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.