Parasite (Ribeiroia ondatrae) Infection Linked to Amphibian Malformations in the Western United States

Abstract

Parasites and pathogens can influence the survivorship, behavior, and very structure of their host species. For example, experimental studies have shown that trematode parasites can cause high frequencies of severe limb malformations in amphibians. In a broad-scale field survey covering parts of California, Oregon, Washington, Idaho, and Montana, we examined relationships between the frequency and types of morphological abnormalities in amphibians and the abundance of trematode parasite infection, pH, concentrations of 61 pesticides, and levels of orthophosphate and total nitrate. We recorded severe malformations at frequencies ranging from 1% to 90% in nine amphibian species from 53 aquatic systems. Infection of larvae by the trematode Ribeiroia ondatrae was associated with, and functionally related to, higher frequencies of amphibian limb malformations than found in uninfected populations (Յ5%). Parasites were concentrated around the basal tissue of hind limbs in infected anurans, and malformations associated with infection included skin webbings, supernumerary limbs and digits, and missing or malformed hind limbs. In the absence of Ribeiroia, amphibian populations exhibited low (0-5%) frequencies of abnormalities involving missing digits or distal portions of a hind limb. Species were affected differentially by the parasite, and Ambystoma macrodactylum, Hyla regilla, Rana aurora, R. luteiventris, and Taricha torosa typically exhibited the highest frequencies of abnormalities. None of the water-quality variables measured was associated with malformed amphibians, but aquatic snail hosts (Planorbella spp.) were significant predictors of the presence and abundance of Ribeiroia infection. Morphological comparisons of adult specimens of Ribeiroia collected from different sites and raised in experimental definitive hosts suggested that all samples represented the same species-R. ondatrae. These field results, coupled with experimental research on the effects of Ribeiroia on amphibians, demonstrate that Ribeiroia infection is an important and widespread cause of amphibian limb malformations in the western United States. The relevance of trematode infection to declines of amphibian populations and the influence of habitat modification on the pathology and life cycle of Ribeiroia are emphasized as areas requiring further research.

Synergism between trematode infection and pesticide exposure: A link to amphibian limb deformities in nature?

“…My findings support the hypothesis that parasite infection explains the development of limb deformities observed in frog populations in nature (19,20,26). By preventing access of cercariae to the developing amphibians, I was able to prevent developmental abnormalities.…”

“…Moreover, accelerated eutrophication associated with agricultural practices has been shown to increase snail abundance and incidence of parasitic infection. However, at this point little is known about how habitat modification can alter the prevalence of Ribeiroia or how these changes may influence developing amphibians to defend against infection (26).…”

Predicted Disease Susceptibility in a Panamanian Amphibian Assemblage Based on Skin Peptide Defenses

“…For example, chytridiomycosis-associated population declines in Queensland, Australia, may have contributed to the extirpation of some species from high elevations, whereas other species persisted in the same habitat (Richards et al, 1993;Berger et al, 1998). Pathogens such as Ribeiroia ondatrae and iridoviruses also affect amphibian species differently (Green et al, 2002;Johnson et al, 2002).…”

“…Although there is an effort to predict the probability of population decline of species within the rainforest amphibian assemblage in Panama based on ecologic characteristics (Lips et al, 2003b), no studies have yet investigated the immune defenses of these species. Defense of the skin is critical for protection from many amphibian pathogens, including Aeromonas hydrophila, parasitic water molds (reviewed in Pessier, 2002;Rollins-Smith et al, 2002a), and Ribeiroia ondatrae (Johnson et al, 2001(Johnson et al, , 2002. Batrachochytrium dendrobatidis colonizes keratinized epithelium (Berger et al, 1998;Longcore et al, 1999;.…”

Ecophysiology meets conservation: understanding the role of disease in amphibian population declines

“…With Ribeiroia, for example, the likelihood of a tadpole dying or become malformed increases monotonically with the number of cercariae to which it is exposed [91,93]. Correspondingly, the mean Ribeiroia infection in an amphibian population can be a strong predictor of the malformation frequency among metamorphosing frogs [95].…”