Do Parasites Rule the World?
Author: Carl Zimmer
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
Standing on a promontory, Kevin Lafferty, a marine biologist at the
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.
The mature lancet fluke, Dicrocoelium dendriticum, nestles in cows and other grazers, which spread
the fluke's eggs in their manure. Hungry snails swallow the eggs, which hatch
in their intestines. The immature parasites drill through the wall of a snail's
gut and settle in the digestive gland. There the flukes produce offspring,
which make their way to the surface of the snail's body. The snail tries to
defend itself by walling the parasites off in balls of slime, which it then
coughs up and leaves behind in the grass.
Along comes an ant, which swallows a slime ball loaded with hundreds of lancet
flukes. The parasites slide down into the ant's gut and then wander for a
while through its body, eventually moving to the cluster of nerves that control
the ant's mandibles. 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 the flukes do some parasitic voodoo on their hosts. As the evening approaches
and the air cools, the ants find themselves drawn away from their fellows
on the ground and upward to the top of a blade of grass. Clamped to the tip
of the blade, the infected ant waits to be devoured by a cow or some other
grazer passing by.
If the ant sits the whole night without being eaten and the sun rises, the
flukes let 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 parasites would die with
it. When evening comes again, they send the ant back up a blade of grass for
another try. After the ant finally tumbles into a cow's stomach, the flukes
burst out and make their way to the cow's liver, where they will live out
their lives as adults.
AS SCIENTISTS DISCOVER MORE AND MORE PARASITES AND UNCOVER the extent and
complexity of their machinations, they are fast coming to an unsettling conclusion:
Far from simply being along for the ride, parasites may be one of nature's
most powerful driving forces.
At the Carpinteria salt marsh, Kevin Lafferty has
been exploring how parasites may shape an entire region's ecology. In a series
of exacting experiments, he has found that a single species of fluke--Euhaplorchis californiensis--journeys
through three hosts and plays a critical role in orchestrating the marsh's
balance of nature.
Birds release the fluke's eggs in their droppings, which are eaten by horn
snails. The eggs hatch, and the resulting flukes castrate the snail and produce
offspring, which come swimming out of their host and begin exploring the marsh
for their next host, the
In his research, Lafferty set out to answer one main question: Would Carpinteria look me same if there
were no flukes? He began by examining the snail stage of the cycle. The relationship
between fluke and snail is not like the one between predator and prey. In
a genetic sense, infected snails are dead, because they can no longer reproduce.
But they live on, grazing on algae to feed the flukes inside them. That puts
them in direct competition with the marsh's uninfected snails.
To see how the contest plays out, Lafferty put healthy and fluke-infested
snails in separate mesh cages at sites around the marsh. "The tops were
open so the sun could shine through and algae could grow on the bottom,"
says Lafferty. What he found was that the uninfected snails grew faster, released
far more eggs, and could thrive in far more crowded conditions. The implication:
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 flukes were absent from the marsh, the snail population would nearly
double. That explosion would ripple out through much of the salt marsh ecosystem,
thinning out the carpet of algae and making it easier for the snails' predators,
such as crabs, to thrive.
Lafferty then studied the killifish. Initially, he found little evidence that
flukes harmed or changed the fish they colonized; the fish didn't even mount
an immune response. But Lafferty was suspicious. He figured that flukes sitting
on the brain were in a good position to be doing something. So he plucked
42 fish from the marsh, dumped them into a 75-gallon aquarium in the lab,
and gave his student Kimo Morris the laborious task
of watching them. Morris would pick out one fish 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. Then
he'd focus 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--all risky things
for a fish to do if a bird is scanning the water. It turns out that fish with
parasites were four times more likely to shimmy, jerk, flash, and surface
than their healthy counterparts.
Lafferty and Morris followed up with a marsh experiment in which they set
up two pens, each filled with 53 uninfected killifish and 95 infected fish.
To distinguish between the two groups, the researchers clipped the left pectoral
fin of the healthy fish and the right fin of the parasitized ones. One pen
was covered with netting to protect it from birds; the other was left open
so birds could easily wade or land inside. After two days, a great egret waded
into the open pen. It stepped slowly into the muddy water and struck it a
few times, the last time bringing up a killifish. After birds had visited
the pen for three weeks, Lafferty and Morris added up how many fish were alive.
(The covered pen acted as a control for the researchers to see how many fish
died of natural causes.) The results were startling: The birds were 30 times
more likely to feast on one of the flailing, parasitized fish than on a healthy
fish.
Predators are often very careful about the prey they eat, avoiding poisonous
insects and frogs, for example. So why would birds pick so many fish that
are guaranteed to pass on an energy-sucking intestinal parasite? The flukes
do drain a bit of energy from the birds. But that is more than offset by the
benefit they provide: They make finding food very easy for the birds.
Scientists have been stunned by the implications of these findings. The birds
that frequent coastal wetlands depend on fish for much of their diet. Without
parasites throwing prey their way, the birds of Carpinteria
might have to put far more time and effort into eating and might reproduce
at a lower rate. "Could we have so many birds out there if it were 30
times harder for them to get their food?" asks marine biologist Armand
Kuris, also of the
The fluke that Lafferty studied is but one parasite, living in one salt marsh.
There are a dozen other species of fluke that live in the snails of Carpinteria and other parasites that dwell in other animals
of the marsh. Every ecosystem on Earth is just as rife with parasites that
can exert extraordinary control over their hosts, riddling them with disease,
castrating them, or transforming their natural behavior. Scientists like Lafferty
are only just beginning to discover exactly how powerful these hidden inhabitants
can be, but their research is pointing to a remarkable possibility: Parasites
may rule the world.
The notion that tiny creatures we've largely taken for granted are such a
dominant force is immensely disturbing. Even after Copernicus took Earth out
of the center of the universe and Darwin took humans out of the center of
the living world, we still go through life pretending that we are exalted
above other animals. Yet we know that we, too, are collections of cells that
work together, kept harmonized by chemical signals. If an organism can control
those signals--an organism like a parasite--then it can control us. And therein
lies the peculiar and precise horror of parasites.