Disease risk perception in animals and its applications

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Credit: Kyoto U/Jake Tobiyama
In our LAST paper, we provide an empirical framework for testing the adaptive function of disgust and associated disease avoidance behaviors in the wild, as well as their applications to wildlife management and conservation. ​​
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Overlooked species in risk perception research and how disease avoidance and disgust may be used in different contexts of conservation and wildlife management. Created with BioRender.
PDF: Sarabian, Wilkinson, Sigaud, Kano, Tobajas, Darmaillacq, Kalema-Zikusoka, Plotnik, MacIntosh (2023) Disgust in animals and the application of disease avoidance to wildlife management and conservation. Journal of Animal Ecology

Hygienic tendencies correlate with low geohelminth infection in macaques

Kojima, the birthplace of Japanese Primatology. Photo: センチョウ成田かな

​Feces avoidance experiment with Japanese macaques
Serori (adult female Japanese macaque from Koshima island) was presented to 3 substrate items, from left to right on the video: fresh macaque feces; piece of brown plastic notebook; and fake plastic feces. On each item was placed a grain of wheat. She already ate the wheat grain on the middle plastic substrate before this video started. The wheat remains on the fresh and plastic feces. Look at what she does... This experiment was part of my Master's study for which I tested whether food processing behaviours (such as rubbing, rolling, and washing) and feces avoidance could limit parasite infection in Japanese macaques, and therefore reflect some kind of hygienic tendencies.
Experimental setup on Kojima beach
Video: Philippe Ricordel
PDF: Sarabian & MacIntosh (2015) Hygienic tendencies correlate with low geohelminth infection in free-ranging macaques. Biology Letters

Avoidance of contaminants through different sensory cues in chimpanzees​ 

​Vision-mediated avoidance of feces in chimpanzees
Vaillant (adult male chimpanzee from the CIRMF in Gabon) was presented here with two items: a brown feces replica on the right and a dark foam control on the left. On top of both items was placed a piece of banana and Vaillant was given the choice to feed on each of them. Look at the video to see what and how he does... This experiment is part of a study on the multimodal recognition and avoidance of biological contaminants in chimpanzees.

​Touch-mediated avoidance of biological contaminants
This adult female chimpanzee attempts to reach food inside an opaque box. Here, the food reward (piece of banana) lies on a dough substrate. After touching the substrate, she refused to feed. Slimy, moist and warm substrates in nature are usually richer in biological contaminants compared to hard and dry substances. This experiment replicates a study conducted in humans on tactile cues to detect pathogen presence.
PDF: Sarabian, Ngoubangoye, MacIntosh (2017) Avoidance of biological contaminants through sight, smell and touch in chimpanzees. Royal Society Open Science

Feeding decisions under contamination risk in bonobos


​Degree of contamination sensitivity in bonobos
​Mabali (adult male bonobo from Lola ya Bonobo Sanctuary in DRCongo) was presented with a "chain of contagion": five successive banana slices leading to a contaminant (a fresh bonobo feces), and the "cherry on the cake": an additional slice of banana on top of the feces. Mabali picked up and ate the slice of banana in position 4 first, followed by slices 6, 3 and 5, and then left the experimental area with slices 1 and 2, in contact with and adjacent to feces, left uneaten.
PDF: Sarabian, Belais, MacIntosh (2018) Feeding decisions under contamination risk in bonobos. Philosophical Transactions of the Royal Society B

Avoidance of contaminated food correlates with low protozoan infection

In this study, we used bonobos’ responses to food contaminated with soil and/or feces in behavioral experiments, and compared the results with an estimate of protozoan infection across individuals. Bonobos who did not feed on contaminated slices of banana had less Balantioides coli cysts in their feces compared to those who did. B. coli is a potentially pathogenic protozoan transmitted through the ingestion of microparticles of feces (aka the ‘fecal-oral route’). The experiment which best highlighted the association between avoidance responses and parasitism was replicating the ‘chain of contagion’ mentioned above. This is likely due to the gradient of avoidance that could expressed in return of this gradient of contamination. The behavioral immunity observed may be a consequence of infection – one of the direct effects of parasites. But parasites can also have ‘indirect effects’ such as modulating feeding decisions or reducing social interactions. Further studies should investigate how such indirect effects may interact with physiological immunity and what can attenuate these effects (e.g. a favorite food item in a foraging context, or kinship in a social context).
PDF: Sarabian, Belais, MacIntosh (2021) Avoidance of contaminated food correlates with low protozoan infection in bonobos. Frontiers in Ecology and Evolution

Evolution of pathogen and parasite avoidance behaviors

In June 2017, I co-organized a Royal Society meeting with Dr. Rachel McMullan (The Open University) entitled "Evolution of pathogen and parasite avoidance behaviors" gathering over 20 experts working on avoidance behaviors in worms, ants, flies, mice, birds, kangaroos, lobsters, dogs, primates including humans and beyond - which also led to the co-edition of a special issue (with the same title) in Phil. Trans. R. Soc. B in 2018.  
PDF: Sarabian, Curtis, McMullan (2018) Evolution of pathogen and parasite avoidance behaviours. Philosophical Transactions of the Royal Society B

​Feces avoidance is not 'specific' to nematode infection risk in mandrills

Photo: Benoît Quintard/Mandrillus Project. The Mandrillus Project studies the socioecology of wild mandrills in the Lékédi Park, in Southern Gabon.
At the CIRMF in Gabon, Dr. Clémence Poirotte and I conducted experiments to test whether mandrills would be able to detect and avoid nematode infection risk in a feeding context. These nematodes are not readily infectious after defecation. They need time to mature in feces before reaching the infective larval stage and emigrating out of the feces to the surrounding environment. As such, we presented 3 leaves on the ground: covered with a mix of feces from parasitized individuals (nematode+); mix of feces from dewormed individuals (nematode-); and control (no feces). We then placed two pieces of bananas on each leaf - one on the side and one in the center. We presented these three leaves at the day of defecation (D0), 7 days later (where for the nematode+ leaf, part of the non-infectious nematode eggs already transformed into infective larvae), and ~2 weeks later (where for nematode+ leaf, all nematode eggs transformed into infective larvae). 
We found that mandrills exhibit feces avoidance in a feeding context, with females being more picky than males. However, they avoided similarly feces of parasitized and dewormed individuals, and the presence of infectious nematode larvae did not influence the level of avoidance. Feces may harbor a wide range of parasites, such as bacteria, viruses and protozoans, that can be infectious right after defecation. As such, nonspecific fecal avoidance during foraging may be a more effective strategy to limit infection with all kinds of pathogens.   
PDF: Poirotte*, Sarabian*, Ngoubangoye, MacIntosh**, Charpentier** (2019) Faecal avoidance differs between the sexes but not with nematode infection risk in mandrills. Animal Behaviour

Different strategies in feces avoidance between primate species

In a series of experiments with mandrills and long-tailed macaques at the CIRMF in Gabon, ​we showed that the sight and smell of a parasite-rich substrate – feces – in a foraging context elicit different responses in both species. While mandrills ate less food associated with such sensory cues, macaques did not vary their consumption, but manipulated the food beforehand. For both species, their favorite food was used - banana for mandrills and peanuts for long-tailed macaques. These results are partially consistent with the predictions of the parasite avoidance theory of disgust, although potential exposure to feces did not preclude feeding entirely. 
PDF: Sarabian, Ngoubangoye, MacIntosh (2020) Divergent strategies in faeces avoidance between two cercopithecoid primates. Royal Society Open Science