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 (≤5%). 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.

Presence of Ribeiroia ondatrae in the developing anuran limb disrupts retinoic acid levels

“…This is an important finding, as infection by R. ondatrae has been shown to cause limb malformations in anurans (e.g. Johnson et al 1999;Johnson et al 2002;Johnson and Sutherland 2003;Schotthoefer et al 2003). The exact mechanism of how the parasite induces these malformations remains unclear, though the mechanical perturbation hypothesis has been the most widely accepted to date.…”

“…This is in part due to the severe and grotesque limb/body malformations caused by infection (Blaustein and Johnson 2003;Johnson et al 1999). For example, Johnson et al (2002) reported a significant association between severe limb malformations and Ribeiroia infection in nine species of natural amphibian populations distributed across the Western USA. Within infected anurans, the majority of metacercariae (i.e.…”

“…cercarial bodies, which have encysted and are maturing) were found embedded in the basal and tail resorption area. Encystment of the parasite within the basal tissue of hind limbs caused multiple malformations including skin webbings, extra digits, missing limbs and limb duplications (Johnson et al 2002). It is important to note that the types of malformations, which result from successful encystment of parasites in limb tissue, are highly dependent on tadpole developmental stage (Schotthoefer et al 2003).…”

Helminth component community of the paradoxal frog Pseudis platensis Gallardo, 1961 (Anura: Hylidae) from south-eastern Pantanal, Brazil

“…The trematode metacercariae infecting P. platensis probably mature in a bird or reptile final host. Likewise, there are several reports of amphibians acting as second intermediate hosts for trematode larvae, emphasizing the importance of these parasites in the helminth communities (Hamann and Kehr 1999;Hamann and González 2009;Hamann et al 2006), and their influence in the host fitness (Kuris 1997, Johnson et al 2002. The prevalence of digeneans is strongly associated with mollusk abundance (Lafferty 1997).…”

Individual and combined effects of multiple pathogens on Pacific treefrogs

“…; hereafter, Ribeiroia), the chytridiomycete fungus B. dendrobatidis (hereafter, BD), and the oomycete Achlya flagellata to test for interactive effects of multiple pathogens on Pacific treefrogs (Pseudacris regilla). All three pathogens are implicated in amphibian mortality or pathology (Tiffney and Wolf 1939;Johnson et al 2002a;Berger et al 1998) and the cosmopolitan A. flagellata (Post 1987;Khulbe 1994;Noga 1996) and globally distributed BD Pearl et al 2009) are likely to co-occur extensively with Ribeiroia throughout its wide range in North America (Johnson et al 2002a.…”