A famous biologist once called nature an evolutionary play set in an
ecological theatre. If so, most ecologists in the audience have always regarded
parasites as mere bit players that wander the fringes of the stage mouthing
trivial lines. Researchers trying to understand the broad outlines of the
plot or its setting have usually simply ignored parasites – and conversely,
most parasitologists have paid little attention to their subject’s role
in the larger show.
But that state of affairs is changing rapidly. Evolutionary ecologists
and behaviourists are beginning to realise that parasites, for all their
inconspicuousness, influence the workings of nature much more profoundly
than most people suspected. Research into animal behaviour has produced
some of the biggest surprises. Animal movement patterns, social behaviours
and even choice of mate may all reflect the bitter biological struggles
that take place between parasites and their hosts.
Parasites can have broad ecological effects as well. Like diminutive
deities, parasites can determine what species of tree live in a forest,
what kinds of maggots seethe in decaying mushrooms and whether hunters will
find many grouse this year. Parasites may foil conservationists’ efforts
to save endangered species, just as they so often hinder farmers raising
crops. Some biologists even suggest that parasites may be the reason organisms
bother to reproduce sexually.
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At this early stage, researchers have far more questions than answers,
but the excitement level is high. Last summer, major scientific meetings
of animal behaviourists and mammal experts featured symposia on the role
of parasites. Next August bird biologists will take their turn at the International
Ornithological Congress in Vienna. ‘It’s the new renaissance of parasitism,’
says parasite biologist Jenella Loye of the University of California at
Davis.
As part of that rebirth, ecologists are broadening their understanding
of the term ‘parasite’ to encompass all organisms that use other living
things as both habitat and food source. So parasites would include not
just the usual tapeworms, fleas and protozoans, but also the bacteria,
fungi and viruses that cause disease. Indeed, even the caterpillars that
nibble cabbage leaves are, from an ecological perspective, parasites. ‘Suddenly,’
says Douglas Gill of the Uni-versity of Maryland, ‘all the insect ecologists
are really parasitologists, and (parasites’) importance becomes rather major.’
Researchers offer several reasons for ecologists’ many decades of near-total
neglect of parasites. To begin with, parasites are not glamorous organisms.
‘Ecologists grow up wanting to study bright, showy birds. They’re kind of
disgusted by intestinal worms,’ says John Jaenike of the University of Rochester,
New York, only semi-facetiously. Parasites are also less conspicuous and
harder to study than most free-living organisms. And until recently ecologists
haven’t really learned how to think about parasitism, Jaenike says. Most
ecology textbooks that are more than a few years old skip over parasitism
in a few pages or omit it altogether.
So ecologists have usually overlooked parasites in the ecosystems they
study, says Janice Moore, a parasite ecologist at Colorado State University.
‘Avian ecologists, (for example) tend to know something about the plants
and a lot of the animals in the area. But they don’t know about any of the
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Over the past few years, however, this has slowly started to change
as ecologists have opened their eyes to parasites and parasitologists have
become more savvy about ecology. Many of today’s parasite ecologists trace
this shift’s origin to two oft-cited contributions from the late 1970s and
early 1980s: a series of mathematical analyses of infectious disease published
by Robert May and Roy Anderson, both now at the University of Oxford, and
a 1980 book, The Evolutionary Biology of Parasites, by Peter Price of Northern
Arizona University in Flagstaff. The interest sparked by these books slowly
kindled and now appears to be catching fire as researchers seek a new understanding
of how parasites figure in the lives of their hosts.
Sometimes, parasites guide their host’s behaviour – a subject Moore
has spent her career studying. Usually, the parasites do this to improve
their slim odds of finding a new host and continuing their life cycle. One
of the most dramatic examples, described by German researchers nearly 30
years ago, involves the parasitic fluke Dicrocoelium dendriticum. The fluke
spends the early part of its life in an ant but must somehow find its way
into the liver of a sheep to reach sexual maturity. To make this difficult
journey easier, Dicrocoelium simply hijacks the ant. A fluke burrows into
the ant’s nervous system, causing the hapless host to climb to the top of
a grass blade, hold tight with its mandibles, and wait for a grazing sheep
to wander by and eat both grass and ant, completing the transfer.
More recently, Moore studied a spiny-headed worm, or acanthocephalan
(Plagiorhynchus cylin-draceus) that parasitises isopod crustaceans, or pill
bugs (Armadillidium vulgare). Infected pill bugs leave their hiding places
and wander in the open where they are easy prey for starlings, the next
host in the parasite’s life cycle. Apart from its foolhardy behaviour, the
isopod shows no outward sign that it is really, in Moore’s words, ‘a parasite
dressed up to look like an isopod.’ Such trickery may be far more common
than most biologists realise, Moore says, since it is difficult to spot
without detailed study.
Pest-ridden slums
But hosts can strike back at the invaders with behavioural weapons of
their own. Grasshoppers (Melanoplus sanguinipes) infected with a protozoan
parasite (Nosema acridophagus), for example, bask in the sun to raise their
body temperature, and this ‘behavioural fever’ helps them fight the parasite
infection. Several other insects appear to use the same strategy. ‘It’s
possible in the right circumstances for the host to cook (its parasites),’
says Moore.
The best defence against parasites, though, is to avoid them entirely,
and many hosts have evolved behaviours that try do just that. Animals groom
and preen – often for long periods of time, as any cat owner will attest
– to keep themselves free of ectoparasites such as fleas. For similar reasons,
cliff swallows (Hirundo pyrrhonata) build several nesting colonies and alternate
between them, rarely nesting in the same place for two years in succession.
This shifting tenancy helps the birds to avoid the bloodsucking fleas, ticks,
and bugs that rapidly turn colonies into pest-ridden slums, according to
a study Loye conducted in Oklahoma. The only nest sites the swallows used
in consecutive years were those under concrete bridges. Here they did not
need to move because bridges have fewer crevices in which parasites can
hide, and consequently fewer parasites.
Loye speculates that the desire to avoid parasites may explain fastidiousness
in humans. ‘Why are we repulsed by faeces?’ she asks. ‘Why do we get so
upset when our dogs eat cat faeces? Why do we like to sleep in clean sheets?
These are all parasite questions.’ On a more serious note, several behaviourists
point out that the threat of HIV and other sexually-transmitted pathogens
(parasites in the broad sense) has prompted some sharp changes in sexual
behaviour in recent years.
Even the gaudy plumage and elaborate courtship behaviour of breeding
male birds may have more to do with parasites than with aesthetics. In 1982,
evolutionary biologists Bill Hamilton (now at the University of Oxford)
and Marlene Zuk (now at the University of California at Riverside) proposed
that males with showy feathers and vigorous courtship rituals, such as the
red jungle fowl (Gallus gallus) may be advertising their freedom from parasites.
Ailing, worm-ridden males, the argument went, wouldn’t be able to spare
the energy for such a costly display. It followed that females should evolve
to choose the showy males because their parasite-resistant genes would produce
fitter offspring. Several studies since then have strengthened Hamilton
and Zuk’s hypothesis, although it remains controversial – like many evolutionary
scenarios that can’t be tested directly in the laboratory.
Another of Hamilton’s ideas is more controversial still. Sex itself,
he suggests, may have evolved because it reshuffles genes, thus helping
animals to resist parasites. There is some remarkable support for this theory.
A species of snail in New Zealand reproduces sexually in habitats where
it is heavily parasitised, but asexually where parasites are scarce, according
to a study by Curtis Lively of Indiana University in Bloomington. However,
explaining the origins of sex is something of a cottage industry among evolutionary
biologists. Competing theories abound, and Hamilton has by no means convinced
everyone.
Devastated rabbits
Parasites can also play a striking role in the ecology of their hosts,
particularly in controlling population sizes. In a few cases, the parasite
– usually a disease organism – has a devastating effect. The myxoma virus,
for example, brought to Australia in the 1950s to control introduced rabbit
populations, killed 99.8 per cent of infected rabbits in its first epidemic.
Chestnut blight, a fungus introduced from Asia in 1904, has all but eradicated
the once-dominant American chestnut from eastern North America.
Most parasites aren’t so histrionic in their effects, but they can still
influence their hosts in important ways. On the moors of northern England,
for example, red grouse suffer from a nematode gut parasite. Wormy grouse
lay fewer eggs, rear fewer chicks and may be easier for predators to catch,
according to research by Peter Hudson of the Game Conservancy, Andrew Dobson
of Princeton University and their colleagues. Dobson and Hudson’s calculations
suggest that the worms reduce their hosts’ birth rate enough to cause a
sharp decline in grouse numbers, followed by a decrease in worm populations
as their hosts become less common. This interplay between the grouse and
their worms may account for the regular, four to five year cycles in grouse
abundance that are characteristic of northern England and Scotland.
Far from this sophisticated world of English country estates with their
red grouse and shooting parties, parasites also play a crucial behind-the-scenes
role in another ecosystem: maggoty mushrooms. In the northeast of the US,
the maggots of two species of fruit fly, Drosophila putrida and D. falleni,
share their humble home almost equally. Further south, D. putrida remains
abundant, while D. falleni fades away into rarity.
According to Jaenike a crucial factor is a nematode parasite in the
northern region that infects flies of both species. The nematode causes
greater harm to D. putrida, the stronger competitor of the two flies. This
handicap equalises the flies’ struggle for dominance in the mushroom. Hot
weather keeps the nematode from surviving south of North Carolina, however,
and without its handicap D. putrida easily dominates its mushroom milieu.
So far, well-documented examples such as these are like a few daubs
of paint on an otherwise blank canvas. For most species and most ecosystems,
experts have little idea whether parasites are ecologically important, because
no one has looked. Indeed, parasitologists have a hard enough time answering
a simpler question – whether or not specific parasites significantly harm
their individual hosts. ‘The number of cases for which we have actually
documented pathological effects is pretty small,’ notes Daniel Brooks of
the University of Toronto.
Brutish world
This information is hard to come by, says Brooks, because parasites
make difficult experimental subjects. Many have intricate life cycles involving
several host species, which makes them nearly impossible to maintain in
the laboratory. And even when such experiments are possible their results
may not mean much in the real world, since pampered lab animals with plenty
of food and no predators can usually tolerate parasites much better than
their counterparts out in the nasty, brutish world. Jaenike’s flies, for
example, suffered much less harm from their nematode parasites in the laboratory.
In natural environments, experimenters face a different set of problems.
Host individuals often carry several kinds of parasites at once, or none
at all; weather conditions vary; predators and competitors come and go.
‘Out there in the real world, everything’s all mixed up and there are no
controls,’ Brooks says. ‘That sort of thing drives an experimental biologist
crazy.’ Under such conditions, ecologists have a difficult time proving
that any particular parasite has much effect.
And there is another complication, says Jaenike: not every ecosystem
shaped by parasites is teeming with parasites today. A naive visitor to
the forests of eastern North America today, for example, would see little
to suggest the enormous impact of chestnut blight fungus decades ago.
Only by looking back at the historical record could the visitor realise
that today’s chestnutless forest is haunted by the Ghost of Parasitism Past.
Given all these obstacles, it is hardly surprising that ecologists have
large gaps in their understanding of parasites’ ecological role. Nevertheless,
in the few studies that have looked carefully for evidence, parasites have
usually displayed important ecological effects. Many researchers have concluded
that these examples could well be the tip of the iceberg. ‘I’m increasingly
persuaded that parasites are a key mortality factor and a key explanation
of the abundance and distribution of a number of large mammals,’ says Gill.
As field biologists begin to make more space for parasites in their
view of how the world works, theoretical biologists are also rethinking
their sense of parasites’ importance. Until recently, most parasitologists
and many other biologists believed that over time, parasites and their hosts
always evolved a kind of truce in which the parasites become more benign
and the hosts become more tolerant of them. Since parasites get both food
and shelter from their host, any parasite virulent enough to kill its host
would, they reasoned, be committing suicide by destroying its own habitat.
So natural selection should favour parasites that go easy on their hosts.
Over the past ten years or so, however, evolutionary biologists have
largely discarded this scenario in favour of a more complex one. Often,
virulent parasites harm the host because they are furiously churning out
offspring. Such parasites may be unable to treat their host more gently
without paying a price in fewer offspring. There is no single best solution
to this trade-off between reproductive rate and longevity, say Theoreticians.
Through natural selection, each parasite species must seek its own evolutionary
nirvana, finding the right balance for its particular ecological setting.
Cry freedom
As parasites begin to loom larger in ecologists’ thinking about the
natural world, some experts now suggest they may be equally important in
applied ecology and conservation biology. For example, says Dobson, many
introduced weeds and animal pests such as rats, cats and goats have few
parasites in their adopted lands. This freedom from parasites may be one
reason for their success. If so, he speculates, introducing carefully chosen
parasites may prove to be a highly effective form of biological control.
On the other hand, parasites may make it harder to preserve rare and
endangered species. On their own, most endangered species are probably too
rare to support a serious parasite outbreak. But if parasites are picked
up from nearby species (usually more common relatives), the parasites might
finish off the rare species. In Hawaii, for example, a malarial parasite
that infects birds has spread from introduced songbirds into native bird
species such as the honeycreepers Vestaria coccinea and Himatione sanguinea,
where it has caused widespread death. As a result, many native birds have
become virtually extinct at low elevations where malaria-carrying mosquitoes
live.
Environmental scientists trying to predict the impact of global warming
should also take note of parasites, Dobson says. Laboratory studies show
that changes in temperature and humidity often alter a parasite’s ability
to infect new host individuals. Global warming – and the changes in rainfall
patterns that accompany it – could therefore shift parasites and diseases
to new regions of the world.
If so, the chaos (or lack of it) that this causes may give ecologists
their best handle yet on whether parasites are mostly spear carriers on
the ecological stage, or whether instead they take a starring role.
Bob Holmes is a freelance science writer based in California.