In the dirt: do primates yuck?

POST BY: Cécile Sarabian

Imagine living in an environment where pathogens and infectious diseases are everywhere. No hand sanitizer, no water purification tablets, no insect repellent, and potentially lots of infected mates. This is the scenario that most wild, social animals – including primates – have to cope with. Therefore, it is imperative for these species’ survival to develop behavioural strategies to reduce infection-risk.

Pic 2
Provisioning at Koshima beach, which gets easily covered by feces

Across the animal kingdom, we can find many examples of behaviours referring to the concept of ‘hygiene’ in humans: ants use specific chambers of their nests to dispose their waste and prevent parasitic fungi infection [1], horses prefer to feed on short grass and far away from feces to avoid parasites [2], boars wash dirty food before feeding [3], and birds even use cigarette butts into their nests to repel ectoparasites [4]! While other hygienic strategies have been described in primates [5], few studies directly investigated how primates deal with potentially contaminated food. Yet, one of the most common pathways to infection is the faecal-oral route, in which pathogens from one host’s feces pass to another host by ingestion of fecal particles. As such, food-related behaviours are intimately linked to infection and infection avoidance.

Pic 1
Gastro-intestinal nematodes first mature in feces before reaching the infectious larval stage; they can then spread to a new host through oral ingestion.

On a small island in Southern Japan called Kojima (which literally means ‘happy island’), Japanese macaques use a set of behaviours to process their food before feeding. “Rub, roll, wash” could be the rule for numerous food items. As you may know, Kojima macaques had their heyday in the 1950s for washing sweet potatoes in seawater before eating them. At the time, scientists were more interested in studying how the behaviour spreads among the group than its actual function [6]. Sixty years later, we revisited this behavior to test its hygienic function [7]. We distributed both sandy and clean pieces of sweet potatoes to the monkeys and recorded the frequency and the diversity of food handling behaviours used in both conditions.

Pic 3
From left to right: acorn rubbing, puffer fish squeezing and puffer fish washing

In another experiment, we aligned a fake plastic poop, a fresh feces, and a piece of brownish plastic. On top of the 3 items, we either placed a grain of wheat (first condition) or half a peanut (second condition) – see the image below! Wheat is provisioned 2-3 times a week on the island, whereas peanuts are more like a Christmas gift – a special treat! We also recorded the frequency of rubbing behaviours during acorn foraging in Koshima forest. In parallel of those 3 experiments, we monitored the infection rates of the target individuals and found that dirty-food “processors” – those that manipulated their food before eating it- and poop-wheat avoiders had fewer parasites than less meticulous individuals. Females were more hygienic than males and interestingly, feces avoidance seemed to be more visually mediated than olfactory mediated as wheat was always eaten on the piece of brownish plastic but avoided on the plastic poop [7].

Pic 4
Spot the fake macaque feces…

This negative correlation between hygienic tendencies and parasite infection brought me many more questions: can this relation be observed in other species of primates? Which contaminants do primates preferentially avoid? Which senses do they use? Does the adaptive system of disgust apply to non-human primates? These are the kind of questions I aim to answer in the next two years. In the middle of my PhD, I’m now investigating this behaviour-health relation in Gabon and Democratic Republic of the Congo through experimental work with chimpanzees, mandrills, bonobos, and macaques… and it’s quite fun!

 

Cecile Sarabian is a Ph.D. candidate in primatology at Kyoto University. 

 

References:

  1. Bot, A.N.M., Currie, C.R., Hart, A.G., Boomsma, J.J. 2001: Waste management in leaf-cutting ants. Ethology, Ecology and Evolution. 13: 225-237.
  2. Fleurance, G., Duncan, P., Fritz, H., Cabaret, J., Cortet, J., Gordon, I.J. 2007: Selection of feeding sites by horses at pasture: testing the anti-parasite theory. Applied Animal Behaviour Science. 108: 288-301.
  3. Sommer, V., Lowe, A., Dietrich, T. 2015: Not eating like a pig: European wild boar wash their food. Animal Cognition. : 1-5.
  4. Suarez-Rodriguez, M., Lopez-Rull, I., Macias Garcia, C. 2012: Incorporation of cigarette butts into nests reduces nest ectoparasites load in urban birds: new ingredients for an old recipe? 9: 20120931.
  5. Nunn, C.L., Altizer, S. 2006: Infectious diseases
in primates. Oxford, UK: Oxford University Press.
  6. Kawai, M. 1965: Newly-acquired pre-cultural behavior of the natural troop of Japanese monkeys on Koshima islet. Primates. 6: 1-30.
  7. Sarabian, C., MacIntosh A.J.J. 2015: Hygienic tendencies correlate with low geohelminth infection in free-ranging macaques. Biology Letters. 11: 20150757.

 

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