Disgust in animals and the application of disease avoidance to wildlife management and conservation.

Disgust is an adaptive system hypothesized to have evolved to reduce the risk of becoming sick. It is associated with behavioural, cognitive and physiological responses tuned to allow animals to avoid and/or get rid of parasites, pathogens and toxins. Little is known about the mechanisms and outcomes of disease avoidance in wild animals. Furthermore, given the escalation of negative human-wildlife interactions, the translation of such knowledge into the design of evolutionarily relevant conservation and wildlife management strategies is becoming urgent. Contemporary methods in animal ecology and related fields, using direct (sensory cues) or indirect (remote sensing technologies and machine learning) means, provide a flexible toolbox for testing and applying disgust at individual and collective levels. In this review/perspective paper, we provide an empirical framework for testing the adaptive function of disgust and its associated disease avoidance behaviours across species, from the least to the most social, in different habitats. We predict various trade-offs to be at play depending on the social system and ecology of the species. We propose five contexts in which disgust-related avoidance behaviours could be applied, including endangered species rehabilitation, invasive species, crop-raiding, urban pests and animal tourism. We highlight some of the perspectives and current challenges of testing disgust in the wild. In particular, we recommend future studies to consider together disease, predation and competition risks. We discuss the ethics associated with disgust experiments in the above contexts. Finally, we promote the creation of a database gathering disease avoidance evidence in animals and its applications.

Le dégoût est un système adaptatif supposé avoir évolué afin de réduire le risque de tomber malade. Il est associé à des réponses comportementales, cognitives et physiologiques adaptées pour permettre aux animaux d'éviter et/ou de se débarrasser des parasites, pathogènes et toxines. On sait peu de choses sur les mécanismes et les conséquences de l'évitement des maladies chez les animaux sauvages. Étant donné l'escalade des interactions négatives entre humains et faune, la traduction de ces connaissances dans la conception de stratégies de conservation et de gestion de la faune - prenant en considération l'évolution des espèces - devient urgente. Les méthodes contemporaines en écologie animale et dans les domaines connexes, utilisant des moyens directs (indices sensoriels) ou indirects (technologies de télédétection et apprentissage automatique), fournissent une boîte à outils flexible pour tester et appliquer le dégoût aux niveaux individuel et collectif. Dans cet article de revue/perspective, nous fournissons un cadre empirique pour tester la fonction adaptative du dégoût et les comportements associés d'évitement des maladies chez différentes espèces - des moins sociales aux plus sociales, et dans différents habitats. Nous prédisons divers compromis en fonction du système social et de l'écologie de l'espèce. Nous proposons cinq contextes dans lesquels les comportements d'évitement liés au dégoût pourraient être appliqués: la réhabilitation d'espèces menacées; les espèces envahissantes; les dommages aux cultures; les nuisibles urbains; et le tourisme animalier. Nous mettons en avant certaines perspectives et défis actuels de l'expérimentation sur le dégoût en milieu naturel. En particulier, nous recommandons la considération de plusieurs risques ensemble: maladie, prédation et compétition. Nous discutons également de l'éthique associée aux expériences sur le dégoût dans les contextes ci-dessus. Enfin, nous promouvons la création d'une base de données rassemblant les stratégies d'évitement des maladies chez les animaux et leurs applications.

Divergent strategies in faeces avoidance between two cercopithecoid primates.

Parasites constitute a major selective pressure which has shaped animal behaviour through evolutionary time. One adaption to parasites consists of recognizing and avoiding substrates or cues that indicate their presence. Among substrates harbouring infectious agents, faeces are known to elicit avoidance behaviour in numerous animal species. However, the function and mechanisms of faeces avoidance in non-human primates has been largely overlooked by scientists. In this study, we used an experimental approach to investigate whether aversion to faeces in a foraging context is mediated by visual and olfactory cues in two cercopithecoid primates: mandrills (Mandrillus sphinx) and long-tailed macaques (Macaca fascicularis). Visual and olfactory cues of faeces elicited lower food consumption rates in mandrills and higher food manipulation rates in long-tailed macaques. Both results support the infection-avoidance hypothesis and confirm similar tendencies observed in other primate species. More studies are now needed to investigate the divergence of avoidance strategies observed in non-human primates regarding food contamination.

Evolution of pathogen and parasite avoidance behaviours.

All free-living animals are subject to intense selection pressure from parasites and pathogens resulting in behavioural adaptations that can help potential hosts to avoid falling prey to parasites. This special issue on the evolution of parasite avoidance behaviour was compiled following a Royal Society meeting in 2017. Here we have assembled contributions from a wide range of disciplines including genetics, ecology, parasitology, behavioural science, ecology, psychology and epidemiology on the disease avoidance behaviour of a wide range of species. Taking an interdisciplinary and cross-species perspective allows us to sketch out the strategies, mechanisms and consequences of parasite avoidance and to identify gaps and further questions. Parasite avoidance strategies must include avoiding parasites themselves and cues to their presence in conspecifics, heterospecifics, foods and habitat. Further, parasite avoidance behaviour can be directed at constructing parasite-retardant niches. Mechanisms of parasite avoidance behaviour are generally less well characterized, though nematodes, rodents and human studies are beginning to elucidate the genetic, hormonal and neural architecture that allows animals to recognize and respond to cues of parasite threat. While the consequences of infection are well characterized in humans, we still have much to learn about the epidemiology of parasites of other species, as well as the trade-offs that hosts make in parasite defence versus other beneficial investments like mating and foraging. Finally, in this overview we conclude that it is legitimate to use the word 'disgust' to describe parasite avoidance systems, in the same way that 'fear' is used to describe animal predator avoidance systems. Understanding disgust across species offers an excellent system for investigating the strategies, mechanisms and consequences of behaviour and could be a vital contribution towards the understanding and conservation of our planet's ecosystems.This article is part of the Theo Murphy meeting issue 'Evolution of pathogen and parasite avoidance behaviours'.

Feeding decisions under contamination risk in bonobos.

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'.

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

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.

Modeling infection transmission in primate networks to predict centrality-based risk.

Social structure can theoretically regulate disease risk by mediating exposure to pathogens via social proximity and contact. Investigating the role of central individuals within a network may help predict infectious agent transmission as well as implement disease control strategies, but little is known about such dynamics in real primate networks. We combined social network analysis and a modeling approach to better understand transmission of a theoretical infectious agent in wild Japanese macaques, highly social animals which form extended but highly differentiated social networks. We collected focal data from adult females living on the islands of Koshima and Yakushima, Japan. Individual identities as well as grooming networks were included in a Markov graph-based simulation. In this model, the probability that an individual will transmit an infectious agent depends on the strength of its relationships with other group members. Similarly, its probability of being infected depends on its relationships with already infected group members. We correlated: (i) the percentage of subjects infected during a latency-constrained epidemic; (ii) the mean latency to complete transmission; (iii) the probability that an individual is infected first among all group members; and (iv) each individual's mean rank in the chain of transmission with different individual network centralities (eigenvector, strength, betweenness). Our results support the hypothesis that more central individuals transmit infections in a shorter amount of time and to more subjects but also become infected more quickly than less central individuals. However, we also observed that the spread of infectious agents on the Yakushima network did not always differ from expectations of spread on random networks. Generalizations about the importance of observed social networks in pathogen flow should thus be made with caution, since individual characteristics in some real world networks appear less relevant than they are in others in predicting disease spread. Am. J. Primatol. 78:767-779, 2016. © 2016 Wiley Periodicals, Inc.

Hygienic tendencies correlate with low geohelminth infection in free-ranging macaques.

Parasites are ubiquitous in nature and can be costly to animal fitness, so hosts have evolved behavioural counter-strategies to mitigate infection risk. We investigated feeding-related infection-avoidance strategies in Japanese macaques via field-experimentation and observation. We first examined risk sensitivity during foraging tasks involving faecally contaminated or debris-covered food items, and then investigated individual tendencies to manipulate food items during natural foraging bouts. We concurrently monitored geohelminth infection in all subjects. We ran a principal component analysis on the observational/experimental data to generate a hygienic index across individuals and found that hygienic tendencies towards faeces avoidance and food manipulation correlated negatively with geohelminth infection. Females scored higher in hygienic tendencies than males, which might contribute to the common vertebrate pattern of male-biased infection. The behavioural tendencies observed may reflect a general form of hygiene, providing a mechanism of behavioural immunity against parasites with implications for the evolution and diversification of health maintenance strategies in humans.