Avoidance of biological contaminants through sight, smell and touch in chimpanzees

Abstract

Avoiding biological contaminants is a well-known manifestation of the adaptive system of disgust. In theory, animals evolved with such a system to prevent pathogen and parasite infection. Bodily products are human-universal disgust elicitors, but whether they also elicit avoidance behaviour in non-human primates has yet to be tested. Here, we report experimental evidence that potential exposure to biological contaminants (faeces, blood, semen), as perceived via multiple sensory modalities (visual, olfactory, tactile), might influence feeding decisions in chimpanzees (Pan troglodytes troglodytes)—our closest phylogenetic relatives. Although somewhat mixed, our results do show increased latencies to feed, tendencies to maintain greater distances from contaminants and/or outright refusals to consume food in test versus control conditions. Overall, these findings are consistent with the parasite avoidance theory of disgust, although the presence of biological contaminants did not preclude feeding entirely. The avoidance behaviours observed hint at the origins of disgust in humans, and further comparative research is now needed.

Primate Infectious Disease Ecology: Insights and Future Directions at the Human-Macaque Interface

“…More research has focused on the impact of (4) parasites in primate conservation and management-while some deal with the implications of introduced species on the prevalence and diversity of parasites in indigenous primates (Petrášová et al 2010(Petrášová et al , 2011, other research has attempted to quantify differences in parasite richness or diversity in primates living in varying degrees of human influence or in relation to their threatened status(es) (Bublitz et al 2015;Chapman et al 2006a;Gillespie et al 2005;Goldberg et al 2007;Kowalewski et al 2011). Finally, emerging lines of research have focused on (5) primate counterstrategies, including avoidance behaviors to minimize exposure to parasites (Amoroso et al 2017;Poirotte et al 2017Poirotte et al , 2019Sarabian and MacIntosh 2015;Sarabian et al 2017), and self-medication that removes or minimizes the impact of an infection on the host (Huffman 2016).…”

Social neuroscience of disgust

“…There is evidence that odor cues are also used to recognize and socially avoid infected same‐ and opposite‐sex conspecifics in humans and non‐human primates . In both humans and rodents stimulation of the immune system by systemic administration of LPS, results in a coordinated set of adaptive behavioral responses termed “sickness behavior”.…”

“…There is evidence that odor cues are also used to recognize and socially avoid infected same-and opposite-sex conspecifics in humans and non-human primates. 16,17,36,46 In both humans and rodents stimulation of the immune system by systemic administration of LPS, results in a coordinated set of adaptive behavioral responses termed "sickness behavior". Sickness behavior constitutes an array of symptoms exhibited by animals during the course of infection, including fever, hypoactivity, reduced food and water intake and reduced social and exploratory behavior.…”

“…Social cognition involves not only successfully assessing other individuals and their behavior and condition (ie, actual or potential infection status and the risk of contamination they present), but also rapidly deciding whether, when, where and how to interact with them . 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 …”

“…11,15 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. 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.…”