Dicrocoelium Dendriticum, the Liver Fluke

NEW EVIDENCE INDICATES OUR IDEA OF HOW NATURE REALLY WORKS COULD BE WRONG

ON A CLEAR SUMMER DAY ON THE CALIFORNIA COAST, THE CARPINTERIA salt marsh vibrates with life. Along the banks of the 120-acre preserve, 80 miles northwest of Los Angeles, thousands of horn snails, their conical shells looking like miniature party hats, graze the algae. Arrow gobies slip through the water, while killifish dart around, every now and then turning to expose the brilliant glint of their bellies. Fiddler crabs slowly crawl out of fist-size holes and salute the new day with their giant claws, while their bigger cousins--lined-shore crabs--crack open snails as if they were walnuts. Meanwhile, a carnival of birds--Caspian terns, willet, plover, yellowleg sandpipers, curlews, and dowitchers--feast on littleneck clams and other prey burrowed in the marsh bottom.

Standing on a promontory, Kevin Lafferty, a marine biologist at the University of California at Santa Barbara, watches the teeming scene and sees another, more compelling drama. For him, the real drama of the marsh lies beneath the surface in the life of its invisible inhabitants: the parasites. A curlew grabs a clam from its hole. "Just got infected," Lafferty says. He looks at the bank of snails. "More than 40 percent of these snails are infected," he pronounces. "They're really just parasites in disguise." He points to the snowy constellation of bird droppings along the bank. "There are boxcars of parasite biomass here; those are just packages of fluke eggs."

Every living thing has at least one parasite that lives inside or on it, and many, including humans, have far more. Leopard frogs may harbor a dozen species of parasites, including nematodes in their ears, filarial worms in their veins, and flukes in their kidneys, bladders, and intestines. One species of Mexican parrot carries 30 different species of mites on its feathers alone. Often the parasites themselves have parasites, and some of those parasites have parasites of their own. Scientists have no idea of the exact number of species of parasites, but they do know one fact: Parasites make up the majority of species on Earth. Parasites can take the form of animals, including insects, flatworms, and crustaceans, as well as protozoa, fungi, plants, and viruses and bacteria. By one estimate, parasites may outnumber free-living species four to one. Indeed, the study of life is, for the most part, parasitology.

Most of the past century's research on parasites has gone into trying to fight the ones that cause devastating illness in humans, such as malaria, AIDS, and tuberculosis. But otherwise, parasites have largely been neglected. Scientists have treated them with indifference, even contempt, viewing them as essentially hitchhikers on life's road. But recent research reveals that parasites are remarkably sophisticated and tenacious and may be as important to ecosystems as the predators at the top of the food chain. Some castrate their hosts and take over their minds. Others completely shut down the immune systems of their hosts. Some scientists now think parasites have been a dominant force, perhaps the dominant force, in the evolution of life.

SACCULINA CARCINI, A BARNACLE THAT MORPHS INTO PLANTLIKE ROOTS, is not the kind of organism that commands immediate respect. Indeed, at first glance Sacculina appears to slide down the ladder of evolution during its brief lifetime. Biologists are just beginning to realize that this backward-looking creature is a powerhouse in disguise.

Sacculina starts life as a free-swimming larva. Through a microscope, the tiny crustacean looks like a teardrop equipped with fluttering legs and a pair of dark eyespots. Nineteenth-century biologists thought Sacculina was a hermaphrodite, but in fact it comes in two sexes. The female larva is the first to colonize its host, the crab. Sense organs on the female Sacculina's legs catch the scent of a crab, and she dances 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--until 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 squirts a blob made up of a few cells. The injection, which takes only a few seconds, is a variation on the molting that crustaceans and insects go through in order to grow. For example, a cicada sitting in a tree separates a thin outer husk from the rest of its body and then pushes its way out of the shell, emerging with a new, soft exoskeleton that stretches throughout the insect's 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 like a microscopic slug.

The slug 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 a set of rootlike tendrils, which spread throughout the crab's body, even wrapping around its eyestalks. Covered with fine, fleshy fingers much like the ones lining the human intestine, these roots draw in nutrients dissolved in the crab's blood. Remarkably, this gross invasion fails to trigger any immune response in the crab, which continues to wander through the surf, eating clams and mussels.

Meanwhile, the female Sacculina continues to grow, and the bulge in the crab's underside turns into a knob. As the crab scuttles around, the knob's outer layer slowly chips away, revealing a portal. Sacculina will remain at this stage for the rest of her life, unless a male larva lands on the crab and finds the knob's pin-size opening. It's too small for him to fit into, and so, like the female before him, he molts off most of himself, injecting the vestige into the hole. This male cargo--a spiny, reddish-brown torpedo 1/100,000 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 10 hours ends up at the bottom of the canal. There he fuses to the female's visceral sac 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.

Eventually, 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 molting 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 new generations, parasitized crabs simply go on eating and eating. They have been spayed by the parasite.

Despite having been 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, then 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 sits exactly where the crab's brood pouch would be, and the crab treats the parasite knob as such. 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 spray out from her body, she waves her claws to help them on their way. Male crabs succumb to Sacculina's powers as well. Males normally develop a narrow abdomen, but infected males grow abdomens as wide as those of females, wide enough to accommodate a brood pouch or a Sacculina knob. A male crab even acts as if he had a female's brood pouch, grooming it as the parasite larvae grow and bobbing in the waves to release them.

SACCULINA'S ADAPTATIONS REFLECT A RELATIVELY SIMPLE LIFE CYCLE for a parasite--it makes its way from one crab to another. But for many other parasites, the game is more complicated--they must journey through a series of animal species in order to survive and procreate. Such parasites exert extraordinary control over their hosts, transforming them into seemingly different creatures. They can change a host's looks or scent to appeal to a predator. They can even alter its behavior to force it into the next host's path.