Parasite Rex

4 A Precise Horror

Ray Lankester had nothing but contempt for Sacculina, the barnacle that degenerates practically into a plant. He was appalled by the way it had clambered down the ladder of evolution, a symbol of all things backward and lazy. Strange, then, that Sacculina now turns out to be an emblem for just how sophisticated a parasite can get.

Lankester’s mistake didn’t stem simply from a loathing for all parasites; biologists of his day just didn’t know much about Sacculina. It’s true that these parasites start life as free-swimming larvae. Through a microscope they look like teardrops equipped with fluttering legs and a pair of dark eyespots. Biologists in Lankester’s day thought Sacculina was a hermaphrodite, but in fact, it comes in two sexes. The female larva is the first to colonize a crab. She has sense organs on her legs that can catch the scent of a host, and she will dance through the water until she lands on its armor. She crawls along an arm as the crab twitches in irritation or perhaps the crustacean equivalent of panic. She comes to a joint on the arm, where the hard exoskeleton bends at a soft chink. There she looks for the small hairs that sprout out of the crab’s arm, each anchored in its own hole. She jabs a long hollow dagger through one of the holes, and through it she squirts a blob made up of a few cells. The injection, which takes only a few seconds, is a variation on the moulting that crustaceans and insects go through in order to grow. A cicada sitting on a tree separates a thin outer husk from the rest of its body, and then pushes its way out of the shell. It emerges with a new exoskeleton that stays soft long enough to stretch as the insect goes through a growth spurt. In the case of the female Sacculina, however, most of her body becomes the husk that is left behind. The part that lives on looks less like a barnacle than a microscopic slug.

The slug (whose existence was discovered only in 1995) plunges into the depth of the crab. In time it settles in the crab’s underside and grows, forming a bulge in its shell and sprouting the roots that so appalled Lankester. Biologists still call these things roots, but they are hardly like what you find under a tree. Fine fleshy fingers cover them, much like the ones lining our own intestines or the skin of a tapeworm. Unlike the exoskeleton of a regular crustacean, it is never moulted. Instead, the roots draw in nutrients dissolved in the crab’s blood. The crab stays alive during this entire time; you can’t tell it apart from healthy crabs as it wanders through the surf, eating clams and mussels. Its immune system can’t fight off Sacculina, and yet it can go on with its life with the parasite filling its entire body, the roots even wrapping around its eyestalks.

The female Sacculina’s bulge grows into a knob. Its outer layer chips away, slowly revealing a portal at the top. She will remain at this stage for the rest of her life unless a male larva finds her. He lands on the crab and walks along its body until he reaches the knob. At its summit, he finds the pin-sized opening. It’s too small for him to fit into, and so, like the female before him, he moults off most of himself, injecting a vestige of it into the hole. This male cargo—a spiny, reddish brown torpedo a hundred-thousandth of an inch long—slips into a pulsing, throbbing canal, which carries him deep into the female’s body. He casts off his spiny coat as he goes, and in ten hours he ends up at the bottom of the canal. There he fuses to the female and begins making sperm. There are two of these wells in each female Sacculina, and she typically carries two males with her for her entire life. They endlessly fertilize her eggs, and every few weeks she produces thousands of new Sacculina larvae.

The crab begins to change into a new sort of creature, one that exists to serve the parasite. It can no longer do the things that would get in the way of Sacculina’s growth. It stops moulting and growing, which would funnel away energy from the parasite. Crabs can typically escape from predators by severing a claw and regrowing it later on. Crabs carrying Sacculina can lose a claw, but they can’t grow a new one in its place. And while other crabs mate and produce a new generation, parasitized crabs simply go on eating and eating. They have been spayed. The parasite is responsible for all these changes.

Despite being castrated, the crab doesn’t lose its urge to nurture. It simply directs its affection toward the parasite. A healthy female crab carries her fertilized eggs in a brood pouch on her underside, and as her eggs mature she carefully grooms the pouch, scraping away algae and fungi. When the crab larvae hatch and need to escape, their mother finds a high rock on which to stand, and she bobs up and down to release them from the pouch into the ocean current, waving her claws to stir up more flow. The knob that Sacculina forms on a crab sits exactly where the brood pouch would be, and the crab treats the parasite knob as if it were its own pouch. She strokes it clean as the larvae grow, and when they are ready to emerge, she forces them out in pulses, shooting out heavy clouds of parasites. As they come spraying from her body she waves her claws to help them on their way. Male crabs aren’t out of reach from Sacculina’s powers, either. Males normally develop a narrow abdomen, but infected males grow abdomens as wide as females, wide enough to accommodate a brood pouch or a Sacculina knob. A male crab even acts as if he has the female’s brood pouch, grooming it as the parasite larvae grow and bobbing in the waves to release them.

Simply living within another organism—locating it, traveling through it, finding food and a mate inside, altering the cells that surround it, outwitting its defenses—is a tremendous evolutionary accomplishment. But parasites such as Sacculina do more: they control their hosts, becoming in effect their new brain, and turning them into new creatures. It is as if the host itself is simply a puppet, and the parasite is the hand inside.

This puppetry takes different forms depending on the particular parasite and what it needs from its host at its particular stage of life. When a parasite has first settled into a comfortable spot in its host, food is the first order of business. Once a tobacco hornworm has been rendered defenseless by the viruses of the parasitic wasp Cotesia congregata, the wasp’s eggs are ready to hatch and grow. Rather than just passively soak up the food around it, the wasp changes the way its host eats and digests its food. The more wasps in a given host, the bigger the host will grow—up to twice its normal size. And once the caterpillar eats a leaf, the wasps alter the way it breaks it down. Normally a hornworm would convert a lot of the leaf into fat, a stable form of energy that it can store away for the time when it will fast inside its cocoon. But once it is infected by wasps, the hornworm turns its food into sugar, a quick source of energy that the parasites use for fast growth.

A parasite lives in a delicate competition with its host for the host’s own flesh and blood. Any energy that the host uses itself could go instead to the growing parasite. Yet, a parasite would be foolish to cut off the energy to a vital organ like the brain, since the host would no longer be able to find any food at all. So the parasite cuts off the less essential things. As Cotesia congregata robs the caterpillar of its fat stores it also shuts down its host’s sex organs. Male caterpillars are born with big testes, and normally they channel a lot of the energy from their food into building them up even more. When a parasitic wasp lives inside the male, however, the testes shrivel up. Castration is a strategy that any number of parasites have hit on independently—Sacculina does it to crabs, and blood flukes do it to the snails they invade. Unable to waste energy on building eggs or testes, on finding a mate, or on raising young, a host becomes, genetically speaking, a zombie: one of the undead serving a master.

Even flowers can become zombies to their parasites. A fungus called Puccinia monoica lives inside mustard plants that grow on the slopes of Colorado mountains. The fungus sends its tendrils throughout the stem of the mustard plant, feeding on the nutrients the flower draws from the sky and the soil. In order to reproduce, it needs to have sex with the Puccinia inside another mustard plant. To do so, the fungus stops the plant from sending up its own delicate little flowers and forces it to turn clusters of its leaves into brilliant yellow imitations of flowers. These fakes look exactly like other flowers found on the mountains, not just in visible light but in ultraviolet light as well. They lure bees, which can feed on a sweet, sticky substance that the fungus forces the plant to produce on the imitation flowers. The fungus crams its sperm and its female sex organs into them, so that the bees can fertilize the fungus as they travel from mustard plant to mustard plant. But the plant itself remains sterile.

No matter how comfortable a parasite may make itself by altering its host, it has to leave sooner or later. Some parasites head on to the next host in their life cycle, others go to a free-living adulthood, and in many cases the parasites stage-manage a careful exit. Simply letting the host go on with its normal life would mean death for most parasites. The tobacco hornworm normally moults five times and then wanders down from its plant to the ground. It digs a few inches into soil and forms its cocoon, where it stays until it emerges as a moth. When hornworms are parasitized by the wasp Cotesia congregata, however, they take a different path. They moult only twice, and they never get the call to wander off their plant. Instead, they go on chewing leaves, nurturing their parasites until the wasps are ready to emerge. The hornworm then slows down and stops eating, losing its appetite. The wasps seem to be responsible for the anorexia, because a healthy hornworm will happily devour dozens of wasp cocoons.

Another species of wasp goes even further, turning its host—the cabbage worm caterpillar—into a bodyguard. When the wasp’s larvae have matured, they paralyze the cabbage worm and push their way out of its abdomen. They then spin their cocoons on the underlying leaf. Yet, even after the wasps have devoured the guts of the caterpillar and riddled it with escape hatches, the cabbage worm recovers. It doesn’t limp away; instead, it weaves a mesh over the wasps to shield them from other parasites and coils itself on top. If anything should disturb the caterpillar as it stands guard, it lashes out, biting and spitting up noxious liquids—in other words, protecting the cocoons. Only when the wasps emerge from their cocoons does the cabbage worm end its duty to them and lie down to die.

While wasps can live on dry land once they’ve left their hosts, many other parasites need to get to water. There are parasitic nematodes, for instance, that live as free-living adults in streams, where they mate and lay their eggs. When their offspring hatch, they attack the mayfly larvae that live alongside them. The nematodes pierce through the mayfly’s exoskeleton and curl up inside its body cavity. There they grow as the mayfly grows, siphoning off its food. The mayflies go through a long, lingering insect adolescence in the water before they transform into delicate, long-winged forms. The males rise from the water and form great clouds that attract the females. The nematodes rise invisibly into the cloud within their hosts.

Male and female mayflies find each other in the swarm. Embracing, they fall to the grasses and reeds along the stream, and mate. You can tell the difference between the sexes not only by their genitals (the males have little claspers to help them mate) but by other parts of their bodies such as their eyes: the female has small eyes pointing out to either side, while those of the male bulge out so much that they touch over the top of its head. Once they’ve mated, the males have finished their life’s work. They fly lazily away from the stream to find a place to die. The females, meanwhile, make their way upstream to find a protruding rock. They crawl under it and bob their abdomens up and down as they lay their eggs. If the female is carrying a nematode, the full-grown parasite breaks out of the mayfly’s abdomen and burrows away into the gravel to find a mate of its own, leaving its host dead.

The nematode’s strategy has one big, obvious flaw: if it happens to climb inside a male mayfly, it will end up in a patch of grass. Instead of getting back to the water, it will die with its host. The nematode has a solution, one that’s reminiscent of Sacculina: it turns the male into a quasi-female. When an infected male mayfly matures, he never forms his claspered genitals or even his high-domed eyes. The nematode makes him not only look like a female but act like one, too. Instead of flying away, he drops down to the stream, even going so far as to try to lay imaginary eggs as the parasite bursts out of his body.

The nematode needs to get back to the stream for two reasons—to move on to the next stage of its life, and to be in a place where its offspring will be able to find a mayfly of their own to invade. Getting to the next host is a consuming passion among parasites, because there is no alternative: “Live free and die” is their motto. A fungus that lives inside house flies provides a spectacular example of this. When the spores of the fungus make contact with a fly, they stick to its body and dig tendrils into the fly’s body. The fungus spreads throughout the fly’s body with Sacculina-like roots and sucks up the nutrients of its blood, making the fly’s abdomen swell as it grows. For a few days the fly lives on normally, flying from spilled soda to cow turd, using its proboscis to sponge up food. But sooner or later it gets an uncontrollable urge to find a high place, be it a blade of grass or the top of a screen door. It sticks out its proboscis but uses it as a clamp this time, gluing itself to its high perch.

The fly lowers its front legs, tilting its abdomen away from the surface. It flaps its wings for a few minutes before locking them upright. The fungus has meanwhile pushed its tendrils out of the fly’s legs and belly. On the tips of the tendrils are little spring-loaded packages of spores. In this bizarre position, the fly dies, and the fungus catapults out of its corpse. Every detail of this death pose—the height, the angles of the wings and the abdomen—all put the fungus in a good position for firing its spores into the wind, to shower down on flies below.

As if this were not enough of an accomplishment for a speck of fungus, infected flies always die in this dramatic way just before sunset. If the fungus matures to the point where it can make spores in the middle of the night, it doesn’t: it holds off the process, waiting through the dawn and the day. It is the fungus, not the fly, that decides not only how it will die but when—just before sundown. Only then is the air cool and dewy enough for the spores to develop quickly on another fly, and only then are healthy flies leaving the air for the night and moving down toward the ground, where they make easy targets.

Parasites such as this fungus use their hosts to get to other hosts of the same species. But for many other parasites, the game is more complicated: they have to make their way though a whole series of different animals. Sometimes they force their current host to get into the vicinity of their next one. Along the coasts of Delaware lives a fluke that uses mud snails as its first host and fiddler crabs as its second. The only problem is that the snails live in the water and the crabs live on shore. But when the snails are infected by the fluke, they change their behavior. They grow restless; they wander onshore or onto sandbars during low tides and linger there while healthy snails keep to the water. They shed their flukes on the sand, putting the parasites so close to the fiddler crabs that they can easily burrow into them. It’s as simple as getting a taxi to a bus station.

Another species of fluke can be found in the meadows of Europe and Asia, along with a few in North America and Australia. Known as Dicrocoelium dendriticum, or the lancet fluke, it makes cows and other grazers its host as an adult, and the cows spread their eggs in their manure. Hungry snails swallow the eggs, which hatch in their intestines. They drill through the wall of a snail’s gut and settle in the digestive gland. There the flukes produce a generation of cercariae, which make their way to the snail’s surface. The snail tries to defend itself from the parasites by blocking them off with walls of slime. The slime balls up around the cercariae, which the snail coughs up and leaves behind in the grass.

Next, along comes an ant. To an ant, a slime ball is positively delicious. Along with the slime, the ant may also swallow hundreds of lancet flukes as well. The parasites slide down into its gut, and they then wander for a while through its body, eventually moving to the cluster of nerves that control the ant’s mandibles. The parasites all travel together on this trip, but after visiting the nerves, they split up. Most of the lancet flukes head back to the abdomen, where they form cysts, but one or two stay behind in the ant’s head.

There they do some parasitic voodoo on their hosts. As the evening approaches and the air cools, the ants find themselves drawn away from their fellow ants on the ground and upward to the top of a blade of grass. Like flies infected with a fungus, the ants clamp down on the tip of the grass. But the lancet fluke has a different goal than the fungus does. The fungus uses its host as a catapult to shower its spores on other insects. The lancet fluke can continue to live only if it can get inside its final host, a mammal. Clamped to the tip of a grass blade, the infected ant is likely to be devoured by a cow or some other grazer passing by. When the ant tumbles into the cow’s stomach, the flukes burst out and make their way to the cow’s liver, where the flukes will live as adults.

But the lancet fluke, like the fungus, is very aware of the passing of time. If the ant sits the whole night without being eaten and the sun rises, the fluke lets the ant loosen its grip on the grass. The ant scurries back down to the ground and spends the day acting like a regular insect again. If the host were to bake in the heat of the direct sun, the parasite would die with it. When evening comes again, it sends the ant back up a blade of grass for another try.

Most parasites rarely try this sort of thing on humans, but a few do it very well. The guinea worm spends its early life curled up inside a copepod swimming in water. A person drinking that water swallows the copepod, and when it dissolves away in stomach acid, the guinea worm escapes. It slips into the intestines and burrows out into the abdominal cavity. From there it wanders through the connective tissue until it finds a mate. The two-inch male and the two-foot female have sex, and then the male looks for a place to die. The female slithers through the skin until she reaches a leg. As she travels, her fertilized eggs begin to develop, and by the time she has reached her destination the eggs have hatched and become a crowd of bustling juveniles in her uterus.

These juveniles need to get into a copepod if they are to become adults themselves, and so they drive their human host to water. They press against their mother’s uterus so hard that they force it partially out of her body, letting some of the larvae spill out. Adult guinea worms tame the human immune system so that they can travel through our bodies unharmed, but the juveniles do just the opposite. They draw a quick reaction that brings immune cells rushing to them, making the skin around them swell and blister. The easiest way for a victim to get some relief from the hot pain of the wound is to pour cool water on it or just stick the leg in a pond. The juveniles that have already escaped their mother inside the blister respond to the splash by swimming free. The mother responds to the water as well by getting rid of more of her young. She doesn’t herniate herself the way she did before; this time she lets her babies escape through an even stranger route: her mouth. For every splash, half a million baby guinea worms come heaving up through her esophagous. The contractions pull her out of the wound bit by bit until she and her young have all left the host—the mother to die, the young to search the water for a new copepod to curl up inside.

This manipulation works best when humans and copepods all depend on scarce supplies of water, because that makes it more likely a person will dump guinea worm larvae where their next host can be found. Not surprisingly, dracunculiasis, the disease caused by the guinea worm, is particularly bad in deserts, where people crowd around oases.

The guinea worm is the sort of parasite that is content to sit in its first host until it is accidentally swallowed by its next one. Other parasites don’t rely so much on luck. Their hosts come into regular contact, usually to eat or be eaten. Biting insects seek out humans and other vertebrates and drink their blood, and they are—not coincidentally—filled with parasites trying to get into us. Malaria and filariasis are spread by mosquitoes, sleeping sickness by tsetse flies, kala-azar by sand flies, river blindness by black flies. (Bacteria and viruses come along for the ride as well, spreading bubonic plague, dengue fever, and other diseases.) These parasites swim into the wound made by the insect and then live in our skin or bloodstream, where they are likely to be taken in the bite of the next passing insect. But simply being in the right place is not enough for many of them—they change the behavior of the insects to make them spread the parasites faster.

Drinking blood is not easy. When a mosquito lands on your arm, it has to drive its proboscis through the tough outer layers of your skin and then snake it around for a while to find a blood vessel. The longer it takes, the better its chances of getting slapped and being reduced to a bloody smear. And once the mosquito hits blood, your body responds by clotting the wound. Platelets swarm around the mosquito’s proboscis, releasing chemicals that make them form sticky clumps and attract other platelets. As the mosquito tries to drink, its smooth cocktail of blood turns into a thick milk shake. To buy themselves more time, mosquitoes put chemicals in their saliva that fight against the clotting. One of them, apyrase, cuts apart the glue made by the platelets; other chemicals widen blood vessels to bring in more blood.

The risks of drinking blood make mosquitoes afraid of commitment. If they find it too difficult to draw blood from a host, they’ll quickly fly to a new patch of skin. But if that host has malaria, the parasites inside will make him more attractive. Malaria interferes with the platelets of its host, making them do a bad job of clotting. When a mosquito hits blood in a person with malaria, it will find it easier to drink and will be more likely to suck it up, and the parasite along with it.

Once it gets into a mosquito, Plasmodium needs time before it can travel into another human. It needs to move into the mosquito’s gut, mate with other Plasmodium parasites, and reproduce. More than ten thousand ookinetes are formed this way in ten days. They develop into sporozoites that migrate up to the salivary gland, where they’re finally ready to enter a human. But up to that point, it doesn’t do the parasite any good for the mosquito to eat. The risks of getting squashed in midbite are offset by no benefit. So Plasmodium does its best to discourage its host from eating. A mosquito with ookinetes in it will give up trying to take a blood meal more easily than a parasite-free one.

Once the parasite has reached the mosquito’s mouth, though, it wants the mosquito to start biting as much as possible. Plasmodium travels to the salivary glands, homing in on a lobe that is responsible for making the anticoagulant molecule apyrase. There it proceeds to cut off the mosquito’s apyrase supply, so that when the insect drives its proboscis into a new host, it has a harder time keeping the blood flowing. It has to visit more hosts to drink the same amount of blood. At the same time, Plasmodium makes the mosquito hungrier, drinking more blood and visiting more hosts to get it. As a result, a sick mosquito is twice as likely as a healthy one to drink the blood of two people in a night. The sick mosquito, carrying more blood to more hosts, becomes a far more effective way to spread malaria.

Plasmodium makes a predator—a mosquito—come into contact with its prey—us. Parasites can use the opposite arrangement as well, by living first in prey and waiting until a predator eats it. Some parasites are willing to sit and wait for their intermediate host to be devoured. But many are not so patient. A fluke called Leucochloridium paradoxum makes snails its first host, but makes insect-eating birds its final host, even though the birds have no appetite for snails. The flukes get the bird’s attention by pushing their way into the eye tentacles of the snail. Covered in brown or green stripes, the parasites are visible through the transparent tentacles, and to a bird they look like caterpillars. A bird attacks the snail and ends up with nothing but a bellyful of parasites.

Other parasites can change their host’s skin to become a more obvious target. Some species of tapeworms live in the guts of the threespine stickleback fish for a few weeks, and when they want to get into a bird, they turn the fish orange or white. They can also alter the behavior of the fish to get the attention of the birds. Normally, sticklebacks keep diligently away from the water birds that like to eat them. They try to stay well below the water’s surface, and if a heron should stick its head underwater, they will dart away, passing up the opportunity to eat. But when they are infected by tapeworms, they become buoyant so that they can’t help but swim near the surface, and they become fearless as well, chasing after food even if a bird is dangerously close by.

Sometimes it’s not enough for a parasite to make its host vulnerable to attack; sometimes it sends its host straight into harm’s path. Such is the case with thorny-headed worms. Many species of these parasites start off inside invertebrates that live in lakes and rivers. They then become adults in birds, where they drive their barbed heads deep into the lining of the intestines. A small crustacean named Gammarus lacustris feeds near the surface of ponds and rivers, but as soon as its predator—a duck—comes around, it escapes by diving away from the light and thus down to the bottom of the water. When a thorny-headed worm gets inside a Gammarus, though, it does the exact opposite. If a duck comes on the scene, Gammarus feels an unshakable attraction toward light—and thus moves up to the surface of the water. When it reaches the surface, it skims along until it finds a rock or a plant. Once it makes contact, it clamps its mouth down, practically offering itself up to the duck.

Toxoplasma, the protozoan lodged in billions of human brains, may seem like a gentle creature that wouldn’t get involved in mind control. After all, it hides safely in its cysts and declines to kill its hosts. But its tameness is only part of its unconscious calculation of how to boost its odds of getting into its final host. Toxoplasma needs to move between cats and their prey and back to complete its life cycle, and a dead rat won’t attract many cats. But Toxoplasma, it turns out, does what it can to help the cats kill their prey.

For several years scientists at Oxford University have been studying the effects of Toxoplasma on the behavior of rats. They built a six-foot by six-foot outdoor enclosure and used bricks to turn it into a maze of paths and cells. In each corner of the enclosure they put a nest box along with a bowl of food and water. On each nest they added a few drops of a particular odor. On one they added the scent of fresh straw bedding, on another the bedding from a rat’s nest, on another the scent of rabbit urine, on another the urine of a cat. When they set healthy rats loose in the enclosure, the animals rooted around curiously and investigated the nests. But when they came across the cat odor, they shied away and never returned to that corner. This was no surprise: the odor of a cat triggers a sudden shift in the chemistry of rat brains that brings on intense anxiety. (When researchers test anti-anxiety drugs on rats, they use a whiff of cat urine to make them panic.) The anxiety attack made the healthy rats shy away from the odor and in general made them leery of investigating new things. Better to lie low and stay alive.

Then the researchers put Toxoplasma-carrying rats in the enclosure. Rats carrying the parasite are for the most part indistinguishable from healthy ones. They can compete for mates just as well and have no trouble feeding themselves. The only difference, the researchers found, is that they are more likely to get themselves killed. The scent of a cat in the enclosure didn’t make them anxious, and they went about their business as if nothing was bothering them. They would explore around the odor at least as often as they did anywhere else in the enclosure. In some cases, they even took a special interest in the spot and came back to it over and over again.

By turning rats into rodent kamikazes, Toxoplasma probably increases its chances of getting into cats. If it makes the mistake of getting into a human instead of a rat, it has little hope of making that journey, but there’s some evidence that it still tries to manipulate its host. Psychologists have found that Toxoplasma changes the personality of its human hosts, bringing different shifts to men and women. Men become less willing to submit to the moral standards of a community, less worried about being punished for breaking society’s rules, more distrustful of other people. Women become more outgoing and warmhearted. Both changes seem to break down the fear that might keep a host out of danger. They’re hardly enough to make people throw themselves at lions, but they’re a very personal reminder of the ways in which parasites try to take control of their destiny.

Scientists have known about these sorts of transformations for more than seventy years, but they didn’t think they were actually manipulations. Parasites couldn’t possibly mastermind pinpoint changes to their plainly superior hosts. They could only cause random kinds of harm, and maybe by chance the damage altered their host. Only in the 1960s did scientists begin to think seriously about the possibility that a parasite might be able to engineer the physiology of its host, or even its behavior. And thereupon emerged a long line of cases that seemed, on their faces, to be just that.

Most of the cases came from eukaryote parasites, although certainly bacteria and viruses can act as puppet-masters sometimes. A sneeze carries away cold viruses to new hosts; the Ebola virus seems to take advantage of our respect for the dying and the dead by making its victims gush blood, which gets on the bodies of people handling their bodies, infecting them as well. But if you look over the documented cases of manipulators, bacteria and viruses make up a tiny portion. It may be that their needs are pretty simple: they rarely need to use more than one species as a host, and they can just ride along during the regular contacts between hosts—be it sex, a handshake, or the bite of a tick. There may in fact be a lot of manipulators waiting to be revealed among bacteria and viruses. They may still be hidden, thanks to the fact that most people who study viruses and bacteria primarily think in terms of diseases, symptoms, and cures. They tend not to think like parasitologists, who treat their subjects more as living beings that have to survive in their hosts and get to new ones.

The great danger in studying parasite manipulations is to see cunning strategies of parasites where none exist. Some changes to a host can be simple damage. And if a person can tell that a parasite has changed the color of a fish, that doesn’t really mean anything. What matters is whether the change actually makes it easier for a bird to eat it. The only way to demonstrate that a manipulation is genuine is to run experiments, and the first ones that demonstrated real manipulations with significant effects were performed in the 1980s by Janice Moore, a parasitologist at Colorado State University. Her parasites of choice were a species of thorny-headed worms that live as larvae inside pill bugs on the forest floor, live as adults in starlings, and pass their eggs out in the bird droppings for more pill bugs to pick up.

Moore built chambers out of Pyrex pie plates to measure the behavior of the infected pill bugs. In one experiment, she wanted to see how the pill bugs responded to humidity. She set one plate on top of another to create an enclosed space. Then she divided the space into two chambers with a glass barrier, leaving only a narrow slit between them, which she covered with a piece of nylon mesh. She made one of the chambers humid by pouring into it potassium dichromate—a chemical that reacts with air to make water. In the other side she poured salt water, which made the air dry by pulling water out of it. She then let a few dozen pill bugs loose inside the pie plate house she had built, and waited to see which chamber, humid or dry, they chose. Afterward, she dissected them and looked inside to see whether they carried the larvae of thorny-headed worms.

In another experiment, she built a little shelter for the pill bugs with a tile sitting on top of four pebbles in the middle of a pie plate. She watched to see whether they hid under it or walked out in the open. And in a third one, she poured colored gravel into a pie plate—one half white, the other black—to see whether pill bugs were drawn to light or dark backgrounds.

Pill bugs live in moist forest soils, where they can hide from the birds that would eat them. If you take them out, they’ll scurry back in. They’re attracted to the soil by factors like humidity, dim light, and dark colors. The healthy pill bugs that Moore studied behaved this way in her pie plates. They stayed in the humid chamber and avoided the dry one; they hid under the shelter she made for them; and they chose dark gravel over light. But the pill bugs that carried thorny-headed worms could be found wandering into the dry part of her chamber much more often than the healthy ones. A parasite would make its host crawl over the white gravel more often, and be far less likely to hide under the shelter. The parasitized pill bugs could no longer recognize these vital clues, and they became easier prey for birds.

But rather than imagine what might make a bird’s life easier, Moore let the birds tell her themselves. She let pill bugs roam around a cage in which she kept starlings. The birds ate the pill bugs, and she found that they preferred the infected ones over the healthy ones. In another experiment, she set up nest boxes for starlings, which came and raised nestlings in them. They would hunt in the surrounding fields for food—including pill bugs—and bring it back to the box. Moore loosely tied pipe cleaners around the necks of the nestlings, closing off their throats just enough so they couldn’t swallow their meals. By picking through their mouths and the nest, Moore could collect the pill bugs the adult birds had brought. She dissected them to check for parasites and found that the parasitized pill bugs turned up in the nests far more often than they should have. At a typical site, fewer than 1 percent of the pill bugs carried the thorny-headed worms, but 30 percent of the ones Moore collected from the nestlings were infected.

Moore’s experiments were followed by other careful tests, and in many cases the parasites in question did indeed boost their success by altering their hosts. Once parasitologists showed that these manipulations were real, they began to ask how exactly the parasites manage them. Each parasite probably uses its own special mechanism, some of which may be pretty simple. When tapeworms grow inside three-spined sticklebacks, filling their entire body cavity and soaking up most of the food their hosts eat, they probably make the fish ravenous. Their hunger pushes the sticklebacks to take more risks to get food, not to dart away when they realize a bird is nearby. To the tapeworm, danger means deliverance.

More often, though, the mechanisms are far more sophisticated. Parasites have mastered the vocabulary of their hosts’ neurotransmitters and hormones. Parasitologists are pretty confident that this is the case, even though they haven’t yet found a particular molecule that they know can alter a host in a particular way. The bodies and brains of animals are just too noisy with the traffic of signals for scientists to catch a quick transmission from parasites. But parasitologists can still say a lot about those parasitic molecules indirectly, in the same way you can judge a man by his shadow.

Recall for a moment poor Gammarus, sent hurtling up to the surface of a pond by a thorny-headed worm, where it clamps down on a rock until a duck eats it. Clearly, something is wrong with its nervous system, because the same sensation that would send a healthy Gammarus to a river bottom produces the opposite reaction in a sick one. Biologists have pulled out the neurons of Gammarus infected with thorny-headed worms. They’ve stained them with compounds that make the neurons light up if they carry certain neurotransmitters. When they’ve looked for a neutrotransmitter called serotonin, the neurons have lit up like Christmas trees.

You can find serotonin in just about any animal you look at. In humans and other mammals, it seems to stabilize the brain. When levels of serotonin drop, people may become obsessive, depressed, violent. (Prozac is designed to counter depression by boosting serotonin.) Serotonin also plays a role in invertebrate brains, although scientists aren’t sure what that role is. They do know that something interesting happens when they inject serotonin into Gammarus. If a healthy Gammarus gets a shot, it will often try to grab on to something and hold tight.

Why should serotonin cause Gammarus to cling? It may have something to do with sex. When Gammarus mate, the male grabs the female with his legs and pulls his abdomen down toward hers. He will ride her for days, waiting for her to moult. When she does, she puts her eggs in a pouch under her belly. The male fertilizes the eggs and continues to hold on, guarding her against other males that want to mate.

The mating male’s pose is exactly like the one that thorny-headed worms force Gammarus to take. And if parasitologists inject a drug into infected Gammarus that blocks the effects of serotonin, they stop clinging for a few hours. It may be that the thorny-headed worm secretes a serotonin-boosting molecule. The parasite may trigger a sequence of signals that makes the Gammarus think it’s having sex, even making the females take on the male’s role in the mating.

When parasitologists figure out the full story of parasitic manipulators, it will turn out to be more sophisticated than this. It’s unlikely that parasites use a single molecule to control their hosts; they come equipped with a big pharmacy full of drugs ready to be dispensed at different times in the parasite’s life when it needs different things. That’s the picture that emerges when scientists have pooled their efforts to study the full cycle of one particular parasite, such as the tapeworm Hymenolepis diminuta. Hymenolepis adults live and mate inside the bowels of rats, where they grow to be a foot and a half long. Their eggs end up in rat droppings, which are regularly devoured by beetles. Once inside a beetle, the tapeworm’s egg membrane dissolves away, revealing a spherical creature with three pairs of hooks. It uses those hooks to claw out of the beetle’s gut and into its circulatory system, where it grows in a little over a week into a short-tailed form. There it waits for the beetle to be eaten by a rat, where it will take its final adult form. The whole cycle often takes place in grain silos or flour warehouses, where the beetles devour the food, the rats eat the beetles, and then the rats leave their droppings in the grain.

The tapeworms begin manipulating the beetles even before they are inside them. Beetles are lured to egg-laden droppings by an aroma that’s apparently irresistible to the insects. If a beetle should come across droppings from a healthy rat and droppings from a parasitized one, it’s more likely to choose the pile with the tapeworm eggs. If you trap the fragrance of infected dung and preserve it in liquid, a drop of this perfume will bring beetles scurrying. No one knows if the eggs themselves produce the scent, or if it’s one of the chemicals produced by the adult tapeworms inside the rats, or if the parasites somehow change that rat’s digestion so that the host itself makes it. Whichever is the case, it’s enough to seduce the beetles into eating a tapeworm, perhaps into being eaten by a rat.

Once inside the beetle, the tapeworm then uses more chemicals to sterilize it. Like most other insects, a beetle stores up reserves of energy in a structure called the fat body that runs along its back. Female beetles use some of this material to build the yolks for their eggs. To get the reserves to the eggs, they have to send a hormone signal to the fat body. The fat body cells respond to it by making a yolk ingredient called vitellogenin. The vitellogenin leaves the fat body and flows through the beetle until it reaches the eggs in the ovaries. A beetle egg is surrounded by a retinue of helper cells that leave only a few cracks between them. The cracks are so few and so small, in fact, that it’s hard for anything to get through them and to the egg itself. But when the right hormones latch onto these helper cells, they make them shrink, opening up the spaces. With enough of these hormones, the vitellogenin can reach the egg itself and turn into yolk.

The tapeworm can destroy this chain of events at several links. It makes a molecule that gets into the fat body and slows down the cells as they make vitellogenin. Some vitellogenin still gets out of the fat body, but little of it seems to reach an egg. It appears that the tapeworm makes yet another molecule that can lock into the receptors on the helper cells in the ovaries. It plugs up the receptors to stop the hormone from latching on and making the helper cells shrink. The helper cells stay swollen, so the vitellogenin can’t get into the egg. The effect of these molecules is to stop the beetle from diverting what could be perfectly good tapeworm food into its own eggs.

Once it has matured inside the beetle, the tapeworm is ready to find itself a rat. The beetle certainly wouldn’t agree, so the parasite has to pull open another drawer of drugs. Some of them—probably opiates that blunt feelings of pain and fear—make the beetle less conscientious about concealing itself. Put it on a pile of flour, and the beetle will be likely to wander the surface instead of burrowing out of sight. The tapeworm makes it sluggish, slow to escape from an attack. Still, an infected beetle does its best to defend itself if a rat should take it in its jaws. A flour beetle comes equipped with a pair of glands on its abdomen that it uses to release a foul-tasting chemical, and a rat that grabs the beetle in its mouth is likely to spit it out. But once the tapeworm reaches maturity, it blocks the gland from making its poison. When the infected beetle tries to defend itself, it doesn’t taste all that bad to the rat; it is thus far more likely to be eaten than a healthy counterpart. From beginning to end, the beetle is guided and tugged by its parasite.

If you turn off the Ventura Freeway at the town of Carpinteria, California, and drive a short way toward the ocean, passing a teddy bear warehouse and a set of train tracks, you come to a chain link fence. Beyond it lies a low expanse covering hundreds of acres of lush low plants like pickleweed. This is the Carpinteria salt marsh. One clear summer day, an ecologist named Kevin Lafferty unlocked the fence gate and led me inside. He wanted to show me how a salt marsh works. Lafferty was dressed in a pair of bathing trunks and a fraying T-shirt with fluorescent lion fish on it; he shuffled along the dirt path in flip-flops, with a pair of scuba booties in one hand. I spent a few days all told in the company of Lafferty, and during my entire visit I saw him in nothing more formal. His face was young and his hair was wheat-colored. He has surfed along these beaches since he came to the University of California at Santa Barbara in 1981. It would be hard now to pick him out on a wave as a biology professor instead of a sophomore.

He talked about the marsh as we walked toward the sea on a raised dirt path. “You need some sort of interior space below sea level to get a salt marsh. You can have a river cut a channel and the sea is able to intrude upon it at high tide. That’s the standard East Coast version. Or you could have tectonic activity that leads to subsidence.” He gestured back inland, up toward the San Ynez Mountains, which loomed over the freeway, fog draped on them like a scarf. “The whole California coast line is a complicated mix of tectonic activity, plus changes in sea level. The basin here is thought to have been flooded by the ocean because it has subsided.” The area is now about a foot below sea level, so that the sediments carried by the Santa Monica and Franklin Creeks are dumped in this basin rather than reaching the sea. Each day the high tide pushes its way into the marsh, spilling over the creek banks and flooding this place all the way back to the chain link fence. “If the sea level stayed the same and there was no tectonic activity, this might be dry land in a hundred years. But if the land is continually subsiding, then the sediment can’t catch up,” says Lafferty. The opposing forces of accumulating sediment, incoming freshwater, and the ebb and flow of sea water have all reached a compromise in the form of this broad, water-logged expanse cut through by channels.

Each day at low tide, the soil bakes in the sun, evaporating its water while holding on to the brine. The soil is actually saltier in places than sea water. In these conditions no trees can survive. Instead, there is a low carpet of tough plants adapted to the salt. Pickleweed, for example, pumps the briny water out of the ground and stocks away the salt in its fruits, using the fresh water left behind. Along the bare mud flats that line the marsh channels, algae grow in dull green varnishes. The algae may look subdued, but they’re actually reveling in almost perfect conditions. The mud is packed with nitrogen, phosphorus, and other nutrients carried down from the mountains. Because the bare flats are exposed every time the tide drops, the algae get far more sunlight than they would if they were always submerged. Today at low tide the algae are photosynthesizing merrily. Scattered along the banks are thousands of miniature birthday hats: the conical shells of California horn snails that graze the algae. “They’re mowing a fast-growing lawn,” Lafferty says.

The many invertebrates here, such as littleneck clams and sand dollars, make good meals for vertebrates. Some fish, like the arrow gobies and the killifish, live in the estuaries year round, huddling in the low water when the tide ebbs and then feeding at high tide, when they’re joined by curious stingrays and sharks wandering in from the sea. Today the killifish are the only fish to be seen. They dart around, every now and then turning to one side to expose the brilliant glint of their bellies. Along the banks of the channels are bigger holes, these the size of fists rather than fingers. When the morning sun hits them, crabs slowly crawl out—lined shore crabs, which crack open the snails like walnuts, and fiddler crabs, which slowly raise their giant claws as if saluting the newborn day. There aren’t many mammal predators here—the growth of towns like Carpinteria has driven away the mountain lions and bears, leaving only raccoons, weasels, and house cats. But the salt marsh is still a carnival for birds—for Caspian terns, willets, plovers, yellowleg sandpipers, curlews, dowitchers—all picking their way through the feast.

Lafferty looks at all of this, the eating and being eaten, this transmutation of sunlight into different forms of life, and doesn’t see it quite the way other ecologists might. A curlew grabs a clam from its hole: “Just got infected,” he says. He looks at the bank of snails and says, “More than 40 percent of these snails are infected. They’re really just parasites in disguise. There are boxcars of parasite biomass here.” He points to the snowy constellation of bird droppings along the bank. “Those are just packages of fluke eggs.” He hears the things he’s been saying to me and shrugs. “I have a pretty warped perspective.”

When Laffterty started graduate school at Santa Barbara in 1986, his perspective wasn’t yet warped. If someone had asked him then to figure out the ecology of this salt marsh, he would have studied the things he could see. He would have measured how much algae the snails could eat, he would have added up the number of eggs a female killifish could lay in a year, he would have recorded the number of clams a bird could eat in a day. He would, he now realizes, have completely missed the real drama of this ecosystem because he would have ignored the parasites.

There’d have been nothing unusual in that. For decades, ecologists have waded into bayous, paddled into lakes, and tramped through forests in order to look at two things: the competition for the necessities of life, such as food and water, and the struggle not to be eaten. They surveyed the density of plants and animals, their distribution from young to old, the diversity of species. They drew diagrams of food webs like tangled mobiles. But never did one of those strands lead to a parasite. Ecologists didn’t deny that parasites existed, but they thought of them as merely minor hitchhikers. Life could be understood as if it were disease-free. “A lot of ecologists don’t like to think about parasites,” says Lafferty. “Their vision of the organism stops at the exterior of it.”

Few ecologists had bothered to back up their indifference with any data. It didn’t matter to them that animals are typically overrun with several different species of parasites. On the other hand, parasitologists had been remiss as well. They had been ogling their parasites in laboratories, but they had no idea what effects they had in the real world.

It turns out that those effects can be huge. Only in the last decade, for instance, have marine biologists discovered that the oceans are swarming with viruses. They had known for a long time that viruses can infect just about any marine life form, from whales to bacteria. But they had thought that there simply weren’t many viruses, or that they were too fragile to cause much harm. In fact, viruses are rugged and abundant. Ten billion of them live in the average quart of surface sea water. Their favorite targets are bacteria and phytoplankton, since those are the most abundant hosts in the sea. They also serve as the bottom link in the ocean food chain, devoured by predatory bacteria and protozoa, which are in turn eaten by animals. Now marine biologists realize that this crucial link is very sick. As many as half the bacteria in the ocean are killed by viruses. When a bacterium dies, it bursts apart in a little organic shower. Other bacteria scoop up its remains, in many cases only to be burst open by another virus. A huge amount of the ocean’s biomass is stuck in this bacteria-virus-bacteria loop, and it can’t feed the rest of the marine food chain. If viruses were to vanish from the sea, it might become crowded with fish and whales.

On land, parasites are just as powerful ecologically. For decades, ecologists who worked on the Serengeti plains thought that the great herds of wildebeest and other grazing mammals there were controlled by two factors: the food that could support them and the predators that kept their population down. Yet, for most of this century it was actually a virus that was most powerful. Known as rinderpest, the disease came to Kenya and Tanzania when infected cattle were imported from the Horn of Africa around 1890. It jumped from the livestock to wildlife and dragged down the population of herbivores, as well as their predators, and kept them down for decades. Only when cattle began to be vaccinated in the 1960s did the mammals of the Serengeti rebound.

Parasites don’t even have to kill their hosts to have huge impacts. A parasite may cut down the competitive edge of a species so that it can’t drive out a competitor, making it possible for the two species to live side by side. Deer carry a nematode that causes them no harm, but when it gets inside moose, it crawls into their spines and makes them stumble around drunkenly before dying. Without that parasite, the deer wouldn’t be able to compete with the moose. And biologists such as Lafferty have shown that the way parasites manipulate their hosts can also have a big effect on the balance of nature.

Going into graduate school, Lafferty thought he had a pretty good idea of the ecology off the California coast, where he had scuba dived since high school (he paid his way through college by scraping mussels off oil rigs). It wasn’t until he took a course on parasitology that he had his mind changed. His teacher, Armand Kuris, stunned him by showing how parasites could be found everywhere in the sea. “Here are all these animals I knew and loved as a diver, and when you opened them up they were full of parasites. I realized marine ecology had been missing a big part of the picture.”

Lafferty began studying the parasites of the Carpinteria salt marsh. There are many to choose from at Carpinteria—a dozen flukes infect the California horn snail alone—but Lafferty chose the most common one, Euhaplorchis californiensis. Birds release Euhaplorchis eggs in their droppings, which are eaten by horn snails. The eggs hatch, and the flukes castrate the snail, producing a couple of generations before cercariae come swimming out of their host. The cercariae explore the salt marsh to find their next host, the California killifish. They latch onto its gills and work their way into its fine blood vessels; they crawl deeper into the fish, finding a nerve that they follow until they reach the brain. They don’t actually penetrate the killifish’s brain but form a thin carpet on top of it, looking like a layer of caviar. There the parasites wait for the fish to be eaten by a shorebird. When they reach its stomach, they then break out of the fish’s head and move into the bird’s gut, stealing its food from within and sowing eggs in its droppings to be spread into marshes and ponds.

Lafferty wanted to understand what effect this cycle had on the ecology of the salt marsh. Would Carpinteria look the same if there were no flukes? He began his ride around the parasite’s cycle at the snail stage. The relationship between fluke and snail is a strange one. It’s not a predator-and-prey arrangement. When a lynx kills snowshoe hares, the tender shoots that the dead hares would have eaten are eaten by the survivors, which can use the energy to raise baby hares. But the flukes of Carpinteria don’t quite kill their snails. In a genetic sense, the snails are indeed dead, because they can no longer reproduce. But they live on, grazing on algae to feed the flukes inside them. If the snails were truly dead, the algae that they ate would be left for surviving snails to graze on. Instead, the flukes-as-snails are in direct competition with the uninfected snails.

Lafferty set up an experiment to see how the competition played out. “What I’d do is make these cages that had mesh so that water could come in and out, but the snails couldn’t go through. The tops were open so the sun could shine through and algae could grow on the bottom. Then I’d bring the snails into the lab and find out who’s infected, who’s uninfected, and what size they were, and assign the snails to particular cages based on whether they were infected or what size they were. So the cages were all identical except for some factor that was altered. The cages were all located in an area the size of a desk, and that was replicated at eight different sites in the salt marsh.”

Lafferty measured how the uninfected snails performed without parasitized snails competing with them. They grew faster, released far more eggs, and could thrive in far more crowded conditions. The results showed Lafferty that in nature, the parasites were competing so intensely that the healthy snails couldn’t reproduce fast enough to take full advantage of the salt marsh. In fact, if you were to get rid of the fluke, the snail’s overall numbers would nearly double. And this being the real world rather than a lab, that explosion would ripple out through much of the salt marsh ecosystem, thinning out the carpet of algae and making it easier for the predators of snails, such as crabs, to thrive.

After Lafferty earned his Ph.D. in 1991, he continued working with Kuris. He began following the flukes from snails to fish. When Lafferty started working with the parasites, nothing was known about their effects on their killifish hosts. If he scooped up a seine’s worth of the fish and dissected them, he found most of them carrying parasites atop their brains. Once they got in, they didn’t seem to cause much harm to the fish—the fish didn’t even mount an immune response. And as I stood with Lafferty in the salt marsh, looking down at the channels, I certainly couldn’t say which killifish were parasitized and which were healthy.

But Lafferty suspected that the flukes might not be passive passengers. Like so many other parasites, they should be taking control of their fates. “Looking at these fish, I didn’t notice anything that struck me. But the more I became familiar with all this behavior modification stuff, it seemed like an obvious thing the parasites should be doing,” says Lafferty. “They’re in a good position to be doing something. Think about a simple molecule like Prozac. It’s simple for the flukes to secrete some neurotransmitter.”

Lafferty set his student Kimo Morris to establish whether or not the flukes affected the killifish. Lafferty gathered up forty-two fish, brought them into the lab, and dumped them into a seventy-five-gallon aquarium. Morris gazed at the fish for days. He would pick out one and stare at it for half an hour, recording every move it made. When he was done, he’d scoop the fish out and dissect it to see whether its brain was caked with parasites or not. And then he’d meditate on another killifish.

What was hidden to the naked eye came leaping out of the data. As killifish search for prey they alternate between hovering and darting around. But every now and then, Morris would spot a fish shimmying, jerking, flashing its belly as it swam on one side, or darting close to the surface. These might be risky things for a fish to do if a bird was scanning the water. And Morris’s vigil had revealed that fish with parasites inside them were four times more likely to shimmy, jerk, flash, and surface than their healthy counterparts. Since then, Lafferty has been working with a molecular biologist to figure out how the parasites make their hosts dance. They’ve found that the flukes can pump out powerful molecular signals, known as fibroblast growth factors, which can interfere with the growth of nerves. They could turn out to be the parasite’s Prozac.

Lafferty decided to see what effect this manipulation had on the salt marsh ecology. “Once we saw that the behavior was different, it was obvious that the field experiments had to follow,” he says. Lafferty wanted to see if what Morris might perceive as an unusual behavior could really translate into a better chance that a fish would be eaten by a bird—and not a bird stuck in a lab cage but one free to fly to another marsh if it was so inclined. He and Morris set up a series of pens that were both open to the sky and flush on one side with the shore, so that fish couldn’t escape, but birds could easily land in the pens or simply wade into them. They filled both pens with a mix of infected shimmying fish and healthy ones, and covered one with netting to protect it from birds.

For two days they watched the pens, not knowing whether birds would even bother with them. Then a great egret waded into the open pen, stepping slowly, as if in deep thought. It stared into the muddy water and then struck a few times, the last time bringing up a killifish.

After three weeks, Lafferty and Morris gathered the fish out of the pens. They brought them back into the lab to look inside their skulls. The results were even more stark than Morris’s fish-watching: the birds were not four times more likely to select one of the flailing, parasitized fish, but thirty times. Either their eye is far keener than Morris’s, or perhaps they are that much lazier.

But why would birds pick so many sick fish when they were virtually guaranteeing themselves an intestinal parasite? The flukes do take a toll on the birds, but a relatively small one. It’s in the parasite’s interest, after all, for the bird to be healthy enough to fly, so that it can carry the fluke to other salt marshes that it can colonize. If the bird scrupulously avoided infected killifish, it might stay healthy, but it would also go hungry. The parasites make so much food available to it that their benefits far outweigh their costs.

Armand Kuris was stunned by what his former student had found. “What blew me away was the conservative estimate that they increased the susceptibility to predation by thirty times. Thirty times. So now I step back, and I look at the birds flitting around out there and think: Could we have those birds out there if it were thirty times harder for them to get their food? It was that that made me go from thinking that behavior modification was just a great story to thinking that it’s really powerful—it may be running a large part of the waterbird ecology. Is there anything to birds other than this?”

This sort of power isn’t limited to a salt marsh on the California coast. Two thousand miles away from the Carpinteria salt marshes, ecologist Greta Aeby has been scuba diving along Hawaii’s coral reefs. Corals are actually colonies of animals, each a soft polyp lodged in a hard chalky scaffolding. The polyp can reach out into the seawater to filter out food or to spawn, but then it retracts back into the safety of its armor. A marine fluke called Podocotyloides stenometra begins its life inside clams that live around the reef; then it invades coral polyps for the next stage of its cycle. From there it needs to get into the intestines of the butterfly fish, which graze the corals. Butterfly fish have to put a lot of effort into nibbling at what little flesh of the polyps is exposed above their drab brown exoskeleton.

A parasite can’t make coral dance like killifish in order to get the attention of its next host. But Aeby has found that Podocotyloides manages to make some changes to the polyp that are just as effective. When the fluke gets inside the coral, the polyp swells up and changes from its normal brown to a bright pink. At the same time it grows a network of calcium carbonate spikes that keep it from retracting. As a result, the swollen brilliant polyp dangles out, making it an easy pick for a passing butterfly fish. In fact, when Aeby put butterfly fish into a tank with healthy and parasitized corals, 80 percent of their bites were directed to the sick coral. In half an hour one fish can swallow 340 flukes.

But Aeby has found that the alliances in her ecosystem are different from the ones that Lafferty has uncovered in salt marshes. When a killifish brings a fluke to a bird, the killifish dies in the process. But corals consist of colonies of clones and when an individual polyp infested with a fluke dies, it is replaced by a healthy new one. An infected polyp can’t feed or reproduce, so allowing a fluke to fester inside it is a drain on the colony, slowing its growth. If a butterfly fish prunes the coral, it can perform as well as a healthy coral. It’s to the coral’s advantage to get rid of its sick polyps, which may mean that the coral is actually contributing to the color or spikes in order to make it easier for the butterfly fish to spot. Lafferty found a case in which a parasite and its final bird host were allied; here, Aeby has found a case where the intermediate host and the parasite work together.

Discovering parasites at work in ecosystems can feel a bit like watching in terror as a bank robbery unfolds and then looking across the street and seeing a movie crew with its cameras and boom mikes. Birds are being guided to their meals, and fish are choosing their coral polyps, thanks to the advertisement of flukes. Uncovering these effects is hard work, and only a few examples have been documented. But they’re enough to suggest that parasites can cast some of the hoariest notions of ecology into doubt. We tend to think of predators as keeping a herd of prey healthy by weeding out the slowest ones. That’s not what’s happening in Lafferty’s salt marsh, or even among those icons of predator and prey, the wolf and the moose.

Wolves are the final hosts for one of the smallest tapeworms in the world, Echinococcus granulosus. Far from a ticker-tape ribbon, it’s lucky if it gets to be a quarter of an inch long as an adult. It doesn’t cause its final host much harm, but its eggs can be vastly vicious. They are eaten by herbivores such as moose, where they slowly transform themselves into cysts in which thirty individuals may sit. They will keep growing if there’s no bone in their way. When they accidentally end up in humans, they have been known to grow so big that they’ve contained fifteen quarts of fluid and millions of baby tapeworms.

One of the tapeworm’s favorite sites for forming its cyst is the lungs. A moose may carry several in its lungs, each tearing through its bronchial tubes and blood vessels. As a result, when wolves sweep down on a herd of moose, they’re more likely to pick out the slow, wheezing one and kill it. It’s even possible that these moose tapeworms can create the same kind of scent used by rat tapeworms to lure beetles. Instead of leaving the scent in droppings, though, the moose tapeworms could release their aroma with their host’s every breath. In any case, the result is that the tapeworm brings the wolf to the moose so that it can get into the wolf. The thinning of the herd is an illusion, not the service of the predator but the side effect of a tapeworm traveling through its life.

On my way to see Lafferty, I stopped one night in a hotel in Riverside, California. It had originally been a Spanish mission, and after unpacking, I prowled around the old shrines, explored the hidden passageways surrounded by vines and palms, crossed the hushed stone courtyard. I came back to my room feeling utterly alone. I turned on the television for company. An episode of The X-Files was on. As well as I could figure out, an FBI man had suddenly turned gloomy and wouldn’t return anyone’s phone calls. When another agent tracked him down and confronted him, the gloomy man threw him to the floor and brought his face close to his, opening his mouth. With wonderful creaking and slithering noises, a scorpionish creature crawled out of his throat and climbed into the other agent’s mouth.

I didn’t feel so lonely after that. Some television screenwriter had parasites on his mind as well. It occurred to me that parasites were the basis for a lot of science fiction novels, of movies and television shows. And I was struck by the fact that these parasites were dangerous because they could manipulate their hosts, just as parasites can in reality. When I got back home I started renting videos. I told my friends, and they’d tell me about other movies I should see, books to read. It got to be a gruesome marathon. The oldest entry I could find was Robert Heinlein’s The Puppetmasters, a 1955 novel. A spaceship full of aliens travels from Saturn’s moon Titan and lands near Kansas City. But the aliens inside aren’t the standard-issue 1950s hairless bipeds; they’re pulsating jellyfish-like creatures that latch onto people’s spines. Hiding underneath the clothes of their hosts, they tap into their brains and force them to help spread the parasites across the planet. The fight against them is a bit ludicrous, with the government forcing everyone to walk around practically naked to be sure they’re not carrying an alien. Humanity is saved when the army finally finds a virus that can kill the parasites, and the book closes with a fleet of spaceships leaving Earth for Titan to exterminate the parasites for good. It’s a stiff, peculiar book—the only one I’ve read that ends with the battle cry “Death and Destruction!”

The Puppetmasters was turned into a pretty mediocre movie in 1994, but its essence—the notion of humans harboring giant parasites—has become a Hollywood institution. Parasites are a part of our shared dramatic language, just as they were in Greek comedies. Any blockbuster can rest its plot on parasites without anyone’s worrying that it will seem too esoteric. One of the biggest movies of 1998, The Faculty, takes place in a high school where parasites from another planet are taking over the bodies and minds of teachers and students. These fluke-like things sprout tentacles and tendrils, and they pull themselves into their new hosts through their mouths or ears. Their hosts change from frazzled teachers and sulking, violent kids to glazed-eyed upstanding citizens who try to spread the parasite to new hosts. It’s up to the assorted losers of the school—drug dealers, geeks, and dropouts—to save the world from the invasion.

Parasites got their first big break at the movies almost twenty years earlier, in the 1979 movie Alien. A spaceship hauling ore stops off to investigate a crash on a lifeless planet. The crew discovers an alien ship that has been destroyed in a ruthless attack, and nearby they come across a clutch of eggs. One of the crew, a man named Kane, takes a close look at one of the eggs, and a giant crablike thing bursts out of it, clamping to his face and wrapping a tail around his neck. His crewmates bring him back to their ship, alive but comatose. When the ship’s doctor tries to get the thing off him, it tightens its tail around Kane’s neck. The next day it has disappeared, and Kane seems fine. He gets up and eats voraciously, to all appearances normal. Of course, no movie monster ever just disappears. This one has been devouring Kane’s guts, and before long he suddenly clutches his stomach, writhing and screaming, and a little knobby-headed alien pierces through his skin and leaps out. As the parasitic wasp is to the caterpillar, so this alien is to humans.

Alien may have made Hollywood safe for parasites, but a lot of the conceptual legwork had already been accomplished four years earlier in a low-budget, little-seen movie directed by David Cronenberg called Shivers. It is set on Starlight Island, an immaculate high-rise building on an island outside Montreal. “Sail through life in quiet and comfort,” says the soothing voice-over on a commercial for the building. But the isolated quiet and comfort is destroyed by an engineered parasite. It’s the work of one Dr. Hobbs. Dr. Hobbs originally set out to create parasites that could play the role of organ transplants. A parasite could be connected to a person’s circulatory system and filter blood like a kidney, for example, while taking only a little blood to keep itself alive. But Dr. Hobbs also has a secret agenda: he’s decided that man is an animal that thinks too much, and he wants to turn the world into one giant orgy. To that end he fashions a creature that will be a combined aphrodisiac and venereal disease: a parasite that will make its hosts sexually voracious and will be spread during sex.

He implants it in a young woman he has been having an affair with, a woman who lives on Starlight Island. She sleeps with some of the other men in the building and spreads the parasite. A stubby worm the size of a child’s foot, it lives in people’s guts and passes from mouth to mouth during a kiss. It transforms people into sexual monsters, attacking each other in apartments, laundry rooms, elevators. Rape, incest, and all sorts of other depravity erupt.

The physician for Starlight Island spends most of the movie trying to stop the parasite from spreading. At one point he has to shoot a man attacking his nurse (and girlfriend), and they escape to the basement. As they cower there, the nurse tells him that she had a dream the night before in which she was making love to an old man. The old man told her that everything is erotic, everything is sexual, “that disease is love of two alien kinds of creatures for each other.” Whereupon she tries to kiss the doctor, with a parasite crouched in her mouth ready to spring. He knocks her out cold. He tries to escape the building, but hordes of infected hosts ring him in and herd him into the building’s swimming pool. His nurse is there, and she finally gives him a fatal kiss. Later that night, all the residents drive out of the garage and leave the island, to spread the parasite and its mayhem throughout the city.

As I watched these movies, I was struck by how easy it was to translate biological reality into movie horror. The creature in Alien comes as no surprise to the entomologist who studies parasitic wasps. Heinlein may not have known that parasites can take over the behavior of their hosts, but he nailed the essence of their control. It may seem ridiculous that the parasites in Shivers can spread themselves by making people have sex, but it’s no more ridiculous than what actual parasites do. The fungus that I discussed earlier, which infects flies and forces them to climb up grass in the evening, actually uses a second trick to spread itself as well. It makes the corpse of its host a sexual magnet. Something about the fly—something brought about by the fungus itself—makes it irresistible to uninfected male flies. They will try to mate with it, preferring it to living flies. As they grope the corpse they become covered with spores themselves. When they die, they themselves become irresistible. When will someone make their movie?

Of course, these parasites are more than just parasites. In Shivers, Cronenberg uses them to expose the sexual tension buried under the blandness of modern life. In The Faculty, parasites represent the stupefying conformity of high school, which only outsiders can fight. And in The Puppetmasters, written in the McCarthyite fifties, the parasites are Communism: they hide within ordinary-seeming people, they spread silently across the United States, and they have to be destroyed by any means necessary. At one point the narrator says, “I wonder why the titans [the narrator’s name for the aliens] had not attacked Russia first; Stalinism seemed tailormade for them. On second thought, I wondered if they had. On third thought, I wondered what difference it would make; the people behind the Curtain had had their minds enslaved and parasites riding them for three generations.”

But all these works do have something in common: they play on a universal, deep-seated fear of parasites. This horror is new, and for that reason it’s interesting. There was a time when parasites were treated with contempt, when they stood for the undesirable, weak elements of society that got in the way of its progress. Now the parasites have gone from weak to strong, and now fear has replaced contempt. Psychiatrists actually recognize a condition they call delusional parasitosis—a terror of being attacked by parasites. The old parasite metaphors, the ones used by people like Hitler and Drummond, were remarkably precise in their biology. And, judging from movies like Alien and The Faculty, so is the new one. It is not just a fear of being killed; it’s a fear of being controlled from within by something other than our own minds, being used for something else’s ends. It’s a fear of becoming a flour beetle controlled by a tapeworm.

This precise horror of parasites has its roots in how we now see our relationship to the natural world. Before the nineteenth century, Western thought saw humans as distinct from the rest of life, created by God with a divine soul in the first week of Genesis. It became harder to keep that dividing line fixed as scientists compared our bodies with those of apes and found the differences to be pretty minor. And then Darwin explained why: humans and apes are related by common descent, as is all of life. The twentieth century has given his realization a fine-grained detail, moving from bones and organs down to cells and proteins. Our DNA is only a shade different from that of chimpanzees. And like a chimpanzee, or a turtle or a lamprey, we have brains that consist of crackling neurons and flowing neurotransmitters. These discoveries may give some comfort if you look at them one way: we belong on this planet as much as the oak and the coral reef, and we should learn to get along better with the rest of the family of life.

But look at them another way, and they bring horror. Copernicus took the Earth out of the center of the universe, and now we have to accept the fact that we live on a watery grain in an overwhelming void. Biologists like Darwin did a similar thing, taking humanity out of its privileged place in the living world—a biological Copernicanism. We still go through life pretending that we are exalted above other animals, but we know that we too are collections of cells that work together, kept harmonized not by an angel but by chemical signals. If an organism can control those signals—an organism like a parasite—then it can control us. Parasites look at us coldly—as food, or perhaps as a vehicle. When an alien bursts out of a movie actor’s chest, it bursts through our pretenses to be more than brilliant creatures. It is nature itself that is bursting through, and it terrifies us.