Ribeiroia ondatrae (Trematoda: Digenea) infection induces severe limb malformations in western toads (Bufo boreas)

Widespread reports of malformed amphibians in North America have prompted investigations into the cause(s) and implications of the phenomenon. Recently, a trematode parasite (Ribeiroia ondatrae) was identified as the probable cause of hind-limb malformations in Pacific treefrogs (Hyla regilla) from California. We exposed a second anuran species, the western toad (Bufo boreas), to specific levels of R. ondatrae infection. In a dose-dependent manner, R. ondatrae infection induced high frequencies (40-85%) of severe limb malformations in surviving toads. Survivorship declined significantly with increasing parasite exposure, falling to 42% in the heaviest treatment. Larvae in control treatments exhibited normal development and low mortality levels. In contrast to previous experiments with R. ondatrae infection in treefrogs, cutaneous fusion was the predominant malformation among infected toads in all treatments. Infection also caused polymely (extra limbs; fore and hind), ectromely (missing limbs), polydactyly (extra digits), and a variety of additional limb malformations. Taken together, these results demonstrate that (i) the teratogenic effects of R. ondatrae are not limited to treefrogs, (ii) the spectrum of R. ondatrae-induced malformations is not confined to the hind limbs, and (iii) the frequency and composition of malformations resulting from infection may vary among amphibian species. Finally, we review historical reports of limb abnormalities in the genus Bufo and discuss established and proposed causative agents, with emphasis on trematode infection and predation.