CHAPTER 4

Turds of Endearment:

what excrement
means to animals

Single-celled organisms depend for their lives on the membranes that surround them, and on the ability to draw in nourishment and to push out waste; ecosystems depend on co-evolved, geographically local rule-sets that characterize excrement and death and recycling. Animals are the most obvious, visible link that ties us all together.

Feces can be grossly classified by shape, color, texture, smell, and location in the environment, and each characteristic tells us something different about the life of the animal and its ecological roles. These attributes might be thought of as defining the public style of excrement — its presentation to the world, if you will — as differentiated from its substance. This is how we first notice excrement. We could also add taste, which is something some have explored as children, but there are not many people who would share such information publicly, so great is the wincing and tut-tutting in the audience when human feces–eating is described. For now, it is enough to say, it happens.

The nutrient content, scent, and structure of feces have co-evolved to serve multiple roles within species and link a variety of plant and animal species into coherent ecosystems. Examining feces, by whatever method, can tell us a great deal.

Scent is a very important characteristic of feces, and not just because it annoys humans. In omnivores and herbivores, including people, the odors of feces can be attributed to bacterial action on undigested food and to the release of sulfur-containing molecules such as skatole, indole, mercaptans, and hydrogen sulfide. Many of the functions of dung within and between animal species — as differentiated from its ecological functions — have to do with the characteristic scents produced by the different chemical composition of foods eaten, how they are processed in the gut, and how they are expelled from the body. At least one Swedish researcher has argued that human excrement has much less scent if it is not mixed with urine, which provides nitrogen that results in some of the foul-smelling products.

Sharks can apparently smell human feces in the water from a mile away, depending on currents and the size of the deposit, but the scent of excrement is used by many mammals to better effect than attracting sharks. Carnivores, for instance, will sometimes eat herbivore scat to mask their own scent for hunting. Some pet dogs have retained this habit from the wild, and one can spend money to “cure” a dog of this behavior, although I would rather have a dog that eats feces than one that bites people. It may be that eating feces adds nutrients to the diet, or enables dogs to maintain a healthy bacterial flora through re-inoculation, or maybe it is just an evolutionary oddity, like singing in the bath to scare away predators (works for me).

Although many a veterinarian might think that the anal glands of dogs were created to get infected, impacted, and squeezed by the nimble fingers of well-trained professionals who had to go to school for many years to learn how to do this, those glands serve other purposes as well. In carnivores (except hyenas), anal gland secretions, which adhere to the feces during defecation, have characteristic and complex odors that communicate such vital information as species, territory, sex, reproductive state, and geographic movements. This information is useful not only for other carnivores but for prey, to detect when a predator is near. Quite sensibly, cattle, sheep, and monkeys stay away from the smell of panther feces.

People generally do not use scent to track animals, but scent is still important in molding our reactions to it. Apart from the different scents given off by cattle, pig, and dog dung, certain diseases result in peculiar scents, because of the kinds of fermentation, carbohydrate or protein breakdown, or chemical production by particular microbes. One of my veterinary colleagues claims she can differentiate a coccidial from a parvoviral infection in dogs by smell, even from a distance. One wonders if feral dogs might use such scents to avoid diseased animals; doing so would certainly confer some evolutionary advantage — but perhaps the gain is outweighed by the strong selection pressures exerted by fast-moving road vehicles.

There is no doubt that the excretions of animals have always posed something of a challenge for some of the individuals and species who deposit them, and much of this has to do with scent. It is not always advantageous, for instance, to have your perfume announce your presence to other animals. This is particularly true for prey animals, where betrayal of one’s presence has been dealt with by a variety of strategies such as coprophagy, burial, or putting the dung in places some distance from where they live. While the stories of birds carrying fecal sacs to drop into streams or sloths burying feces may be more common, some butterfly larvae have evolved more spectacular behaviors to lead predators astray, such as ballistic fecal ejection, sometimes called frass-shooting.

Brazilian skipper caterpillars, about 1.5 inches long, can shoot their feces six feet away, but most ballistic frass-shooters are satisfied with a 20– to 40–body-length fling — albeit at 1.5 meters per second. (I wonder, if at some future “Green” Olympic Games, humans might attempt to better those records.) In a variation of this, colonies of giant honeybees (Apis dorsata) — up to 40,000 bees at a time — have been known to fly en masse and drop about 20% of their body weight in yellow shit. During the Vietnam War, some military commentators, not knowing about the bees, wondered if this was some sort of biological warfare. Perhaps it was, but the war was being waged by another species, no doubt furious at human destruction of their habitat.

Not all animals have developed such dramatic tactics. Many, like humans, simply create a space away from where the food and babies are. This serves both to redirect the predators and to announce one’s presence to friendly animals (perhaps of the same species). Pigs, for instance, do not naturally, as some have suggested, roll in their own poop. They have areas in the pens where they defecate, well away (if possible) from where the food is. They have this in common with llamas, who defecate in well-defined areas (a meter or two across); the impalas of Selous Park in Tanzania, who have their dung middens; giant South American otters, who trample a large communal toilet area along the riverbank to define territory; badgers; and African mole rats, who will sometimes set aside special dung-tunnels.

Two-toed sloths create dung middens to indicate mating sites not just for themselves, but for the moths that live in their coats. Genets are solitary, long-tailed, mongoose-like animals that create treetop or rock-top communal latrines. These serve as a kind of Facebook, allowing strangers passing through to sniff out potential mates or rivals. Bushbuck use defecation sites for inter-sexual communication. The females put out the signals and the males monitor the females for receptivity. One could speculate whether dung middens played any similar roles in human evolution, indicating places where other humans might be found for breeding purposes. Although “meet me tonight at the dung midden” seems to me to be a pick-up line with little chance of success, I confess that, in my mate-seeking days, I never actually tried it, so I have what is called an absence of evidence rather than evidence of absence. I would be interested to know if anyone has used it successfully.

The scents emanating from animal excrement are important, as well, for biologists who wish to study animal behavior and ecology. Examining the scats of animals (a so-called fecal-centric approach to studying wildlife ecology and conservation) is often as informative as, and more ethically defensible than, other more invasive methods of gathering information about the eating habits of wildlife, such as radio-collaring.

Finding those scats, however, is a big challenge, especially in wilderness landscapes. One tactic is to use dogs, who are great sniffers. They have already been used to detect drugs and other contraband at airports, and to track down crooks and hostages. Why not train them to find wild animal scats? In fact, this has been done. Karen DeMatteo, a biologist at the University of Missouri, has trained a Chesapeake Bay Retriever named Train to detect scats of several South American wild animals. By studying the distribution of the hundreds of scats detected by Train, DeMatteo has been able to describe the habitat preferences of pumas, jaguars, spotted cats, and bush dogs. Another dog — a Labrador cross named Tucker which had failed as both a house pet and a police dog — was hired by the Center for Conservation Biology at the University of Washington. He is afraid of water but loves the scent of whale poop so much he will jump into the ocean after it, which is very helpful for those who wish to track whales.

A mixture of information from scat-sniffing dogs and the latest technologies for genetic analysis and DNA characterization can provide a wealth of data on where animals travel in the wild and what they eat. This is important evidence for determining the extent and types of habitats that need to be protected in order to prevent species extinctions and for understanding the relationships among multiple species on a landscape.

Once the scats are found, we can — like my guides in Selous — use the shape, color, size, and content of scats to identify which animals are around and what they have been eating. For instance, the bear scats I find on the Bruce Trail, along the Niagara Escarpment north of where I live, are usually thick logs chock-a-block with berry seeds. On the west coast of Canada, one might see fish bones mixed in with berry seeds in bear scat.

The characteristics of human excrement have been used to determine what people eat, and the health consequences of that diet, particularly in parts of the world where outdoor defecation is still common. Based on comparative studies between countries in Africa and Western industrialized nations, Denis Burkitt and his colleagues suggested that a fiber-rich diet helps prevent a variety of diseases and complaints in people including hiatus hernia, diabetes mellitus, coronary artery disease, colonic diverticulosis, colorectal cancer, appendicitis, varicose veins, and hemorrhoids. Burkitt also became famous for his numerous slides of human feces taken on his early morning walks in the bush in Africa. This, my wife should note, is a step beyond the pictures of animal shit that I have sometimes pursued on our holidays. He was apparently quoted as saying that the health of a country’s people could be determined by the size of their stools — more fiber in the diet resulting in larger stools — and whether they (the feces, not the people) floated or sank. From these observations, North American baby boomers (myself among them, I confess) made a great obsessive leap of dietary faith and began a long romance with oat bran, wheat bran, and granola.

The land use and excrement consequences of this baby-boomer shift in diet have never been adequately explored. We are producing more excrement. But is it better excrement? Are the foods that end up in this excrement better for the soils? These questions are of far greater importance for the planet than whether or not we suffer from irregularity.

Burkitt’s observations on fiber and health were almost single-handedly responsible for the huge demand in North America for high-fiber foods and diets. He made no reference to bear populations, however. Whatever the seeds in the scat say about the health of the bears, they do tell us that these animals are important in the ecology of the plants in the region, carrying seeds to new places, along with the remains of fish, which contain some excellent fertilizer to get the plants off to a healthy start. Take away the bears, and what happens to the berries? What happens to the riparian zones along streams frequented by bears?

While bears are key species in the ecological systems they call home, other animals have played a central role in the development of human cultures. Herbivores are capable of digesting the cellulose of plants and converting it into milk, blood, meat, and other materials, which can then be digested by people. It is perhaps no accident, then, that the woman on the airplane asked about sheep, cattle, and horses. All three, it turns out, are well adapted for life on semi-arid grasslands and a nomadic life, which represent the origins of modern human societies.

Sheep, like all their even-toed hoofed relations (even-toed ungulates, also called artodactyls) except for cattle and buffaloes, drop small piles of cylindrical or rounded pellets usually pointed at one end and concave at the other.

Cattle, buffalo, and bison leave behind flattened feces that accumulate in circular piles, which we used to call pies or pats. These are sufficiently well defined that they attract flying insects, which lay eggs, which turn into larvae, and in so doing turn shit into edible protein for birds. They also attract dung beetles, which can turn the dung into another generation of dung beetles.

Horse droppings, which look similar to those of warthogs — a random piece of information to share with your seat-mate in the airplane — are said to be kidney shaped, but to me they look like dark rye buns. I am not alone in this perception, as at least one enterprising company has developed what they call “bun bags” to catch horse manure before it hits the road. Someone must have once imagined that horse turds look like apples; hence the term “road apples,” although that American slang term was apparently first applied to traveling actors.

Why do these differences in shape and appearance exist?

Cattle and sheep are both ruminants, and both are grazers; that is, they eat mostly grass, rather than shrubbery or tree leaves.¹ The rumen part of their multiple-stomach system is like a great big fermenting and digesting barrel whose functions I described earlier; you can hear the rumbling and gurgling sounds (called “borborygmus”) if you place your ear against the warm fuzzy upper left flank of a cow, just ahead of where the hip bone sticks out. This rumen soup has, to some of us, a rich and sweetly sour scent. Digestion is helped further when the ruminant belches up some of the food, re-chews it, and then re-swallows, which is called rumination (and is only vaguely related to what your parents did when you first asked them about sex).

There is nothing more wonderful and peaceful than sitting on a straw bale in a barn with a herd of ruminating cows. I hope I can die in those surroundings, or am at least reincarnated there, which is a more likely possibility.

Even though sheep and cows both graze, sheep get much of their water needs from the grass itself, and so drink a lot less water than cattle; their feces are drier and more discrete. Sheep are thus more efficient in water use, which is why you see them in desert environments more often than cows. They also eat closer to the ground, which is why they have been used to try to decontaminate radioactive pastures (by eating and removing the radioactive plants). This feeding behavior also has larger ecological implications. Australia ships about 25,000 tons of sheep meat and more than a million live sheep to Saudi Arabia every year: what, one might ask, are the implications of this for the movement of nutrients out of Australian soils and into the Arabian peninsula? Of course, sheep do sometimes graze on wet, verdant pastures, and there produce what biologist Ralph Lewin calls morular “shitlets,” a term which I find endearing and shall have to find greater opportunity to use.

Giraffes, like goats, are primarily browsers, which has nothing to do with their use of the internet; they prefer foliage from trees and shrubs, rather than low-growing grasses. They are also ruminants and are nature’s way of transferring nutrients from high up in the trees to the bacteria, protozoa, and dung beetles on the ground. They are very efficient in water use, and can go longer than a camel without drinking. Hence their feces tend to be similar to, but larger than, sheep pellets, like chocolate-colored baseballs.

Horses don’t have the complex stomachs of ruminants. They do, however, have a big cecum, a large sac where the small intestine joins the large intestine, like an enlarged appendix. Because of this cecum, they are sometimes called “hindgut fermenters.” The cecum is full of billions of bacteria and protozoa that help break down and ferment plant fiber. The horse gets some benefit from this as fluids and some nutrients can be absorbed in the large intestine. However, since most of the nutrients are absorbed into the body from the small intestine, much of the work of these microbes in the cecum is for the benefit of the ecosystem at large rather than for the individual horse. The horse has to compensate for this relative loss by eating a greater volume of hay or grass, or wait for indulgent owners to feed them oats, which are more nutrient-dense than hay or grass. One might wonder if this process led to fertilization of grassland where horses (and the cows and sheep and their owners) lived, enhancing the growth of the grasses, and hence helped the population sustain itself, even if it was of no great benefit to the individual horse. Some evolutionary biologists would consider this heresy, whatever the evidence, but I tend to prefer to refer back to evidence, rather than ideology, in trying to understand the world.

In any case, turds of horses are firmer than those of cattle because they contain a lot of undigested straw and chaff, and they aren’t slurried up in rumen juice.

For those of you readers who wish only to impress your neighbor in the airplane, you may stop reading here, and respond to her. For the others, who are, I hope, most readers, and who are unexpectedly interested in the subject of excrement and its importance for ecological sustainability, please read on. Maybe on the next plane ride, you can be the one to ask the difficult question to put off an annoying seat-mate, or engage someone with the same warped turn of mind as you (and me).

Rabbits, hares, and pikas are also hindgut fermenters, but they get around the nutrient loss problem by eating some of their own feces. Like horses, they drop hard, fibrous shitlets, but unlike horses, they also squeeze out clusters of soft, dark, sticky currant-like pellets (cecotrophs). These delicacies are formed in the cecum, which in the rabbit is ten times larger than the stomach. Made up of fermented food and bacteria, and coated with mucous, cecotrophs are passed at night in domestic rabbits (which eat and pass normal stools during the day) and during the day in wild rabbits (which are nocturnal). They are usually eaten directly from the anus, so that they do not dry out or lose their nutritional value.

Watching a rabbit carefully nip cecotrophs from his anus must be an educational experience, surely, for pet rabbit–owning parents and children alike. “Daddy, what is Bunnykins doing?” asks the child, trying to figure out if he could manage the same dexterous act, the anxious parents fearing that, limber little kid that he is, he just might be able to. Perhaps this will lead to a career in yoga instruction, the parents never once suspecting the origins of such a choice in a family that only ever played hockey.

For non-humans, coprophagy — the deliberate eating of shit — is a behavior that has evolved in situations where survival trumps moral pretention. While most people know about rabbits, dedicated scientists (or sometimes just people with time on their hands and no access to television) have observed various excrement-eating behaviors in horses, rabbits, capybaras, ringtail possums, guinea pigs, mountain beavers, lemmings, chinchillas, nutrias (coypus), rats, mice, gerbils, degus (bush-tailed rats), and other rodents, dogs, cats, and shrews.

Eating shit has evolved among non-humans to fulfill both nutritional and protective roles. Parents want to prevent predators from detecting the scent, particularly of newborn animals. A deer doe, for instance, will eat her fawn’s feces for the first month of its life in order to avoid attracting predators. Funny, I don’t remember that from Bambi. Some songbirds also eat the feces of their young (also don’t remember that from Disney), especially when the nestlings are very young, a practice that some behavioral ecologists have attributed to good bird economics: the parents are avoiding the transportation costs of fecal sac disposal. Still, many species of birds do pick up the mucous-coated packages of baby poop and drop them into streams or ponds nearby, especially as nestlings get older. Which means that if the birds disappear (for instance, through deforestation or predation from the roaming of gangs of unemployed feral cats), the richness of life in the waterways is also diminished.

In several species coprophagy is about fostering health and protecting against disease. Rabbits are gaining proteins and water-soluble vitamins. Mice are said to gain vitamin B12 and folic acid from eating feces, and if you prevent lab rats from eating their own feces, they don’t grow well and can develop vitamin B12 and vitamin K deficiencies.

If a cow is sick and not eating for a long time, the micro-organisms in her rumen will start to die off; one way to get her eating again is to siphon the rumen contents from a healthy cow (just like siphoning gas from a car!) and infuse them into a sick cow. Like community motivators and facilitators, the incoming bacteria will kick-start the moribund population of bacteria and protozoans and get them living and working (and having fun?) again.

Termites, too, consume their own excrement and undigested debris (frass), in order to acquire necessary gut flora, including protozoa, to aid in digestion.

A variation of this idea, called competitive exclusion, involves getting beneficial bacteria into the gut to keep out bacteria one doesn’t wish to have there. The basic idea is simple: if there are beneficial bacterial already occupying a certain ecological niche, then the pathogenic bacteria cannot get a foothold. In Finland, where competitive exclusion was first developed as a poultry disease management technique, newborn poults (baby turkeys) were fed cocktails of mature turkey feces in order to prevent Salmonella infection.

People, apart from children and those with disordered mental states or abnormal appetites (a state called “pica”), do not normally eat feces, although there may be some titillation associated with eating something that has been associated with, or derived from, shit. In 2011 Mitsuyuki Ikeda, a Japanese researcher at the Environmental Assessment Center in Okayama, reported that he had fabricated artificial meat from sewage containing excrement. The “meat,” which is said to taste like beef, is 63% proteins, 25% carbohydrates, and 3% fats. Apparently much of the food value comes from the bacteria in the feces.

This risqué skirting of the impolite may explain at least part of the fascination with “Kopi Luwak,” the name given to coffee made from beans that have passed through the bowels of Asian palm civets. The civets eat coffee berries, the coverings are digested, and the seeds are pooped out. It has become famous, or infamous, especially as a result of Jack Nicholson’s love for it in the movie The Bucket List.

The coffee’s infamy comes from its expense, from the ambiguities about its quality, from its association with feces, and from periodic rumors that it may be a hoax played by marketing-savvy Indonesians and Vietnamese coffee sellers on wealthy Westerners. Others may drink it to honor the peasant workers who discovered it: because the Dutch colonialists prohibited their Indonesian workers from picking coffee beans for their own use, the workers scavenged, cleaned, and roasted seeds from Asian palm civets’ droppings. Because the taste of any Kopi Luwak depends on the coffee beans that were eaten by the civets, the flavors vary widely. The Balinese variety I am drinking as I write this, a gift from an Indonesian colleague, has none of the sharp, rich scents and pleasantly bitter aftertaste that I usually associate with coffee. The chocolate-colored powder has a faint, musty, earthy scent, as does the smooth drink prepared from it. Massimo Marcone, a food scientist at the University of Guelph, has studied the properties of the beans, and found them to be lower in protein (apparently a source of bitterness in coffee beans) and to have different volatile compounds, than standard Colombian coffee beans. These differences from “ordinary” beans are the result of enzymatic action in the civet’s stomach.²

Despite the cringing responses of most people to the very idea of coprophagy, the principle of competitive exclusion used to such good effect in turkeys provides the basis for an effective therapy for a deadly hospital-acquired infection by Clostridium difficile. These organisms, part of a group of anaerobic organisms that are widespread in nature, occur at low levels in many animal intestines, including those of people. In many North American hospitals, C. difficile has been transformed into a killer bug as the result of intensive antibiotic treatment, which has killed off competing, non-killer bacteria. An important part of the treatment involves taking bacterial flora from the intestines (that is, the shit) of healthy donors, which are then infused through enemas or nasogastric tubes into the patient. This replenishes their healthy gut flora, which then out-compete the disease-causing Clostridia.

Competitive exclusion may also explain the fact that, in some studies, dogs that eat excrement are less likely to be found infected with certain bacterial pathogens such as Clostridium difficile. Having said this, I should point out that poop-eating dogs are more likely to shed some other dangerous bacteria such as Salmonella. The fact is that bacterial ecology in shit is not something we understand very well, and we should manipulate it with care.

Hyraxes are cute rabbit-like animals that live in trees and rocks in eastern and southern Africa; the rock hyraxes peer at you as you walk through their land, like creatures from a Star Wars movie. The tree hyraxes make a sound in the night like a creaking door, followed by a blood-curdling scream, which is quite unnerving if one is sleeping in a tent in what one thought was the middle of nowhere. Hyraxes create dung middens, and urinate on them to increase the scent, as territorial markers. These animals are related to Sirenians (dugongs and manatees), elephants, and aardvarks, and have multi-chambered stomachs in which bacteria break down plant fibers, their abilities in this regard being similar to ungulates. The Sirenians poop in water, which means that most of us are rarely afforded the opportunity to see the shit’s shape.

Elephants are, of course, considerably larger than hyraxes, which explains why their daily output of big coarse cylinders can in no way be referred to as shitlets. Elephants can both browse on shrubs and woody plants and graze on grasses. When they browse, they can bring down whole trees; if populations are crowded together, this can be very destructive. However, elephants only digest about 40% of what they consume. Thus they are bringing down nutrients from high places and making them available for animals that are more constrained in their reaching ability, but less finicky in their eating habits, and are willing to nose around in elephant shit.

The 35-million-year-old aardvarks suck and lick and dig termites out of the ground, a diet which they supplement with a kind of underground tuber (Cucumis humifructus) whose seeds they disperse when they bury their feces; this burying is good for the ecosystem, but not so good for those who keep a journal of fecal sightings.

Medieval English hunters referred to the feces of hunted animals as “fewmets,” a term derived from Old English feawa, meaning “scant” or “few,” and “encounter” (metan), which suggests that wildlife turds are difficult to find. The turds of aardvarks seem to be fewmets indeed. Some use the term “fumets” to refer to deer droppings. The difficulty in finding feces from many wild species (and hence the need for zoologists to train sniffer dogs) reflects the conflicting implications of announcing one’s presence in the woods, and the various behaviors that have evolved to deal with that conflict. It also reflects the fact that any organic material is, given the right temperature and moisture, quickly used as food by bacteria and fungi, broken down into materials that are usable by other animals and plants. Usually, if you find a pile of excrement (or a dead bird) it is either very fresh or there is a lot of excrement (or a lot of dead birds) around.

What emerges from these observations of animal shitting behavior is that a variety of species has survived because the types of food they can process, the types of feces they produce, and the behaviors that evolved to dispose of those feces are not only of benefit to themselves, but to the sustainability of the ecosystems within which they live.

Animals do not plan to enrich the ecosystems in which they live. Nevertheless, the co-evolutionary, complex webs of eating, defecation, and renewal across species have provided habitats that enable those animals to thrive. Feces, which are food for bacteria, fungi, plants, and micro-fauna, are “reborn” in the form of new food and shelter for the descendants of the original animals.

Ecologically, defecation behaviors of all species are a kind of gift giving that binds us together in a beautiful community of life, birth, eating, shitting, death, and rebirth. When we eat, we are taking a gift from the biosphere. When we shit, we are giving back. Our eating and defecating behavior says far more than any voting behavior about what kinds of citizens we are on this planet. This is why, fundamentally, shit matters.

1 In aquatic systems, grazers are animals such as snails and beetles that eat algae.

2 What is often missed in the cute culinary story of Kopi Luwak is the importance of the civet behavior in natural systems. In a natural system, the poop helps the wild civet to mark territory; the ecological effects of this would serve to disperse the coffee plants to new locales. What people view as a culinary curiosity was thus, evolutionarily, important for the survival of the civets and coffee plant populations in the wild. Today, most Kopi Luwak is produced by farmed civets.