Download The Effect of Trematode Infection on Amphibian Limb

The Effect of Trematode
Infection on Amphibian Limb
Development and Survivorship
Johnson, P, K. Lunde, R. Haight, J.
Bowerman, and A. Blaustein
30 April, 1999. Science, 284: 802-803
Background
• Over the past decade there has been increasing
reports of deformed amphibians throughout North
America
• North American Reporting Center for Amphibian
Malformations (NARCAM) has received over
2100 reports from 1032 sites encompassing 82
species of amphibians.
• Of these, there are 944 reports with verifiable
cases of malformations involving 52 species in 46
states and 4 provinces.
A map of North America showing the
counties from which reports have been
submitted
Examples of Frog Deformities
Polydactyly - the complete duplication
of one or more digits.
Polymelia - supernumery (extra) limb
segments are present.
Common species of frogs
reporting malformations
Possible Causes of Frog
Deformities
• Ultraviolet radiation:
– Continuous exposure of developing frog embryos to UV-B results in
bilaterally reduced or missing limb segments (Ankley et al., 1998)
• Chemical agents:
– Certain limb malformations can be induced in the laboratory frogs
by retinoids (Gardener and Hoppe, 1999)
• Parasites:
– Fungal infections suffocate frogs by clogging pores in their skin
– Positive correlation between ponds with high frequencies of limb
malformations and infections with trematodes (Sessions et al., 1999)
The Bottom Line
• Despite these and other suggested
hypotheses, proximate causes of frog
limb malformations have not been
identified.
Observations by Johnson et al.
• Surveyed 35 ponds in Santa Clara, CA between 199698 to determine the prevalence of deformities among
amphibian populations in the field
• 4 of 13 ponds supporting Pacific treefrogs, Hyla
regilla, revealed severely abnormal frogs
• Intensive monitoring programs (N=8818) at 2 of the
ponds revealed 15-45% of frogs with extra limbs
(polymely) and other hind limb deformities
Possible Cause(s)
• Water tests failed to detect unusual concentrations of
pesticides, PCBs, or heavy metals from the ponds
• Eggs (N= 200) collected from the ponds hatched and
developed normally in the lab
• Community analysis of the 35 ponds revealed that the 4
ponds with abnormal frogs were the only ponds to support
Hyla regilla and an aquatic snail, Planorbella tenuis, that
serves as the 1st intermediate host for the parasitic
trematode, Ribeiroia
• Dissections of frogs from these 4 ponds revealed larval
stages (metacercariae) of this parasite in these treefrogs
Ribeiroia Life Cycle
Question
• Is Ribeiroia infection responsible for
the limb abnormalities observed
among Hyla regilla?
Experimental Design
• Collected egg masses of H. regilla from a field site
with no known records of abnormal frogs
• After hatching, tadpoles were held individually in
1-L containers randomly assigned to 1 of 4
treatments: 0 (control; N=35), 16 (light; N=45), 32
(intermediate; N=45), 48 (heavy; N=45) Ribeiroia
cercaria
• A fifth group (N=10) was exposed to 80 cercariae
of Alaria mustelae
• A sixth group (N=10) was exposed to both
species: 80 A. mustelae and 32 Ribeiroia
H. regilla survivorship and abnormality
frequency with Ribeiroia infections
 Exposure to Ribeiroia resulted in
abnormal limb development in 85%
of frogs (N=71) surviving to
metamorphosis
 The frequency of abnormalities was
high in all Ribeiroia treatments and
showed a positive relationship with
parasite density
 Tadpole survivorship declined with
increasing parasite load
 In the control group 88% of
tadpoles survived and all survivors
showed normal development
Survivorship
Abnormality
H. regilla survivorship and abnormality
frequency across parasite treatments
 Alaria did penetrate tadpoles
but did not increase mortality
or cause limb development,
even at when at very high
densities
 The combination of infections
with Ribeiroia and Alaria has
effects that were similar to
those of Ribeiroia alone
Survivorship
Abnormality
Conclusions
• The frequency and composition of
abnormalities observed in Pacific treefrogs
appears to be the result of parasitic
infections by trematodes of the genus
Ribeiroia
• Trematode infections appear to represent a
substantial source of mortality among
amphibians
Future Directions
• Examine the relationship between parasite infection
and the susceptibility to predation among treefrogs,
especially as it relates to the transmission success of
trematode parasites
• Examine the degree to which trematode infections are
responsible for abnormalities in other populations of
frogs
• Determine the condition(s) leading to a sudden
increase in limb abnormalities among frogs parasitized
by trematodes
• Address the mechanism by which Ribeiroia interferes
with limb development