Don't Look, Don't Touch, Don't Eat: The Science Behind Revulsion

by Valerie Curtis

  Over 250 species of bird are known to “ant,” rubbing crushed insects over their plumage. This distributes compounds that protect them from bacteria, fungi, and arthropods.21 Gray squirrels and colobus, owl, and capuchin monkeys also rub their fur with leaves and fruit juices, probably for similar reasons.22

  The effects of ectoparasite infestation can be serious: a cow calf (Bos primigenius) with a moderate tick load, for example, gains 10–44 kg less per year than a tick-free calf.23 Bloodsucking mites reduce the body mass of house sparrow (Passer domesticus) chicks.24 Apart from absorbing nutrients directly, biting insects serve as disease vectors; they introduce other, smaller, epiparasites such as the mosquito-borne plasmodium that causes malaria in perching birds and the tick-borne flavivirus that causes encephalitis in cattle. Parasites within parasites are a double burden, best avoided by all behavioral means possible.

  Among primates, grooming to remove ectoparasites is of so much value that it can be exchanged for other resources like food or sex. Long-tailed macaques (Macaca fascicularis) have a biological market system where they pay for sex at the going rate in the currency of time spent grooming.25 And what better time for a parasite to hop onto a new host than when the hosts are having sex? Ectoparasite transmission during mating has been documented in guppy, stickleback, sage grouse, pheasant, rock dove, barn swallow, grackle, zebra finch, and bowerbird,26 not to mention humans.

  Most animals need sex to produce offspring and can’t avoid the disease risk that this brings. But they can take precautions. Primatologist Sean O’Hara observed that chimpanzees (Pan troglodytes) in the Budongo forest in Uganda regularly cleaned their penises, either with leaves or with their hands, after copulation.27 And rats that are prevented from grooming themselves after sex catch more genital infections.28

  Biologist Mark Pagel has proposed that being covered in a furry blanket—which requires constant grooming to keep lice, ticks, and other parasites under control—was so costly for some primates that, once they found other ways of keeping warm (fire, caves or clothes, for example), they pretty much gave up on hair altogether.29

  In a hot-zone world, animals also face a real dilemma when it comes to deciding about food. On one hand, a morsel may be tasty and nutritious, but on the other hand, it may contain a hungry microparasite. This is one of the most ancient problems animals have had to solve, and, as with sex, each species has had to find a balance: a trade-off between the likely benefits and risks. To the oystercatcher (Haematopus ostralegus), the biggest cockles (Cerastoderma edule) are the most appetizing and easiest meal. However, the biggest cockles also harbor the most helminthic parasites, for which the birds are the definitive hosts. Ecologist Ken Norris showed that birds were feeding not on the smallest, least-parasitized cockles, because they were too much effort to open, nor on the fattest, but the middle-sized cockles, balancing the need for a cheap and a safe feed.30 Butterfly fish (Chaetodon multicinctus), on the other hand, strike a different balance, actually preferring to feed on the bulbous lumps produced by coral infected with the cercariae of a tiny trematode. It seems that the extra energy gained from eating these fleshy extrusions that can’t retract themselves like healthy coral outweighs the costs of ingesting more parasites.31

  Predators have the same dilemma. It is much easier to kill and eat the sicker, weaker members of a prey troupe, but the predator that does so runs the risk of ingesting the parasite that made that individual sick and weak. Prey killed by predators are consistently infected with more trematodes, nematodes, and ectoparasites than randomly collected individuals.32 Feasting on the sick and the dead requires investment in a robust immune system.

  Humans, of course, also need to perform task 2. One of the categories of human disgust that our study identified is other species that might pose a parasite risk. We are repulsed by parasites themselves, when we can see them (including fictional versions in sci-fi horror movies); we avoid parasite hosts such as rats and parasite vectors such as cockroaches. And we are extremely careful about what we eat, especially when the food is another animal species or if it has been in contact with parasites.

  Task 3: Stay Away from Parasite Hot Zones in the Environment

  Conspecifics and other species are not the only places to encounter parasites. Animals that can detect and avoid hot zones in the environment have a comparative advantage in the race to get genes into the next generation.

  Ants of the species Temnothorax albipennis avoid building nests in sites where they find dead ants, because corpses signal a possible hot zone.33 If Acromyrmex striatus ants encounter a patch of fungal spores close to their nest, they close off the nearest entrance to help stop their nestmates from importing contamination.34 The water flea Daphnia magna has to make a difficult and dangerous trade-off calculation: If it swims near the surface, it may be eaten by murderous predatory fish. If it swims near the bottom, it may encounter the spores of murderous bacteria lurking in the mud. In a neat experiment, daphnia were forced to swim nearer to the bottom of their tank by the addition of “extract of predator” to the top. They paid the price: picking up an increased load of microbial parasites.35

  A nest is a handy adaptation for many species, providing shelter and protection from predators, but the downside is that your cozy home can also become a hot zone for parasites. Biologists in Switzerland offered great tits (Parus major) two kinds of used nest boxes to choose from. Half were infested with bloodsucking hen fleas (Ceratophyllus gallinae), while the other half had been microwaved. Of the twenty-three pairs of great tits that started breeding, three-quarters chose the parasite-free nests. The few that chose parasitized nests started their clutch an average of eleven days later, perhaps in the hope of outwaiting the fleas’ breeding cycle.36

  Nests can also harbor larger parasites—other birds. Cowbird chicks throw out resident chicks from a nest and assume their place; at least thirty-seven species of bird have been documented abandoning nests because of infestation with cowbirds.37

  Environments that are contaminated with excreta are also likely parasite hot zones. Soils that have been fertilized with dung produce richer, lusher, more nutritious grass, but they also tend to contain more parasite larvae. Through parasite-detecting lenses, the greenest grass shines brightest. In tests, sheep avoided grass laced with feces that contained gastrointestinal nematodes. They became less picky about what they ate when they were hungry,38 however, a phenomenon that has also been observed in humans. The parasitic potential of poo has even been evoked as an explanation for the phenomenon of animal migration. Reindeer and caribou may seek new pastures every year, not because of some mysterious wanderlust, but because they are looking for clean, dung-free pastures on which to feed, calve, and rear their young.39 When I alluded to this explanation for migration at a dinner party hosted by anthropologists, one guest told me that Kalahari bushmen have similar worries. “It’s getting dirty round here, time to move on!” she overheard one say to another. Another anthropologist related that Mongolian pastoralists do the same: timing migration to the buildup of human waste in camp.

  Humans have one more, possibly unique (mice are another candidate),40 means of detecting parasites in the environment. Humans pay attention when a parasite hot zone comes into contact with another object and remember what has happened. Like the infrared image of the hot spot left behind when a bird takes off, so humans remember the chain of contamination as if it were a series of hot spots. They can, for example avoid food that has fallen on the floor or a toothbrush that has been used by a stranger (we labeled this phenomenon “fomite” disgust in our web study).

  Task 4: Modify the Environment to Discourage Parasites

  There is one more strategy that animals can employ to reduce the dangers of parasitization—rather than avoiding them, they can make sure that hot spots don’t arise. They can actively modify their environments to discourage parasites. An animal that has found a nice bit of habitat to feed and multiply in doesn’t want it to fill up with wastes. Feces get in the
way, contain toxins, and harbor parasites and pathogens. So what to do with your poo? As we’ve seen, you can just migrate and leave it all behind you. If you are a sedentary species, however, your ancestors will have evolved ways to deal with this problem.

  Martha Weiss is the world expert on the poo-disposal practices of insects—although entomologists call it frass, not poo. She documents how leaf-cutting insects, like the caterpillars of the butterfly Chrysoesthia sexguttella, eat outward from the center of a leaf, leaving their droppings in the center, while those that eat inward, like the hispine beetle, leave a fringe of frass around the outside of the leaf. Her collection includes examples of “frass-flinging,” “turd-hurling,” and “butt-flicking.” Skippers use hydrostatic pressure to fling their pellets up to thirty-eight times their body length away (153 cm for a 4-cm-long larva). Geometrid larvae hurl their turds with their thoracic legs, and noctuids jerk their abdomens to flick poo pellets twenty body lengths away. Butterfly larvae remove their frass by head-butting it away or by hauling it with their mandibles off the side of the leaf.41

  Some animals are master compartmentalizers. Burrowing crickets use a specific corner of their chamber as a toilet and clean it up later.42 Eastern tent moths (Malacosoma americanum) build silken latrines. They string huge webs across tree branches and use the lowest point as a toilet; when it becomes overloaded with feces, it detaches under its own weight and falls to the forest floor.43 Fecal matter can also be put to good use. Some species of ambrosia beetle larvae pierce the walls of their cradles to eject feces, which the mother beetles carry off to manure fungus beds. Termites and some species of ants use their frass for nest building and for manuring their fungus gardens. Frass can even provide defense against predators. Cassidine beetle larvae exude a huge sticky wet fecal shield over their anal forks, to stop them from being bitten by predatory ants.44

  Though fecal wastes are a nuisance to solitary or familial insects, the social species require sanitation systems. Ants and the other eusocial insects have to take parasite control seriously because they are both sedentary, having to live with their wastes, and highly related, making it easy for infections to spread. Most ants remove fecal material, as well as sick and dead colony members, from their nests.45 The social crickets (Anurogryllus muticus) share a special latrine chamber, and social spider mites (Schizotetranychus miscanthi) always use the same spot within their nest for defecation.46

  Eusocial insects are masters at engineering their niches to make them unsuitable for pathogens and parasites. The nests of most social insects have many separate chambers rather than one huge hall. Mathematical models show that dividing nests into a series of rooms helps slow epidemics of disease.47 Ventilation systems help to the same end. Apart from modifying their physical environment to avoid the evils of excreta, insects can also modify their social environments—getting others to do their dirty work. Many species of ant have castes of cleaning workers who collect the feces, the sick, the dying, and the dead and carry them off to refuse piles a safe distance from the nest.48 There are subdivisions of labor, with the ants that do the dirtiest work—on the midden—being segregated from those that collect the wastes. Any attempt by midden workers to socialize with others is met with aggression.49 Older workers are more dispensable and are more likely to be found doing the dirty work.50

  Sedentary fish, reptiles, birds, and mammals all have the same problems as insects—they need to engineer their environments to keep them from becoming parasite hot zones. They also build parasite-free homes, keep them clean, throw out wastes, and get others to help in the task—if at all possible. Some fish species invest energy in not fouling their living and eating areas. In the Red Sea, the surgeonfish (Ctenochaetus striatus) stops feeding every five to ten minutes and swims to a spot of deeper water beyond the reef edge to defecate.51 Captive pike (Esox lucius) defecate away from the “home” area of their tank,52 and damselfish (Plectroglyphidodon lacrymatus) defecate in specific sites around the edges of their small territories.53

  Defecating around the edge of one’s territory is common in many animals (for example, gecko, elk, and antelope) and is usually explained as scent marking.54 However, it makes sense to keep parasite-ridden dung as far as possible from your feeding and living areas, as it does to deter rivals for your territory with the parasites that your dung may contain. Chimpanzees in zoos often throw feces at passersby, which may serve a similar function—to threaten rivals with parasites.

  Parasites are a big problem for baby birds—nestlings are a juicy and defenseless feed for a variety of ectoparasites, including ticks, mites, and blowflies. Parent birds try to make sure that the nest is not a hot zone for parasites by defecating elsewhere and by removing nestling excrement, eggshells, foreign debris, ectoparasites, and dead nestlings.55

  Most birds keep their nests clean of droppings. The chinstrap and Adélie penguins are a spectacular example. Like the frass-flinging insects, they stand up on the edge of their stony nests, turn their backs nest-outward, bend forward, lift their tails, and shoot out a projectile poo. The expelled material hits the ground about half a meter away from the bird.56 In fact, emperor penguin (Aptenodytes forsteri) poo makes such a mess on the ice around nests that it can be seen from space, providing a useful means of monitoring the breeding success of this vulnerable species.57 Barn swallows (Hirundo rustica) do it differently. Parent birds remove the fecal sacs of their nestlings and fly away with them, as can be seen on YouTube.58

  Sometimes nests need more than just keeping clean: they need fumigating. Blue tits (Parus caeruleus) on the island of Corsica adorn their nests with fragments of aromatic plants such as lavender and thyme, which contain many of the same compounds used by humans to make aromatic house cleaners and herbal medicines.59 These substances (linalool, camphor, limonene, eucalyptol, myrcene, terpinen-4-ol, pulegone, and piperitenone) have antibacterial, antiviral, fungicidal, insecticidal, and insect-repellent properties. Similarly, compounds in plants used for nest material have been shown to reduce the effects of fungi, bacteria, and ectoparasites on falcons and starling nestlings.60

  Female great tits (Parus major) also spend a good deal of time sanitizing nests. In most cases, only the female birds do the nest cleaning—if a male great tit loses its mate, the nest soon becomes contaminated with remains of food, pieces of peeling skin, or even dead chicks, and the chicks are more likely to die.61

  Some species even outsource their nest cleaning. One study found live blind snakes (Leptotyphlops dulcis) in 18 percent of the nests of eastern screech owls (Megascops asio). The snakes eat detritus and parasite larvae, which may make the owl broods healthier.62

  Many species of animals thus modify their physical niches by cleaning up wastes. Some even modify their niches by influencing the behavior of others so as to reduce the threat of infection from parasites and pathogens—not unlike the cleaning and tidying behavior of the human animal.

  From Disease Avoidance to Disgust

  The animal world presents a stunning array of behaviors that help to prevent parasite invasion and infection. From selective feeding, to grooming, to frass flinging, to outsourcing cleaning to other species or castes, it seems that every animal that has been studied has “parasite-detecting lenses” and commensurate parasite-avoidance practices. While some of these behaviors could serve purposes other than avoiding infection, there is enough here to suggest that animals have a huge variety of infectious-disease-avoidance strategies. But is this “disgust”?

  These behaviors are uncannily familiar, and the language used to describe animal disease avoidance is taken from the vocabulary of human behavior.63 Some animals even respond in ways that look very like human expressions of disgust. Lab rats (Rattus norvegicus) gape, open their mouths, gag and retch, shake their heads, and wipe their chins on the floor when fed aversive tasting substances. Coyotes (Canis latrans) have been recorded retching, rolling on offensive food, and then kicking dirt over it. Monkeys react to offensive objects by sniffing and mani
pulation followed by breaking and squashing the item, dropping or flinging it away, and then wiping their hands.64

  Given the overlap between what humans find disgusting and what animals avoid, and given that the same purpose is served (the avoidance of infection with parasites), should we keep the use of the word disgust for humans alone?

  We are so used to thinking of disgust as a feeling that it seems odd to suggest that animals might have disgust, as we don’t know if animals have feelings or not. But if disgust is reframed as the system in brains that drives parasite-avoidance behavior, in whatever species, then whether animals feel disgust or not becomes irrelevant.

  If the function of disgust is the same across species, does this imply that the mechanisms that animals use to detect and avoid parasite hot zones are the same as in humans? Surely not. As with all adaptive features of all animals, some are similar because they share a common ancestry (homology), and some are similar due to parallel evolution (different solutions being found to the same problem). The systems that help ants avoid their infections will have little in common with the systems that make primates avoid theirs, for example.65 Nevertheless, animals with which we share recent common ancestors, such as rats and primates, are likely to share some of the mechanisms that we use in implementing disgust. In the near future, when we better understand its brain mechanisms and its genetic determinants, it will be possible to construct a comparative phylogeny of disgust across the animal kingdom, showing what is shared and what is not, including Homo sapiens as but one branch on the tree. It is exciting that it is rapidly becoming possible to trace the deep ancestry of animal traits such as disgust.

  While it is clear that disgust did not emerge fully formed in Homo sapiens, as many writers on the topic seem to propose,66 we might still expect human disgust to have some special features. Humans alone have a much expanded prefrontal cortex, and we can use the imaginative ability that this gives us to apply disgust more widely (and perhaps more wisely) than can other animals. Humans are conscious of disgust; we have feelings about it; we are able to visualize and talk about it; we are able to learn from it and about it, and to make plans to avoid it; and we are able to weave it into our social and cultural fabric. In short, we humans are able to use disgust in new ways that are unimaginable to our insect, bird, mammal, and primate relatives.