Influence of <i>Ribeiroia ondatrae</i> (Trematoda: Digenea) infection on limb development and survival of northern leopard frogs (<i>Rana pipiens</i>): effects of host stage and parasite-exposure level

Schotthoefer, Anna M.; Koehler, Anson V.; Meteyer, Carol U.; Cole, Rebecca A.

doi:10.1139/z03-099

Cited by 67 publications

(84 citation statements)

References 44 publications

(80 reference statements)

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“…While most previous work on this system and for aquatic parasites generally has involved laboratory, mesocosm or cage studies (Kiesecker 2002, Schotthoefer et al 2003, ecosystem-scale experiments play an important role in ecology by testing the validity of findings reported from more artificial settings or correlative studies (Tilman 1989, Carpenter et al 1995, 2011, Schindler 1998, Vredenburg 2004, Sato et al 2012. By using a BACI design in an experimentally divided lake, we found that the addition of ;500 Ribeiroia infected snails, which represented a small fraction of the overall snail biomass but a significant increase in parasite cercarial release, resulted in a seven-fold increase in observed infection abundance among larval and metamorphic P. regilla.…”

Section: Discussionmentioning

confidence: 99%

“…Similarly, Goodman and Johnson (2011a, b) found that frogs with parasite-induced malformations exhibited poorer performance both under field and laboratory conditions, likely contributing to a significantly lower survival post-metamorphosis. Laboratory studies have also reported that direct exposure to Ribeiroia cercariae can cause 60-100% mortality in larval amphibians (Johnson et al 1999, Schotthoefer et al 2003, highlighting the potential for both direct and indirect mortality stemming from infections.…”

Section: Discussionmentioning

confidence: 99%

“…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. However, only one study (Kiesecker 2002) has examined Ribeiroia-malformation dynamics using field experiments and none has conducted an ecosystem manipulation of this system to test the causal relationship under natural conditions.…”

Section: Introductionmentioning

confidence: 99%

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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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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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

2012

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“…By linking previously collected field data on host richness from 345 wetlands in California with new information on the full macroparasite communities of 1,686 hosts, we tested the influence of amphibian host and parasite richness on realized transmission of the pathogenic trematode Ribeiroia ondatrae, which causes mortality and malformations in amphibians (24)(25)(26). However, because we expected host diversity, parasite diversity, and parasite load to correlate in the field owing to links between colonization and diversity, we used an experimental approach first in the laboratory and then in seminatural outdoor mesocosms to decouple the unique effects of each form of diversity on infection by Ribeiroia and the total parasite community.…”

Section: Significancementioning

confidence: 99%

Host and parasite diversity jointly control disease risk in complex communities

Johnson

Preston

Hoverman

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

127

136

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Host-parasite interactions are embedded within complex communities composed of multiple host species and a cryptic assemblage of other parasites. To date, however, surprisingly few studies have explored the joint effects of host and parasite richness on disease risk, despite growing interest in the diversity-disease relationship. Here, we combined field surveys and mechanistic experiments to test how transmission of the virulent trematode Ribeiroia ondatrae was affected by the diversity of both amphibian hosts and coinfecting parasites. Within natural wetlands, host and parasite species richness correlated positively, consistent with theoretical predictions. Among sites that supported Ribeiroia, however, host and parasite richness interacted to negatively affect Ribeiroia transmission between its snail and amphibian hosts, particularly in species-poor assemblages. In laboratory and outdoor experiments designed to decouple the relative contributions of host and parasite diversity, increases in host richness decreased Ribeiroia infection by 11-65%. Host richness also tended to decrease total infections by other parasite species (four of six instances), such that more diverse host assemblages exhibited ∼40% fewer infections overall. Importantly, parasite richness further reduced both per capita and total Ribeiroia infection by 15-20%, possibly owing to intrahost competition among coinfecting species. These findings provide evidence that parasitic and free-living diversity jointly regulate disease risk, help to resolve apparent contradictions in the diversity-disease relationship, and emphasize the challenges of integrating research on coinfection and host heterogeneity to develop a community ecology-based approach to infectious diseases. biodiversity | dilution effect | community assembly | amphibian decline | disease ecology

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“…However, whether changes in host performance are caused directly by morphological deformities or indirectly owing to other parasite-induced changes (e.g., behavior, physiology) remains unexplored. Because the parasite Ribeiroia ondatrae only causes malformations when tadpoles are infected during susceptible stages of development (Schotthoefer et al 2003), individuals co-occurring within the same pond are typically infected with the parasite but exhibit considerable variation in malformations. Infected individuals range from having externally normal features to being completely immobilized in both hind limbs (Johnson et al 2002), thus providing a rare opportunity to disentangle the direct effects of infection from those involving changes in body plan.…”

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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Influence of Ribeiroia ondatrae (Trematoda: Digenea) infection on limb development and survival of northern leopard frogs (Rana pipiens): effects of host stage and parasite-exposure level

Cited by 67 publications

References 44 publications

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

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

Host and parasite diversity jointly control disease risk in complex communities

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

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