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The
Trouble with Frogs
When
deformed frogs started hopping out of this country's wetlands during
the last decade, scientists and the public alike took notice. biologist
David Skelly thinks he knows why the deformities occurred -- and
what they have to say about human health.
October
2002
by Bruce Fellman
At first
glance, the Ward Marsh wildlife management area on the western border
of Vermont is the epitome of nature at its most pristine.
Surrounding the wetland is a grassy meadow through which deer and
wild turkeys roam, and guarding it is a rugged cliff that shelters
the Green Mountain State's last remaining population of rattlesnakes.
The marsh's sparkling waters are rich with cattails, dragonflies,
catfish, and birds, and this calm backwater of the Poultney River
just might be amphibian heaven.
But in 1997, there
was serious trouble in paradise. For when the resident leopard frogs
began making the age-old transition from tadpole to adult, nearly
half of the creatures emerged missing limbs, eyes, or other body
parts.
The scene was unnerving,
and it was repeated throughout the state. Since these animals spend
so much of their early lives in close contact with the water, they're
often seen as the equivalent of the canaries that miners once carried
to warn them of impending doom. Amphibians unable to hop in a straight
line were surely a warning sign -- but of what?
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"We
all know that the environment is under a well-documented
assault."
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Last summer, ecologist
David Skelly, an associate professor at the School of Forestry and
Environmental Studies (FES), waded into Ward Marsh and other sites
in Vermont as part of an ambitious effort to solve what remains
a scientific mystery. Although there are many theories, no one knows
precisely why the frogs suddenly failed to develop normally -- or
why the "hot spots" where deformities were prevalent tended, like
fireflies in a meadow, to wink on and off.
"The key is to figure
out why it happened then, and why it isn't happening now," says
Skelly, a scientific detective on the trail of an old crime. "If
we can understand what caused the abnormalities, maybe we can determine
how to prevent them in the future."
Armed with a $2.1 million,
five-year grant from the National Institutes of Health (NIH) and
the National Science Foundation (NSF), Skelly and Joseph Kiesecker,
a former postdoctoral researcher at Yale and now an assistant professor
at Penn State, are midway through a massive study aimed at discovering
what can turn batrachian heaven into frog hell in Vermont and, it
turns out, elsewhere. In the mid-1990s, observers in Minnesota spotted
frogs that had developed too many legs and since then, deformed
amphibians have been discovered in 44 states and 4 Canadian provinces.
For
scientists hoping to find a single cause for the problem, nothing
has seemed to add up. "The more I looked, the more I realized
that there wasn't going to be a magic bullet," says Skelly. "The
patterns we're seeing don't fit any one explanation. More likely,
the cause will be a complex interaction among several factors."
Rick Levey, a Vermont
department of environmental conservation aquatic biologist who has
monitored the deformities since the first reports started arriving,
agrees. "When you examine everything that might be involved, it
begins to read like a Chinese restaurant menu: one from column A,
one from column B, and so forth," says Levey. "I'm still hoping
that the bulk of the abnormalities will be chalked up to fluctuations
in natural conditions, but we all know that the environment is under
a well-documented assault."
Skelly and Kiesecker
proposed looking at how the perfectly normal changes in nature and
a multitude of human-caused insults to the natural world might come
together to wreak havoc among frogs. This approach appealed to the
NIH and the NSF. Two years ago, the federal agencies inaugurated
a joint research program called "The Ecology of Infectious Diseases,"
and the Skelly-Kiesecker proposal was among the first funded by
the initiative. Deformed amphibians, the NIH and NSF felt, might
have something profound to say about our own health.
"We're
trying to understand how human modifications of the natural world
can influence the patterns of disease we see in frogs as well as
in our own species," says Skelly.
Amphibians seem to be
an ideal model system for testing theories that could explain the emergence of new ailments, such as West Nile fever and Lyme disease,
and the reappearance of old scourges, tuberculosis among them. "We
can do experiments in the lab and in the field and modify the frogs'
natural environment in ways we could never do with humans," the ecologist continues. "Then, we can see if these changes alter an
animal's ability to cope with infection and if they have longer-term
consequences for the population. We can also determine if there
are ways in which we can minimize our impact."
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"The tadpoles in the mesocosm grew way beyond anything in
the natural world. I called them Frankentadpoles."
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It is a tall order,
and to ferret out answers, Skelly and his research crew -- Susan
Bolden, Nicole Freidenfelds, and Nancy Cothran, an FES master's
degree student -- have spent much of the past year slogging through
a wide variety of Vermont wetlands. Some of the ponds, marshes,
and swamps under study are located in the relatively urban area
of Burlington, while others are in the neighborhood of farm fields
or hidden in undeveloped mountain hollows. The research followed
a similar tack in Connecticut in 2001, surveying wetlands along
an urban-to-rural gradient from city parks in Manchester to the
relatively untouched woodlands of the Yale-Myers Forest in the northeastern
part of the state. (Kiesecker and his colleagues are conducting
comparable investigations in Pennsylania and upstate New York.)
In Vermont, the Skelly
team routinely monitored some 40 sites, each of which is within
the Lake Champlain watershed in the western part of the state. The
study area began at Ward Marsh in the south and continued almost
200 miles north to the Canadian border, and the researchers gave
special attention to four spots. These were among the sites that
had been monitored since 1996 by Rick Levey, so there was already
plenty of data that Skelly could use to determine what effect, if
any, his experiments might have on the deformity situation.
Since the first reports
surfaced almost ten years ago, scientists have attributed the abnormalities
to a variety of factors. Among the favorites are parasites, pollutants,
changes in ultraviolet light, shifts in the weather due to the El
Nino phenomenon, amphibian overcrowding, even an increase in the
number of amateur naturalists. (In response to the news, many conservation
organizations enlisted corps of citizen observers; perhaps they
were seeing a phenomenon that had always been present but that,
for lack of human eyes, had been overlooked.) But while a "one size
fits all" explanation might be desirable -- if for no other reason
than a single cause could suggest a single solution -- Skelly's
lengthy experience in wetlands suggested that nature isn't likely
to be so accommodating.
For most of his career,
the scientist has concentrated on the ecology of "temporary" ponds
-- "mudholes" that teem with life for part of the year and then
dry to a dusty memory. "These are small, complete worlds," says
Skelly. "I work in places in which I can walk around the entire ecosystem and characterize it, and then sample the universe of nearby
ponds, compare them, and experience first hand how dynamic these
habitats are."
Skelly
began this pursuit early. "I had the great fortune to grow up in
a swamp," he explains. Raised in Wilton, Connecticut, then
a largely undeveloped town in northern Fairfield County, the scientist
recalls rearing frog eggs, culled from nearby wetlands, in styrofoam-lined
milk coolers when he was 6 years old. His first love, however, was
fishing, and after completing a bachelor's degree at Middlebury
College in 1987, he went to the University of Michigan with the
intention of studying fish. But ecologist Earl Werner, his mentor
at graduate school (and, since that time, a frequent collaborator),
had begun to study amphibians. Skelly was quickly hooked on frogs,
toads, salamanders, and the like.
As Skelly's career
progressed, ecology was making a transition from a descriptive science,
in which practitioners spent years outdoors observing aspects of
the natural world, to an experimental endeavor where nature could
be mimicked in the laboratory. Among freshwater ecologists, the
cattle watering tank, a fixture on dairy farms and ranching operations,
became the set-up of choice, and in these tubs -- researchers also
used kiddie wading pools and plastic sweater boxes -- scientists
would put a standard "recipe" of water, nutrients, amphibians, and
other aquatic life. By carefully measuring what happened to each
component of these ersatz ponds, ecologists attempted to zero in
on the fundamental principles, particularly the roles of predation
and competition, that drove the ecosystem and determined winners
and losers.
The results might have
been statistically rigorous, but the more Skelly worked with cattle
tanks and other "mesocosms," the more he felt they weren't providing
an adequate proxy for nature. "The tadpoles in the tanks were growing
superfast and getting enormous -- way beyond anything I'd ever seen
in the natural world," he says. "I called them 'Frankentadpoles.'"
Something was missing
in the mesocosm, the underappreciated but critically important factors
of disease and parasites. "We were raising tadpoles in what amounted
to little quarantine wards," says Skelly. "But we've learned that
a wild tadpole, however healthy it looks, is usually infected with
something that makes it grow slower. This is entirely normal, and
we believe that infection and disease play an important, though
overlooked, role in population regulation and in how communities
are structured."
And
in why frogs developed abnormal limbs.
Skelly has developed
an experimental approach which, he believes, provides a more realistic
look at the basic workings of the natural world than can be seen
in mesocosms. While he still uses tanks and wading pools, the ecologist
does much of his work in the wetlands themselves. In Vermont, for example, the intensive research at the four sites involves raising
tadpoles in special cages designed to help the scientists understand
the importance of parasites in causing deformities.
In laboratory studies,
biologists have shown that infection by trematodes, a group of parasites
known to cause such human diseases as schistosomiasis, can result
in the abnormal limbs found in frogs. And in a landmark paper published earlier this year, investigators demonstrated a convincing correlation
in several western states between the presence of trematodes and
instances of malformed and missing legs in amphibian populations.
But researchers note
that correlation is not causation, so in the four Vermont study
sites, Skelly and his crew put together an experiment that would enable scientists to see how -- or if -- parasites were working
in the real world. A parasite is a plant or animal that makes its
living at another organism's expense; the trematodes of interest
to deformity investigators actually need to exploit three "hosts"
in order to prosper.
This complicated life
cycle begins when a trematode egg, carried in the feces of an infected
raccoon, snake, heron, or the like, is deposited in a pond. The egg hatches, and from it emerges a microscopic creature that swims
off in search of snails, which are very common in wetlands. Once
the parasite has located and entered a snail host, it bides its
time. At a certain point, when it is ready for another round of
travels, it undergoes a transformation, emerging from the snail
as a cercaria, a sperm-like swimmer looking for tadpoles. If the
mission goes as planned, the cercariae form persistent cysts in
the infected animal, which, the parasite hopes, will soon be eaten
by a predator. Once ingested, the cysts open and give rise to sexually
mature trematodes, and inside the third host, these meet, mate,
and lay eggs. The cycle starts anew.
Scientists suspect
that the cysts, which are often found attached to the places from
which limbs develop, are interfering with the process. From the
parasite's viewpoint, this is an ideal tactic. "It needs to get eaten by a predator to continue the life cycle, so what better thing
to do than mess up limb development and make the host easier to
capture?" says Skelly.
To show that this is
actually happening in nature, both Skelly and Kiesecker set up a
series of similar experiments. From the ponds they would study,
the scientists harvested frog eggs, which were hatched and reared
in parasite-free conditions in laboratories in New Haven and State
College. The uninfected tadpoles were then brought back "home" and
placed in cages built from plastic mesh.
In three of the cages,
the mesh was too small to allow cerceriae to enter; in the other
three, the parasites could cruise in at will. If all went as planned,
the tadpoles in the smaller mesh cages would develop a normal complement
of legs, while their vulnerable colleagues would show clear signs
of abnormal limbs.
If
this prediction came to pass, it would establish beyond a reasonable
doubt that parasites played a major role in causing the deformities.
But the two scientists also believed that it wasn't going to be
the entire answer.
As long as tadpoles
have patrolled the wetlands, these animals have had to contend with
parasites, and, except for a handful of rare reports, development
has proceeded without a hitch. Something else had to be going on,
too -- something that made tadpoles unusually vulnerable.
Kiesecker believes
he's found at least one critical factor: a common herbicide called
atrazine. Earlier this year, researchers showed that when tadpoles
in a laboratory setting were exposed to levels of this chemical
that were well within EPA limits in drinking water, some of the
animals developed into hermaphroditic adults. And in a paper published
in July in the Proceedings of the National Academy of Sciences, Kiesecker demonstrated that atrazine could greatly enhance the ability
of trematodes to cause limb abnormalities in frogs.
"Our working hypothesis
is that this chemical somehow surpresses the amphibian immune system
and leaves the animals more susceptible to parasite infection,"
says Kiesecker. "It's not killing them -- it's a subtle effect."
Together, trematodes
and atrazine can, the theory goes, act in synergy. However, the
past few years in Vermont and elsewhere have shown that often enough,
they don't act at all. The parasites are going through their complicated
life cycle, low levels of the herbicide are washing off corn fields
and entering wetlands, but in places where deformities had been
common, the frogs are doing just fine.
This was just what
occurred in Skelly's cages in Vermont, a finding that mirrored the
relative paucity of limbless frogs in the state in 2002. The explanation,
the ecologist surmises, lies in a third suite of factors: the year-to-year
changes that take place in the natural environment.
Water levels fluctuate
annually. If they're too low, tadpoles may be crowded too closely
together, become overly stressed, experience higher levels of atrazine
or other pollutants, and wind up as relatively easy targets for
parasites. On the other hand, if precipitation is unusually abundant,
as it was this spring in Vermont, fewer of the stress-producing
situations are present and, Skelly would predict, fewer of the frogs
should be stricken with abnormalities.
The scientist will
have a better handle on the complex interaction of factors that
are required to create trouble among frogs -- and people -- in a
year or so when he gets the results of an experiment just underway
at Yale-Myers. There, Skelly is working with a dozen woodland ponds,
all currently free of amphibian deformities. He's thinning the forest
around half of the ponds and leaving the trees around the other
half. In half of the altered ponds, Skelly is adding snails; he's
doing the same thing in half of the untouched ponds.
"We're modifying the
vector of infection directly, and we're also modifying the context
in which infection might occur," he says.
Skelly calls this his
"field of dreams" experiment. "We're building various scenarios
and seeing who comes," the ecologist continues, noting that what
happens may have important implications for frog and human health.
"People tend to consider only the vector of a disease, that is,
animals get sick because there's more of the infection source present.
But there's another way to think about it -- the reason you get
sick is because the environmental context has changed. The way we
change the environment may come back to change us."  |
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