Review of the Trematode Genus Ribeiroia (Psilostomidae): Ecology, Life History and Pathogenesis with Special Emphasis on the Amphibian Malformation Problem

Johnson, Pieter T. J.; Sutherland, Daniel R.; Kinsella, John M.; Lunde, Kevin B.

doi:10.1016/s0065-308x(04)57003-3

Cited by 113 publications

(135 citation statements)

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“…When the free-swimming cercarial stages of these parasites encounter an amphibian host, they lose their tails and form encysted metacercariae (Ribeiroia and Echinostoma) or unencysted mesocercariae (Alaria). Ribeiroia encysts subcutaneously, typically near the hind-limb buds or the oral disc (Johnson et al, 1999;Johnson et al, 2004), while Echinostoma enters through the cloaca and encysts in the nephric tissues of its amphibian host (Beaver, 1937;Thiemann and Wassersug, 2000). Alaria mesocercariae can be found throughout the host and exhibit little tissue specificity Johnson et al, 1999).…”

Section: Study Systemmentioning

confidence: 99%

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Experimental infection dynamics: using immunosuppression andin vivoparasite tracking to understand host resistance in an amphibian-trematode system

LaFonte

Johnson

2013

Journal of Experimental Biology

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SUMMARYAlthough naturally occurring hosts often exhibit pronounced differences in infection and pathology, the relative importance of factors associated with host life history and immunity in explaining such patterns often remains speculative. Research in ecoimmunology highlights the trade-offs between host physiology and immunity, for which natural variations in disease susceptibility offer a valuable platform to test predictions within this framework. Here, we combined use of a novel, in vivo assay for tracking parasite fate and an experimental manipulation of host immune function (via chronic corticosterone exposure) to assess the role of host immunity in regulating susceptibility of amphibian hosts to three larval trematodes: Ribeiroia ondatrae, Echinostoma trivolvis and Alaria sp. 2. Results from the in vivo parasite-tracking assay revealed marked differences in initial parasite penetration and subsequent host clearance. Relative to infections in a highly susceptible species (Pseudacris regilla), the virulent trematode R. ondatrae was ~25% less successful at penetrating larvae of three hylid frog species and was cleared >45× faster, such that all parasites were rapidly cleared from hylid hosts over 72h following a Weibull distribution. Immune suppression of Hyla versicolor sharply reduced this resistance and increased infection of all three trematodes by 67 to 190%, with particularly strong increases for R. ondatrae. Diminished resistance correlated with a 62% decrease in circulating eosinophils. Correspondingly, 10days after corticosterone exposures ended, infections declined dramatically while eosinophil levels returned to normal. In light of ongoing declines and deformities in amphibian populations, these findings have application potential for mitigating disease-driven effects.

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Section: Study Systemmentioning

confidence: 99%

“…We identified Ribeiroia, Echinostoma and Alaria based on morphological features of the cercariae (Schell, 1985;Johnson et al, 2004). Previous molecular work from this region has helped validate these identifications .…”

Section: Experimental Exposuresmentioning

confidence: 99%

Experimental infection dynamics: using immunosuppression andin vivoparasite tracking to understand host resistance in an amphibian-trematode system

LaFonte

Johnson

2013

Journal of Experimental Biology

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“…Other potential causes of limb deformities include chemical contaminants (e.g., pesticides) and aquatic predators such as dragonfly larvae (Ouellet 2000. Typical of digenetic trematodes, Ribeiroia ondatrae (hereafter ''Ribeiroia'') has a complex life cycle that involves snail, amphibian, and bird hosts (Johnson et al 2004). In laboratory studies, exposure to Ribeiroia increased mortality and/or induced limb deformities in 13 species of frogs, toads, and salamanders (Kiesecker 2002, Stopper et al 2002, Schotthoefer et al 2003.…”

Section: Introductionmentioning

confidence: 99%

Using an ecosystem‐level manipulation to understand host‐parasite interactions and how they vary with study venue

2012

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Abstract. We investigated interactions between the virulent trematode Ribeiroia ondatrae, which has been linked to amphibian malformations across the United States, and its amphibian host (Pseudacris regilla) using a hierarchical approach involving multi-year regional field surveys, replicated pond enclosures, and an unreplicated ecosystem manipulation of parasite infection. Results of this multi-tiered approach provide strong evidence of the causal linkage between infection and malformations while offering additional insights about the influence of experimental venue on effect size. Among years and across 18 wetlands in northern California, Ribeiroia infection was a strong predictor of malformation frequency, which ranged from 0 to 77% at all sites (n ¼ 6,511). Correspondingly, the addition of .500 Ribeiroia infected snails to an experimentally divided wetland using a three-year Before After Control Impact (BACI) design caused sharp increases in Ribeiroia infection and severe malformations in P. regilla during the manipulation year (but not pre-or post-manipulation). These results were complemented by the findings from a replicated (n ¼ 16) enclosure/exclosure study conducted on both sides of the divided wetland (Hog Lake), which showed increased infection and malformations only among larvae within cages that allowed parasite entry and only on the manipulated side. No differences in mortality were observed among animals as a function of cage type. A comparison of the slope between observed infection and malformations as a function of venue (previous laboratory work and the two spatial scales of this study (cages and whole-pond)) indicated that small-scale experiments exhibit stronger effects relative to results from larger spatial extents. Multi-year sampling also indicated that malformed frogs were unlikely to return as breeding adults, highlighting the potential for population-level impacts associated with high Ribeiroia infections. Taken together, these results provide support for the causal relationship between Ribeiroia infection and amphibian malformations under realistic conditions while simultaneously emphasizing the influence of study venue on the strength of this relationship.

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“…Natural history and study system.-The trematode parasite Ribeiroia ondatrae has a complex life cycle involving transmission among bird or mammal definitive hosts, snail intermediate hosts, and amphibian or fish second intermediate hosts (Johnson et al 2004). The parasite reproduces asexually within planorbid snails, releasing free-swimming cercariae into the aquatic environment that encyst around the developing limbs of larval amphibians, including those of the species examined in this study the Pacific chorus frog (Pseudacris regilla), and frequently cause developmental malformations, including extra, missing, or malformed limbs (Johnson et al 2002).…”

Section: Methodsmentioning

confidence: 99%

“…This extreme form of phenotypic manipulation is hypothesized to increase parasite transmission by increasing predation (''parasite-induced trophic transmission''; Lafferty 1999, Johnson et al 2004. Empirical and theoretical research on ecomorphology has repeatedly emphasized the survival value of effective locomotor performance (Jayne andBennett 1990, Langerhans andDeWitt 2004), suggesting that parasite-induced malformations have the potential to alter host interactions with the environment and, consequently, survival.…”

Section: Introductionmentioning

confidence: 99%

Ecomorphology and disease: cryptic effects of parasitism on host habitat use, thermoregulation, and predator avoidance

Goodman

Johnson

2011

Ecology

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Abstract. Parasites can cause dramatic changes in the phenotypes of their hosts, sometimes leading to a higher probability of predation and parasite transmission. Because an organism's morphology directly affects its locomotion, even subtle changes in key morphological traits may affect survival and behavior. However, despite the ubiquity of parasites in natural communities, few studies have incorporated parasites into ecomorphological research. Here, we evaluated the effects of parasite-induced changes in host phenotype on the habitat use, thermal biology, and simulated predator-escape ability of Pacific chorus frogs (Pseudacris regilla) in natural environments. Frogs with parasite-induced limb malformations were more likely to use ground microhabitats relative to vertical refugia and selected less-angled perches closer to the ground in comparison with normal frogs. Although both groups had similar levels of infection, malformed frogs used warmer microhabitats, which resulted in higher body temperatures. Likely as a result of their morphological abnormalities, malformed frogs allowed a simulated predator to approach closer before escaping and escaped shorter distances relative to normal frogs. These data indicate that parasite-induced morphological changes can significantly alter host behavior and habitat use, highlighting the importance of incorporating the ubiquitous, albeit cryptic, role of parasites into ecomorphological research.

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Review of the Trematode Genus Ribeiroia (Psilostomidae): Ecology, Life History and Pathogenesis with Special Emphasis on the Amphibian Malformation Problem

Cited by 113 publications

References 65 publications

Experimental infection dynamics: using immunosuppression andin vivoparasite tracking to understand host resistance in an amphibian-trematode system

Experimental infection dynamics: using immunosuppression andin vivoparasite tracking to understand host resistance in an amphibian-trematode system

Using an ecosystem‐level manipulation to understand host‐parasite interactions and how they vary with study venue

Ecomorphology and disease: cryptic effects of parasitism on host habitat use, thermoregulation, and predator avoidance

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