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Johnson,
PTJ, KB Lunde, EM Thurman, EG Ritchie, SN Wray, DR Sutherland, JM
Kapfer, TJ Frest, J Bowerman and AR Blaustein. 2002. Parasite
(Ribeiroia ondatrae) infection linked to amphibian malformations
in the western United States. Ecological
Monographs 72:151-168.
Building
upon earlier laboratory experiments
demonstrating that trematode parasites can induce deformities in
developing frogs, this remarkable and ambitious field survey establishes
conclusively that parasites are a major contributor to frog deformities
in the American west. The research team, led by Pieter Johnson,
found a strong geographic association between the abundance of Ribeiroia
ondatrae, a trematode parasite, and the frequency of deformities
in a series of amphibian species, including the western toad Bufo
boreas, the Pacific treefrog Hyla regilla and the long-toed
salamander Ambystoma macrodactylum. Their research also revealed
no relationship between the concentrations of a large number of
pesticides measured in pond water and the frequency of deformities.
As
noted below, these results do not absolve contamination of a role
in amphibian deformities, but they certainly demonstrate the importance
of parasites in the American west.
What
did they do? Johnson et al. surveyed amphibian deformities,
parasite abundance, chemical characteristics and a host of other
parameters (including presence of fish, cattle, snails, surrounding
land use, wetland origen) in aquatic habitats in California, Oregon,
Washington, Idaho and Montana. Their chemical measurements involved
determining the concentrations of 52 different pesticides (and nine
metabolites), plus pH, levels of nitrate and orthophosphate. At
each site they collected 3-6 specimens of each amphibian present;
these specimens were later dissected and examined for parasite infections.
They
then carried out a series of statistical analyses looking for associations
between observed incidence of amphibian deformities and the many
environmental parameters they measured.
What
did they find? Johnson et al. inspected 12,369 individuals
representing 11 species of amphibians and reported deformities in
9 of the species examined. The frequency of abnormalities in sites
varied from 0 to nearly 90% of animals examined. Deformities included
a diversity of limb anomalies (including missing limbs and digits,
extra limbs and digits) and, less frequently, missing eyes, jaw
malformations and other abnormalities.
Three
findings stand out.
First,
they observed a very strong association between the abundance of
Ribeiroia and amphibian deformities. This association
is demonstrated in the following two graphs:
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The
frequency of amphibian malformations in relation to the presence
or absence of Ribeiroia. In sites where Ribeiroia
is absent, deformities were observed in fewer than 5% of animals
surveyed.
graph
from Johnson et al. 2002.
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The
frequency of deformities rose in relation to the frequency
of parasite infections measured in amphibians dissected.
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graph
from Johnson et al. 2002
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Second,
parasite abundance and amphibian deformities appeared to be associated
with sites that were heavily affected by human disturbance, particularly
cattle grazing, or were small impoundments such as constructed farm
ponds.
Johnson
et al. found Ribeiroia in 59 sites in the 21 counties
across 5 states where they sampled. The only significant predictors
of parasite presence or abundance were the presence and abundance
of snails in the genus Planorbella, a natural host of Ribeiroia.
They
could not establish the link between human disturbance and Ribeiroia
abundance conclusively because, as they noted: "unimpacted
sites were poorly represented in our survey and were usually at
high elevations, precluding rigorous comparisons."
They
suggest:
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"dramatic
and widespread alterations of aquatic ecosystems, particularly
the construction of small impoundments or farm ponds, may
have created environments conducive to Ribeiroia infection.
These modified habitats are frequently permanent or semi-permanent
and highly productive, facilitating high densities of Planorbella
snails. As natural wetlands continue to be lost, such aquatic
systems may be becoming increasingly important to amphibians
and waterfowl.
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Third,
there was no association between deformities and the chemical parameters
they measured in water samples. Of the 77 sites they sampled,
only 3 had measurable levels of any pesticide compounds, despite
their use of relatively sensitive assays (detection limits of 0.05
µg/L). This must be interpreted cautiously, however. First,
measurements in the water column may reflect only poorly exposure
sources in sediment and in biota. This is a common pattern for contaminants,
especially lipophilic compounds. Second, while Johnson et al.
sampled for a large number of pesticides and other chemicals, it
is always possible that they missed the causative agent. Third,
recent discoveries by Hayes et
al. demonstrate severe impacts on developing frogs at levels
of exposure similar to the detection limits of measurements in this
study.
What
does it mean? In the American west, parasitic trematodes are
an important, if not the principal, proximal cause of amphibian
limb deformities. While the effects of contamination cannot be ruled
out completely, it is apparent from this work that the geography
of Ribeiroia distribution is the major determinant of when
and where amphibian limb deformities are found in the American west.
Johnson
et al. point out appropriately that the fact that a natural
parasite is inducing limb deformities does not mean, necessarily,
that human influence is not involved in the recent surge of abnormalities.
In particular, their finding that the abundance of Ribeiroia's
host snails is linked to disturbance of aquatic habitats and artificial
impoundments implicates human activities as a causal factor via
two pathways. First, for some reason the snails thrive in these
disturbed habitats, providing abundant hosts for the parasite and
hence high parasite populations. Second, natural wetlands have been
reduced, rendering the disturbed sites increasingly important for
amphibian populations.
Johnson
et al. speculate about whether parasite-induced limb deformations
may contribute to amphibian population declines. They conclude this
remains a conjecture. Data from a
previous study suggest that deformities increase mortality rates,
but no information is available to ascertain whether this affects
population levels.
Questions
also remain about why the deformity link to parasites is so clear
in this study area yet remains more elusive in the mid-west and
east, particularly southern Ontario.
Finally,
an important research question to pursue is whether contaminant
impacts on amphibian immune systems make frogs more vulnerable to
parasitic infections. Work
in press indicates that very low levels of some pesticides reduce
frog immune system competency by over 90%. Whether this reduces
a frog's ability to reject foreign tissue--in this case the Ribeiroia
infection--becomes an important question. Frog immune system impairment
might also underlie vulnerability to fungal infection, which has
been documented in the tropics as a major contributor to massive
frog die-offs.
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