Feeding decisions under contamination risk in bonobos

Abstract

Threats from parasites and pathogens are ubiquitous, and many use pathways that exploit host trophic interactions for their transmission. As such, host organisms have evolved a behavioural immune system to facilitate contamination-risk assessment and avoidance of potential contaminants in various contexts, including feeding. Detecting pathogen threats can rely on different sensory modalities allowing animals to screen for a wide array of contaminants. Here, we present a series of experiments in which bonobos showed clear avoidance of contaminated food items, and were sensitive to risk along a contamination probability gradient. Across experiments, bonobos appeared to use multisensorial cues to inform their feeding decisions. In addition, bonobos showed reduced tactile, gustatory and tool use activities when in the presence of contaminant versus control odours in a challenging foraging context. Our experiments build on previous work conducted in Japanese macaques and chimpanzees aiming at a better understanding of the ways in which the behavioural immune system operates in primates.This article is part of the Theo Murphy meeting issue 'Evolution of pathogen and parasite avoidance behaviours'.

Divergent strategies in faeces avoidance between two cercopithecoid primates

“…Other animal species, however, such as pigs, dogs and rabbits exhibit coprophagy to acquire certain digestive enzymes lacking in their diet, obtain nutrients that were unabsorbed in the gastrointestinal tract during the first passage and/or to develop their microbiome [13]. However, it was only very recently that scientists started testing whether faeces or other faecally contaminated substrates elicit avoidance in non-human primates [14][15][16][17][18][19]. This group of animals has a popularized reputation for being rather liberal when it comes to their disposition towards faeces, owing to the many anecdotal reports of coprophagy, throwing faeces and even 'painting' their enclosure walls or other substrates with faeces [20,21].…”

Social neuroscience of disgust

“…Pathogen/parasite and infection avoidance behaviors of hosts can range from either directly avoiding or removing parasites or pathogen themselves, avoiding conspecifics with signs of infection or avoiding toxins and contaminated areas . Hosts can avoid interacting with individuals with whom they are likely to share parasites, especially if the conspecifics show signs of infection (eg, rats avoid interacting with bacterial treated conspecifics, primates avoid grooming group members infected by orofecally transmitted parasites). If hosts can detect infective and threatening parasites they can avoid them directly (eg, mice self‐bury to avoid biting and bot flies, cattle enter ponds to evade warble flies .…”

“…Similar disgust responses and behavioral avoidance responses to fecal materials are also seen in primates. Bonobos that were offered either clean apple slices, apple slices covered in either feces or soil and placed at various distances from fresh feces tended to avoid the contaminated fruit with the likelihood that they would eat a piece of fruit rising as its distance from the source of contamination increased . These responses in part involved olfaction as the bonobos were less likely to reach for food in the presence of aversive odors associated with contamination.…”

“…For example mandrills and chimpanzees are able to gauge on the basis of social cues the infection status of their group members avoiding the parasite contaminated feces of neighbors and refraining from grooming infected conspecifics . Similarly, bonobos that are exposed to food contaminated with potentially infected conspecific feces modify their feeding decisions to minimize infection risk …”

“…16,17 Similarly, bonobos that are exposed to food contaminated with potentially infected conspecific feces modify their feeding decisions to minimize infection risk. 18 Here we briefly consider the social neuroscience of disgust.…”