Ribeiroia () is a genus of trematode parasites that sequentially infect freshwater snails in the family Planorbidae (ramshorn snails) as first intermediate hosts, fish and larval amphibians as second intermediate hosts, and birds and mammals as definitive hosts (see § Life history). In North America, infection by Ribeiroia has been linked to amphibians with limb malformations. The connection between parasitic infection and limb malformations has generated questions about (a) whether parasite-induced malformations in amphibians are increasing (see § Evidence for emergence), and (b) the consequences of such abnormalities for amphibian population conservation (see § Parasite-induced malformations and amphibian conservation).
Taxonomy Ribeiroia is a genus of parasites in the class Trematoda, phylum Platyhelminthes. Currently three species and one subspecies of Ribeiroia are recognized: R. ondatrae in North America, R. marini in the Caribbean, R. m. guadeloupensis on the Caribbean island of Guadeloupe, and R. congolensis in Africa (Johnson et al. 2004). The trematode Cercaria lileta is also closely related to Ribeiroia, and molecular sequence data indicates that it may be a species of Ribeiroia (Johnson et al. 2004). All species of Ribeiroia share the distinctive morphological characteristic of esophageal diverticula (i.e., two short dead-end branches that extend laterally from the esophagus). Other genera closely related to Ribeiroia include Cladocystis trifolium, Cathemasia, and Echinostoma (Johnson et al. 2004). See Johnson et al. (2004) for more details on morphological and ecological differences as well as phylogenetic relationships between these species.
Life cycle Ribeiroia ondatrae has an indirect complex life cycle. The adult worms live inside predatory birds or mammals (the definitive hosts), wherein they reproduce sexually if other worms are present. Mature adults release eggs into the host’s intestinal tract, which are passed with the feces of the host, and to develop need to end up in water. The eggs typically develop in 2–3 weeks, but the time varies depending on water temperature. Eggs hatch into miracidia, a ciliated free-living parasite stage, which infect the first intermediate host, ram’s horn snails in the family Planorbidae, colonizing the snail’s reproductive tissue and eventually forming rediae, a slow-moving worm-like parasite stage. The rediae reproduce asexually, castrating the snail as they feed on its reproductive tissue. The infection becomes mature in about six weeks, when the rediae within the snail begin to release a second free-swimming stage called cercariae. The key identifying characteristic of Ribeiroia ondatrae cercariae is the bifurcated esophagus (although this trait can occur in some closely related genera such as Cladocystis trifolium). Cercariae infect amphibians or fish (the second intermediate hosts) wherein they encyst in (with amphibians) the limb buds or (with fish) along the lateral line and scales of the head, body and gills. Encysted cercariae become metacercariae, a dormant parasite stage with a thin outer membrane. Metacercariae resemble cercariae without their tails and do not reproduce. The definitive hosts (birds and mammals) become infected when they consume an amphibian or fish that has encysted metacercariae. The life cycle is completed when the metacercariae emerge from their cyst and attach to the definitive host’s intestinal tract and develop into adults, typically in the proventriculus of birds and the stomach of mammals.
Infection and amphibian malformations
Laboratory studies Experimental exposure to Ribeiroia ondatrae cercariae has been shown to cause limb malformations in various frog, toad and salamander species, including Pseudacris regilla, Anaxyrus boreas, Lithobates pipiens, A. americanus, Ambystoma macrodactylum, L. clamitans and L. sylvatica. Cercariae appear to prefer to infect in and around the developing limb buds of larval amphibians, which can alter or inhibit limb development. The risk of malformation and mortality varies as a function of parasite exposure level, host development stage, and the amphibian species involved. As expected for macroparasitic infections, a dose-dependent relationship exists between cercariae exposure and pathology, particularly among larval amphibians at pre- or early-limb development stage. Cercarial penetration of host tissue involves proteolytic enzymes. The exact mechanism which alters limb development is unknown, but potential pathways include mechanical disturbance by invading parasites, release of a teratogenic chemical by parasites, or a combination of the two. Susceptibility to infection and the subsequent pathology differs among amphibian species. For example, gray tree frogs (Hyla versicolor) are largely resistant to infection, but toads (e.g. A. americanus) exhibit high frequencies of mortality and malformations following parasite exposure (Johnson and Hartson 2009). The types of limb malformations also vary among species and developmental stage of exposure. The most common errors in development associated with Ribeiroia exposure are skin webbings (cutaneous fusion), missing limbs and limb elements (ectromelia and hemimelia), supernumerary limbs and digits (polymelia and polydactyly), and bony triangles. The factors determining variation in susceptibility among species remain poorly understood. However these observations suggest that the type of malformation alone is unlikely to be diagnostic of Ribeiroia exposure.
Field studies Ribeiroia infection has been linked to malformations in naturally occurring amphibian populations, especially in the western and midwestern US. In a large-scale study in the western US, both the presence and abundance of Ribeiroia infection predicted higher-than-baseline (e.g. >5%) frequencies of abnormalities in one or more amphibian species. Limb malformations were observed in nine species and ranged in frequency from <5% to nearly 90%. The role of Ribeiroia in explaining accounts of amphibian malformations in other regions is varied; Ribeiroia has been associated with malformation "hotspots" in the midwestern and northeastern US, but it was not detected in malformation surveys from Vermont, Alaska, Bermuda, and Michigan.
… excerpt ends here. Continue reading the full article.
