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.