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Box Elder, OR, United States

Johnson P.T.,University of Colorado at Boulder | Bowerman J.,Sunriver Nature Center
Journal of Experimental Zoology Part B: Molecular and Developmental Evolution | Year: 2010

Renewed controversy has emerged over the likely causes and consequences of deformed amphibians, particularly those with missing limbs. The results of a series of experiments by Ballengée and Sessions (2009) implicate aquatic predators (i.e. dragonfly larvae) in causing such abnormalities. Skelly and Benard (2010), however, argued that the small scale of these experiments and the absence of a correlation between predator abundance and deformity frequencies in natural amphibian populations undermine such a conclusion. Drawing upon our experiences with frog malformations, we suggest that the study of amphibian deformities has been hindered by two, interrelated problems. First, empirical studies often fail to critically define the expected baseline level of abnormalities and differentiate between "epidemic" and "endemic" frequencies of malformations. Second, recognizing the likelihood of multiple causes in driving amphibian malformations, continued research needs to embrace a "multiple lines of evidence" approach that allows for complex etiologies by integrating field surveys, diagnostic pathology, comparative modeling, and experiments across a range of ecological scales. We conclude by highlighting the results of a recent study that uses this approach to identify the role of aquatic predators (i.e., fishes and dragonflies) in causing high frequencies of deformed frogs in Oregon. By combining long-term data, comparative data and mechanistic experiments, this study provides compelling evidence that certain predators do cause deformities under ecologically relevant conditions. In light of continuing concerns about amphibian deformities and population declines, we emphasize the need to integrate ecological, epidemiological, and developmental tools in addressing such environmental enigmas. © 2010 Wiley-Liss, Inc., A Wiley Company. Source


Bowerman J.A.Y.,Sunriver Nature Center | Johnsonfi P.T.J.,University of Colorado at Boulder | Bowerman T.,Utah State University
Ecology | Year: 2010

While many predators completely consume their prey, others feed only on blood or tissue without killing the prey, sometimes causing ecologically significant levels of injury. We investigated the importance of sublethal predator attacks in driving an emerging issue of conservation importance: missing-limb deformities in amphibians. We combined longterm field data and manipulative experiments to evaluate the role of sublethal predation in causing abnormalities in two regions of central Oregon, USA. Since 1988, western toads (Bufo boreas) in Lake Aspen have exhibited abnormalities dominated by partially missing limbs and digits at annual frequencies from < 1 % to 35%. On Broken Top volcano, we found comparable types and frequencies of abnormalities in Cascades frogs (Rana cascadae). Field sampling and observational data implicated two aquatic predators in these abnormality phenomena: introduced sticklebacks (Gasterosteus aculeatus) at Lake Aspen and cordulnd dragonfly larvae (Somatochlora albicincta) at Broken Top. In experiments, these predators produced limb abnormalities identical to those observed in the respective regions. At Lake Aspen, in situ predator exclosures effectively eliminated abnormalities in toads, while comparisons among years with low and high stickleback abundance and between wetlands with and without sticklebacks reinforced the link between fish and amphibian abnormalities. Neither trematode parasite infection nor pesticide contamination could explain observed abnormalities. Our results suggest that predators are an important explanation for missing-limb abnormalities and highlight the ecological significance of sublethal predation in nature. © 2010 by the Ecological Society of America. Source


Johnson P.T.J.,University of Colorado at Boulder | Rohr J.R.,University of South Florida | Hoverman J.T.,University of Colorado at Boulder | Kellermanns E.,University of Colorado at Boulder | And 2 more authors.
Ecology Letters | Year: 2012

Parasite infections often lead to dramatically different outcomes among host species. Although an emerging body of ecoimmunological research proposes that hosts experience a fundamental trade-off between pathogen defences and life-history activities, this line of inquiry has rarely been extended to the most essential outcomes of host-pathogen interactions: namely, infection and disease pathology. Using a comparative experimental approach involving 13 amphibian host species and a virulent parasite, we test the hypothesis that 'pace-of-life' predicts parasite infection and host pathology. Trematode exposure increased mortality and malformations in nine host species. After accounting for evolutionary history, species that developed quickly and metamorphosed smaller ('fast-species') were particularly prone to infection and pathology. This pattern likely resulted from both weaker host defences and greater adaptation by parasites to infect common hosts. Broader integration between life history theory and disease ecology can aid in identifying both reservoir hosts and species at risk of disease-driven declines. © 2012 Blackwell Publishing Ltd/CNRS. Source


Johnson P.T.J.,University of Colorado at Boulder | Kellermanns E.,University of Colorado at Boulder | Bowerman J.,Sunriver Nature Center
Functional Ecology | Year: 2011

An emerging framework in animal disease ecology seeks to 'decompose' a host's response to disease into resistance, or its ability to resist infection following exposure, and tolerance, or its ability to limit the damage associated with infection. How these processes vary over the life history of a host, however, and whether developmental changes in resistance and tolerance account for 'critical windows' of disease vulnerability remain open questions. Critical developmental windows are particularly important for infections that alter host development. Recently, increased observations of amphibians with severe limb malformations have stimulated debate over the causes responsible and whether malformation types can be used to infer the agent responsible. The trematode parasite Ribeiroia ondatrae, for example, is often implicated in accounts of extra-legged frogs, but is believed to be unimportant in explaining missing legged animals. Here, we test the influence of host developmental stage, from eggs to post-metamorphosis, on the risk of mortality and the types of malformations produced in Pacific chorus frogs (Pseudacris regilla) following exposure to trematode infection. Consistent with a critical window of vulnerability, host mortality and malformations were greatest among animals exposed during pre-limb and early limb development (15-90%) and decreased to <5% with progressive development. Early stage animals also exhibited a higher frequency of missing limbs, whereas extra limbs and limb elements developed predominantly among tadpoles exposed after limb development was initiated. Hosts infected later in limb development were normal or exhibited only minor outgrowths and abnormal skin webbings. Increases in host tolerance rather than host resistance largely explained the observed changes in pathology. Prior to host metamorphosis, parasites exhibited comparable success invading host tissue, but the amount of resulting damage differed significantly as a function of host size and developmental stage. Following metamorphosis hosts were significantly more resistant to infections, however. These findings highlight the importance of critical developmental windows for infectious diseases and underscore the role of developmental changes in host tolerance in controlling this process. Forecasted changes in climate, for example, have enormous potential to influence both the timing and intensity of host-parasite interactions in nature. © 2011 The Authors. Functional Ecology © 2011 British Ecological Society. Source


Moser W.E.,Smithsonian Institution | Bowerman J.,Sunriver Nature Center | Hovingh P.,721 2nd Avenue | Pearl C.A.,U.S. Geological Survey | Oceguera-Figueroa A.,National Autonomous University of Mexico
Comparative Parasitology | Year: 2014

Placobdella sophieae Oceguera-Figueroa et al., 2010 (Hirudinida: Glossiphoniidae) is reported from Oregon, California, and British Columbia for the first time. New hosts reported for P. sophieae include Taricha granulosa (rough-skinned newt), Rana pretiosa (Oregon spotted frog), and Anaxyrus boreas (western toad). Placobdella sophieae exhibits relatively low host specificity and all amphibians occurring in the Pacific Northwest are potential hosts. © The Helminthological Society of Washington. Source

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