Matter of taste

15 November 2013 by Malcolm Campbell, posted in Biology

Stercus accidit.” Said by many, attributed to David Hume (1711-1776)

There’s just no way around it, given the opportunity, our young dog will eat faeces.

The strange thing is that the young dog is not normally prone to engaging in unsavoury behaviours. Oh sure, he’ll roll on worms and worm casings, but that’s pretty well the extent of it. He’s picky about where he deposits his own excrement – there’s no defecating or urinating near his own backyard. In fact, if one was pressed to anthropomorphise, it would be easy to imagine him in a sharp, tailored suit, neatly pressed, over a pristine, crisp button-down shirt, while sporting well-polished shoes.

And yet, there’s this faeces-eating business.

The thing is, the young dog is picky about the faeces he eats. No indiscriminate poo diner is he. Most piles he encounters he is happy to let well enough alone – sniff them, urinate on them, and then move along. For those piles where he lingers, he can be warned off in most instances. But, every now and then, there is a pile that, by his reckoning, is delectable. With the gusto of a great wine taster, he takes a deep nose full of the aroma, and then ever so tenderly nibbles at it, before taking a good mouthful. Lest anyone think that this all occurs while under the calm and distant surveillance of a field biologist, rest assured that the faeces connoisseur partakes of his amuse bouche against a backdrop of frantic running, arm waving, and shouts of “Leave it! Leave it! Leave it!”

What drives a dog to this behaviour? What’s more, how can a being so acutely sensitive to odours consume something that, to us, so foul?

As it turns out, as mammals go, our young dog is not alone. In fact, he’s in very good company across the taxonomic class mammalia. From the small to the large, one can find plenty of examples of mammals that consume faeces.

Generally speaking, faeces consumption is referred to as coprophagy or coprophagia. The name originates from the Greek for faeces, copros, and eating, phagein.  Coprophagy may involve eating one’s own faeces or those of another individual, or even another species.

For some mammals, coprophagy is not a matter of choice. They are obliged to consume faeces. They are a special type of herbivore.

Herbivores have a particular challenge when it comes to their diet. The fibre-rich nature of the plants they eat makes it difficult to extract nutrients. The cells that make up plant matter are like little wooden boxes of nutrients – proteins and sugars encased within a box made of cellulose and other polymeric molecules. Getting the nutrients out of these boxes is not easy. They have to be physically disrupted, and then digested, to liberate their contents. Herbivores have evolved to do just that. Powerful chewing capability precedes novel fermentation mechanisms, which digest the fibre-rich mulch to extract its nutrients.

Herbivorous mammals have evolved two distinct types of fermentation mechanism to digest plant matter. The mechanisms are based on where the fermentation takes place. Some mammals are foregut fermentors. Many foregut fermentors are ruminants, like cattle, goats, sheep, camels, and some kangaroos and wallabies. With ruminants, plant matter is initially chewed then swallowed so that it takes up residency in the foregut, the rumen. Here, specialised microbes digest the plant matter, liberating nutrients. Periodically, the semi-digested plant matter, known as cud, is regurgitated, so that it can be further broken down by more chewing, followed by more digestion in the rumen.

Hindgut fermentation is the other major digestive mechanism used by mammalian herbivores. Hindgut fermentors operate in a very different manner from their distant ruminant relatives. As its name implies, in hindgut fermentation, chewed plant matter is swallowed, initially digested in the stomach and small intestine, but then most thoroughly digested in the hindgut. The fermentation chamber in this instance is a specialised region of the gastrointestinal tract located between the small and large intestine, called the caecum. In some mammals, like horses, elephants, and rhinos, the remainder of digestion occurs in an extensively elongated colon. In other mammals, after a prescribed period of time, the partially digested plant matter is immediately excreted, in what is known as caecotrophes. In order to recover the full nutritional value of the plant material, hindgut fermenters that make caecotrophes must immediately consume these faeces.

Caecotrophe consumption is a highly specialised form of coprophagy, known as caecotrophy. Caecotrophic mammals include rabbits, hares and pikas, as well as some rodents, like the capybara.

Coprophagy is exquisitely integrated into caecotrophy. The foregut of caecotrophic mammals is very ineffective – newly chewed food passes through with very little nutritional content removed. When it initially passes into the colon, the food is shunted back to the caecum by reverse peristalsis. In the caecum, the chewed, semi-digested plant matter is incubated with bacteria that are able to break down the plant matter. Some 4 to 8 hours later, the caecotophe will emerge, and is immediately eaten. On its passage through the upper gastrointestinal tract, nutrients are extracted from the caecotrophe. Notably, it is the bacteria derived from the fermentation in the caecum that actually make the proteins and sugars that are absorbed by the stomach and intestines.  Critically, these bacteria are a vital source of protein for animals that are consuming a high carbohydrate diet. In keeping with the importance of these bacteria, the intestinal tract is perfectly designed to support and augment the activity of these bacteria.

Caecotrophic mammals must eat at specific times of the day so that the timing of excretion of the caecotrophe occurs when it can be consumed – generally in the evening. In some ways, the consumption of caecotrophes is analogous to cattle chewing their cud – a means by which to best extract nutrients from their diet.

In caecotrophic mammals, coprophagy is obligatory. Evolution has crafted them into the ultimate faeces eaters. By human standards it may appear an unseemly way to get the best nutritional value from a meal, but it is a useful one. Obviously, dogs are not caecotrophic, but this doesn’t mean that there mightn’t still be a value to eating faeces.

For herbivores that aren’t caecotrophic, there is still a value to eating their own faeces. Young elephants are thought to eat the faeces of their mothers in order to obtain the gut microbes that will help them digest the tough plants they encounter as the herd wanders. In fact, coprophagy has been shown to be common amongst pachyderms, including extinct mammoths. In mammoths, coprophagy may have supplemented the diet in particularly lean times, including winter months, ensuring that the maximum amount of nutrients were extracted from scant food resources. What’s more, and intriguingly, coprophagy would have supplemented the mammoth (and other pachyderm) diet in other ways. The microbes that colonise faeces are able to produce vitamins, including K, B12 and B7 that are critical to good health.

The nutritional value of faeces is enough to encourage coprophagy across species. Amongst the most intriguing examples of this is the consumption of macaque monkey faeces by sika deer. In fact, sika deer are so intent on eating macaque faeces that they will waken the sleeping monkeys to eat their faeces, as they lay nesting on the ground. Consumption of macaque faeces is not uniform over the course of the year – the deer seem to prefer them in the summer months – potentially because of varying nutritional quality. It remains to be seen if the deer are dependent on the macaque faeces, but they have certainly developed a taste for them.

A taste for faeces is not something limited to species distantly related to our own. Other great apes, including gorillas, as well as our closest relatives, chimpanzees and bonobos, will engage in coprophagy. Such instances are not frequent in the wild, but they do occur. It is thought that great ape coprophagy may arise due to five factors. Four of these factors are nutrition based – faeces provide roughage; may include important nutrients; can supplement diet in lean times; or, may contain really valuable, but hard to digest foodstuffs, like seeds or nuts. The fifth factor is more specific to the nature of great apes, and other highly social, intelligent animals. Eating faeces can help alleviate boredom and stress – something to while away the hours of the day. Regardless of the motivator, being able to eat faeces has adaptive value for great apes. Unless there is a significant disadvantage in eating faeces, there is no reason for apes to lose this particular capability.

Which brings us back to the young dog. Why eat poo? Perhaps the question should be, why not? While his species has been on the road of domestication for tens of thousands of years, it is easy to imagine that being an opportunistic poo eater along the way would not be a bad trait to carry. Provided there is no selective disadvantage to being able to eat faeces, there would be no need to be as repulsed by them as we are. Indeed, there could be great advantage to being able to consume faeces in lean times. Today, given the diets that we feed modern dogs, it may be that some particularly savoury items make their way into faeces – at least as far as a dog is concerned. Beyond this, as an attention-getter, eating poo is a sure winner. It’s even been suggested that coprophagy might be a pleasurable, or at least stress-relieving, activity for dogs. For our young dog, given his choosiness, and his generally calm manner, faeces eating would appear to be just something that, for what ever reason, brings pleasure from time to time. It’s only his human companions that seem overly bothered by it.

In the end, the bigger question is really not “Why do dogs eat poo?”, but rather, “Why are we so repulsed by it?”. What happened in the trajectory of our species that we lost the capacity of so many of our mammalian relations to stomach that which we now find repulsive? What advantage was conferred by turning up our noses at our own faeces? Has faecal-borne disease been so rampant in our evolutionary history so as to drive this repulsion? What makes us, relative to our fellow mammals, so nauseated by our own excrement? We are so revolted by our own faeces that we hide them, flush them, bury them and base our profanity upon them. It’s intriguing, even if it’s crappy.

Images: All photographs by Malcolm M. Campbell.

References:

Boze, B. G. (2010). Correlates of coprophagy in the domestic dog (Canis familiaris) as assessed by owner reports. Journal of Applied Companion Animal Behaviour 4: 28-37

Krief, S., Jamart, A., & Hladik, C. M. (2004). On the possible adaptive value of coprophagy in free-ranging chimpanzees. Primates 45: 141-145

Herrera, E. A. (2013). Capybara digestive adaptations. In Capybara (pp. 97-106). Springer New York.

Naumova, E. I., Zharova, G. K., Kuznetsova, T. A., Chistova, T. Y., & Danilkin, A. A. (2013). Morphological provision for the specialization of hares to coprophagy: The architectonics of the mucous surface of the intestine. Biology Bulletin 40: 539-544

Nishikawa, M., & Mochida, K. (2010). Coprophagy-related interspecific nocturnal interactions between Japanese macaques (Macaca fuscata yakui) and sika deer (Cervus nippon yakushimae). Primates 51: 95-99

Sakamaki, T. (2010). Coprophagy in wild bonobos (Pan paniscus) at Wamba in the Democratic Republic of the Congo: a possibly adaptive strategy? Primates 51: 87-90

van Geel, B., Guthrie, R. D., Altmann, J. G., Broekens, P., Bull, I. D., Gill, F. L., ... & Gravendeel, B. (2011). Mycological evidence of coprophagy from the feces of an Alaskan Late Glacial mammoth. Quaternary Science Reviews 30: 2289-2303

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2 Responses to “Matter of taste”

  1. May Reply | Permalink

    Excellent commentary. A recent publication in the New England Journal of Medicine has shown that "The infusion of donor feces was significantly more effective for the treatment of recurrent C. difficile infection than the use of vancomycin." The treatment was so successful, the trial (Netherlands Trial Register number NTR1177) was stopped after an interim analysis and the therapy was offered to patients in the control groups off protocol.
    Nood e. et. al., Duodenal Infusion of Donor Feces for Recurrent Clostridium difficile. N Engl J Med. 368;5 January 2013

    • Malcolm Campbell Reply | Permalink

      Interesting point about faecal transplants, May! Perhaps there will be more reasons for us to embrace poo in the future!

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