Disease risk perception in animals and potential applications

This blog post is provided by Cécile Sarabian (cognitive ecologist and current Canon Foundation Research Fellow at Nagoya University, Japan; center), Andrew MacIntosh (behavioural ecologist and Associate Professor at Kyoto University, Japan; left) and Jorge Tobajas (conservation ecologist at the University of Cordoba, Spain; right) on behalf of all co-authors, and tells the #StoryBehindthePaper for the paper “Disgust in animals and the application of disease avoidance to wildlife management and conservation”, which was recently published in Journal of Animal Ecology. In their paper they review the implications and applications of disgust and disease risk avoidance in animals.

It’s the end of December, 2022. I (Cécile Sarabian) am on a packed train going to Edinburgh for the British Ecological Society Annual Meeting. I arrive from Hong Kong where masks are still mandatory, even outdoors, and where the government applies a ‘Zero Covid’ policy. In comparison, the UK is like a parallel world: no masks, no air circulation, but lots of coughing and not into elbows or hands, and loads of shoes on seats.

My perception of disease risk at that point was high. I was trying not to face these disgusting conspecifics, holding my breath behind my mask. This is the human world perceived by a scientist who has studied disgust and pathogen avoidance for a decade. But what about the animal world, where being picky with what or who can make you sick can be much more costly?

Do arboreal and relatively solitary Javan slow lorises avoid other’s droppings and sick conspecifics? (Photo credit: Marie Sigaud)

Animals have evolved various ways to handle disease risk, which can be packaged as the ‘ART’ of pathogen handling. And no, I’m not talking about painting or dancing to juggle between viruses, bacteria and parasitic worms. I’m talking about Avoidance, driven by one’s behavioural immunity, Resistance, one’s physiological immune response, and Tolerance, one’s resilience to pathogens – ART.

Depending on the species, the individual, the ecological context, and more, the investment in these responses may differ. Think of your neighbour’s dog sneaking into your yard to eat your dog’s droppings, or that school mate licking the edges of the playground’s sandbox. Well… maybe their physiological immune system could afford it?

Or maybe they were building a stronger one?

These are fascinating avenues to investigate, but we are not there yet. Among these strategies, avoidance is preventive and likely the most cost-effective. Though, it is not as well studied as the immunology or genetics of infection.

Olive baboon with genital lesions caused by the bacterium Treponema pallidum (Photo credit: Filipa M. D. Paciência)

Disgust is an emotion and a system that regulates avoidance to prevent pathogen infection and becoming sick. For a long time considered uniquely human, research over the past decade shows that the primers and outcomes of disgust are present in a much wider array of species. Social insects, rodents, birds, ungulates and primates are cast in starring roles in the behavioural immunity show. These roles include getting rid of the dead, dying and diseased in the colony; avoiding group mates that look a bit off or have lesions; or taking care of themselves by licking, preening, screening food and substrates.

In the wild, over 30 species were previously reported to exhibit disease avoidance strategies and the list keeps expanding. There are many others, though, for which the adaptive system of disgust and the disease avoidance responses have never been tested.

Adélie penguins are among the understudied species when it comes to pathogen avoidance. (Photo credit: Andrew J. J. MacIntosh)

Novel methods in ecology and related disciplines now allow more refined designs to test responses to disease risk in the wild and compare them with responses to other forms of risk such as predation and competition. Playing sounds when animals pass by is one way to test that. In a species management context, such as crop damage, the presentation of sounds of diseased conspecifics, predators or competitors coupled with camera traps (aka an ‘Automated Behavioral Response system’) can be a way to record and modulate space- and resource-use under different landscapes of risk.

Automated Behavioural Response system that could be used to display sounds of sickness. (Photo credit: Michael Clinchy)

Another way to measure the implications and applications of disgust combines 3D-printing and Conditioned Food Aversion (CFA). The former allows us to replicate biological contaminants, food and/or conspecifics to which other sensory cues can be added such as odours, textures or sounds that mimic disease risk. CFA uses the memory of taste. By adding an undetectable emetic substance to a food, targeted individuals associate that food, its features or cues nearby (e.g. odour) to the episode of sickness they have experienced and will later want to avoid.

This joint method is used for the conservation of endangered species by deterring predators from eating them, but could also apply to the management of invasive species and urban pests.  

3D replica of a critically endangered Mojave Desert tortoise (Techno-tortoiseTM) to lure predators (ravens and coyotes) and induce conditioned food aversion. Photo credit: Tim Shields/Hardshell Labs

What about our own disgust sensitivity and disease risk perception? Could it be used to protect the most vulnerable species?

Disgust has been used in public health largely to promote hand washing behaviour. Today, it could be used to encourage us to wear masks or keep an adequate distance away from those endangered species that we can hurt by being too close, for example by spreading infectious diseases to them. This is the case with mountain gorillas, which are visited by tens of thousands of tourists every year in their natural habitat. These apes are vulnerable to Covid-19 and other respiratory diseases that have previously decimated a good number of their population.

Tourists visiting mountain gorillas and taking pictures (Photo credit: Ryoma Otsuka)

By being reminded of the disease risks (online and onsite) via our very own adaptive system of disgust, and thereby avoiding proximity with such magnificent apes, or other species at risk, human emotion and behaviour can be leveraged as a tool to increase their survival.

Read the paper

Read the full paper here: Sarabian, C., Wilkinson, A., Sigaud, M., Kano, F., Tobajas, J., Darmaillacq, A.-S., Kalema-Zikusoka, G., Plotnik, J. M., & MacIntosh, A. J. J. (2023). Disgust in animals and the application of disease avoidance to wildlife management and conservation. Journal of Animal Ecology, 00, 1– 20. https://doi.org/10.1111/1365-2656.13903

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