High Resolution Images available Deformed Frogs Form when Parasites
and Pesticides Combine EMBARGOED
until 8 July 2002 at 5:00 p.m. -- Deformities in Pennsylvania wood
frogs are linked to the combination of their infection by parasites and
a weakening of their immune system caused by exposure to pesticides, according
to a study by Penn State researchers to be published in the 9 July issue
of the Proceedings of the National Academy of Sciences. The research includes the first experimental studies of amphibian deformities
conducted in ponds where the animals live. The discoveries, which show
the effect of environmental stress on disease outbreaks, may help to explain
how disease affects the distribution, growth, development, and survival
of frogs, which have been disappearing during recent years at alarming
rates worldwide. "It is not uncommon now for 20 to 30 percent of the frogs at many
locations to have limb deformities," says Joseph Kiesecker,
an assistant professor of biology at Penn State and the leader of the
research team. Since the early 1990s, when school children and amateur
naturalists first began finding frogs with deformed legs in U. S. wetlands,
scientists have been trying to determine the reason for the problem's
escalating occurrence. These deformities in frogs have a chilling resemblance
to the deformities in human caused decades ago by the drug Thalidomide.
"Both the general public and scientists suspect that whatever is
causing these problems in frogs may also cause harm to humans," Kiesecker
says. A decade of scientific research has resulted in two prominent hypotheses
about the causes of frog deformities: one is that they are caused by human-induced
contamination of the frogs' environment with chemicals like pesticides,
and the other is that they are caused by a common naturally-occurring
parasite, the trematode worm. Scientists had found evidence to support
each hypothesis, but the research results were not conclusive enough to
resolve the controversy. "More rigorously designed experiments were
required to determine which factor is more important and how these two
factors work together," Kiesecker explains. Kiesecker's breakthrough was in designing a study that combined field
experiments at the ponds where the frogs live with experiments in the
laboratory. "The kind of field experiments that we did in this study
have never been done before," Kiesecker says. The Kiesecker team
collected tadpoles from ponds in Centre County, Pennsylvania, then used
some of those tadpoles in a series of laboratory experiments and some
in a series of field experiments conducted in six ponds within the same
region. Half of the ponds receive runoff from agricultural fields and
contain detectable levels of pesticides, and half are free of pesticides
and agricultural runoff. The Kiesecker team designed the experiments to test four key hypotheses
regarding the relationship between pesticides, trematode parasites, and
limb deformities in frogs. The first hypothesis was that limb deformities
occur in frogs that are infected with the trematode parasite. Trematode
parasites inhabit a series of host species during their life cycle, including
pond snails. When they leave the snail, in the form of trematode larvae
called cercariae, they swim around in the pond in search of a tadpole,
which is the next host they need to invade in order to survive. The researchers
placed groups of their tadpoles in the six ponds within two kinds of enclosures
located side-by-side--one with a fine screen that prevented the trematode
larvae from entering the enclosure, and the other with a larger-mesh screen
that allowed the trematode larvae to infect the tadpoles. "These same trematode larvae cause "swimmer's itch," which
is a common problem among people who swim in lakes in this part of the
country," Kiesecker says, explaining that the swimmer's immune system
eventually kicks the larvae out, leaving just an annoying rash. "A
more serious problem for people occurs in tropical climates, where trematodes
cause an infection known as Schistosomiasis that kills millions of people
every year." The
only tadpoles that developed limb deformities in the first experiment
were from cages that were exposed to the trematode larvae, while tadpoles
in cages that protected them from the larvae did not get any limb deformities.
"We learned from the first field experiment that tadpoles have to
be exposed to trematode infection for limb deformities to develop,"
Kiesecker explains. The second hypothesis the team tested is that limb deformities in trematode-infected
tadpoles are affected by pesticides. When they analyzed the rates of limb
deformities among their research animals, they found much higher rates
of deformities in trematode-infected tadpoles at the three ponds that
receive agricultural runoff and contain pesticides than in the ponds that
do not. The team then moved into the lab to test their third hypothesis, which
is that pesticide exposure--not some other factor--influenced the increased
rates of deformities developed by the trematode-infected tadpoles in the
field study. These laboratory experiments involved three groups of tadpoles
that the researchers exposed to three different pesticides, plus one group
that they did not expose to pesticides. The pesticides were Atrazine--the
most commonly used pesticide in North America, Malathion--a common household
pesticide that also is used to control insect pests in agricultural fields,
and Esfenvalerate--a synthetic pyrethroid pesticide. "Synthetic pyrethroids
have become increasingly popular during the last couple of years because
they are not very toxic to birds and mammals; however, they are highly
toxic to many other kinds of organisms," Kiesecker says. The researchers also took a blood sample from each tadpole, and then
exposed the four groups of tadpoles to trematode larvae under conditions
that assured the tadpoles would be invaded by the parasites. Trematode
infections can cause limb deformities if the larvae are able to evade
the defenses of the tadpole's immune system long enough to transform themselves
into hard cysts. If the location of the cyst is on cells that are supposed
to develop into legs, the cyst will cause growth disruptions that lead
to missing limbs, split limbs, or multiple limbs. The researchers counted the number of cysts that developed in each infected
tadpole and found a higher number of cysts in the animals that were exposed
to pesticides. "From this experiment, we learned that a trematode-infected
tadpole that is exposed to pesticides is more likely to develop limb-deforming
cysts than is an infected tadpole that is not exposed to pesticides,"
Kiesecker says. Kiesecker and his team designed their experiments to learn how pesticide
exposure affects the immune response of the animals and their ability
to fight off trematode parasites. They studied the blood of all the trematode-infected
tadpoles--both those that were and were not exposed to pesticides during
the laboratory experiments--to determine the prevalence of a type of white
blood cell that fights parasites like trematode larvae. Kiesecker's team
then compared this measure of immune-system strength with the number of
trematode cysts that had formed in each animal. "The tadpoles that
we exposed to pesticides had fewer of this particular kind of white blood
cell compared to the tadpoles that we did not expose to pesticides, suggesting
that pesticides make these animals more susceptible to parasitic infections,"
Kiesecker reports. "The kicker is that the concentrations that caused
deformities were incredibly low for Esfenvalerate and Atrazine--low enough
for humans to drink, based on Environmental Protection Agency standards,"
Kiesecker says. In summary, Kiesecker says, "The field experiments showed that only
the tadpoles that were infected with trematodes developed limb deformities
and that these deformities occurred with more frequency in the groups
of tadpoles that also were exposed to pesticides." The researchers
had found a correlation with pesticides, but they needed to do the laboratory
experiments in order to establish with certainty that pesticides were
the cause of the different rates of deformities. "The lab experiments
show that pesticides can weaken the immune response of the tadpoles, which
can result in more infections, making these tadpoles more likely to develop
limb deformities," Kiesecker says. "We can learn a lot from experiments with amphibians because they
are particularly sensitive to environmental changes that appear to be
associated with the recent emergence of new diseases and resurgence of
old diseases that infect humans," Kiesecker comments. "Frogs
may be a sentinel species that is warning us about the interplay between
human-caused environmental change and disease susceptibility. Hopefully,
people will listen." This research was supported by an Ecology of Infectious Diseases Grant
from the National Institutes of Health
and the National Science Foundation.
[ B K K ]
CONTACTS: Joseph M. Kiesecker, phone: (+) 814-865-8778, e-mail: jmk23@psu.edu
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