three conditions: keeper present/food unavailable; keeper present/food available; keeper absent/food unavailable. A total of 118 video sequences (equally distributed across conditions) were analyzed. Keepers were categorized as more or less familiar based on their experience with bonobos. Food was categorized as absent, low-quality (fruit/vegetables), and high-quality (kibbles). The negative binomial distribution was selected for data analysis based on the Bayesian Information Criterion (BIC). Generalized linear models (GLMs) were used to analyze behavioral frequencies. Initially, a GLM assessed the impact of keeper presence and food type. A second GLM, where the first model was significant, tested keeper familiarity, controlling for keeper sex. Finally, a third GLM, if the second model was significant, included keeper identity as a fixed factor. Likelihood ratio tests evaluated model significance, and post-hoc Tukey tests, corrected using Bonferroni's method, performed pairwise comparisons for food type. Effect sizes were calculated to quantify the influence of predictors.

Generalized linear model analyses revealed significant effects of keeper presence, familiarity, and food type on various bonobo behaviors. Anxiety-related behaviors were significantly higher in the keeper's presence without food (likely due to food anticipation), indicating that the mere presence of the keeper, linked to feeding, increased anxiety rather than reduced it. Contrary to initial predictions, the frequency of sociosexual interactions was higher in the presence of the keeper, particularly familiar keepers, and was also significantly higher in the absence of food, suggesting its use as a tension-regulation mechanism in the anticipation of food. The number of requesting gestures increased when keepers were present, especially familiar keepers, and was higher with low-quality, easily catchable food (fruit and vegetables), supporting the idea of targeted communication for readily available resources. Play behavior, however, did not show significant changes based on the factors considered, possibly due to the relatively short time windows involved. In contrast, aggression levels significantly increased with high-quality food, regardless of keeper presence, suggesting competition over a highly valued resource. Statistical analysis shows that in all cases, the full models were significantly different than the null models.

The findings demonstrate a complex relationship between bonobo behavior, keeper familiarity, and food provisioning. The unexpected increase in anxiety in the presence of a keeper highlights the potential for stress associated with anticipation, even with familiar caregivers. The increased sociosexual interactions in the keeper's presence and food absence support the hypothesis that such behavior serves as an anxiety buffer. The finding that bonobos used more gestures to obtain low-quality, easily-accessible food suggests a strategic communication approach based on resource availability and accessibility. The lack of significant play variation may be attributed to the short time frame of the observations. The increased aggression observed with high-quality food confirms the resource-based nature of this behavior. These results collectively emphasize the importance of both keeper familiarity and food type on bonobo welfare, suggesting that a holistic approach is necessary for optimizing captive management.

This study provides valuable insights into the complex interplay between keeper-animal interactions, food availability and bonobo behavior. The results highlight the importance of considering both environmental and social factors in optimizing captive welfare. Future research should explore the long-term effects of keeper familiarity on bonobo well-being, the effects of food provisioning schedules, and the potential of interventions to further enhance captive management strategies. A more detailed investigation of inter-individual differences in how bonobos respond to food and keepers could also provide a deeper understanding of individual welfare.

The study's limitations include the relatively short observation windows (two-minute slots), which may not fully capture the full spectrum of behavioral responses. Furthermore, the study focused on a single bonobo group at one location. Future research could benefit from expanding the sample size to include more bonobo groups and locations to improve generalizability. The study didn't investigate other factors that may influence welfare, such as social dynamics within the group beyond immediate interactions with food or the keeper.