Host species composition influences infection severity among amphibians in the absence of spillover transmission

Wildlife epidemiological outcomes can depend strongly on the composition of an ecological community, particularly when multiple host species are affected by the same pathogen. However, the relationship between host species richness and disease risk can vary with community context and with the degree of spillover transmission that occurs among co‐occurring host species. We examined the degree to which host species composition influences infection by Batrachochytrium dendrobatidis (Bd), a widespread fungal pathogen associated with amphibian population declines around the world, and whether transmission occurs from one highly susceptible host species to other co‐occurring host species. By manipulating larval assemblages of three sympatric amphibian species in the laboratory, we characterized the relationship between host species richness and infection severity, whether infection mediates growth and survivorship differently across various combinations of host species, and whether Bd is transmitted from experimentally inoculated tadpoles to uninfected tadpoles. We found evidence of a dilution effect where Bd infection severity was dramatically reduced in the most susceptible of the three host species (Anaxyrus boreas). Infection also mediated survival and growth of all three host species such that the presence of multiple host species had both positive (e.g., infection reduction) and negative (e.g., mortality) effects on focal species. However, we found no evidence that Bd infection is transmitted by this species. While these results demonstrate that host species richness as well as species identity underpin infection dynamics in this system, dilution is not the product of reduced transmission via fewer infectious individuals of a susceptible host species. We discuss various mechanisms, including encounter reduction and antagonistic interactions such as competition and opportunistic cannibalism that may act in concert to mediate patterns of infection severity, growth, and mortality observed in multihost communities.There are many ways in which infection can be influenced by species diversity. Here we show experimentally that the interactions between species in a multi‐host amphibian community drive the severity of infection by the amphibian chytrid fungus. We find no evidence that infection is transmitted between two host species in our study, suggesting that spillover infection is not a cause of dilution effects in this system.Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/111214/1/ece31385.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/111214/2/ece31385-sup-0001-FigureS1.pd

Sensitivity to nitrate and nitrite in pond-breeding amphibians from the Pacific northwest, USA

In static experiments, we studied the effects of nitrate and nitrite solutions on newly hatched larvae of five species of amphibians, namely Rana pretiosa, Rana aurora, Bufo boreas, Hyla regilla, and Ambystoma gracile. When nitrate or nitrite ions were added to the water, some larvae of some species reduced feeding activity, swam less vigorously, showed disequilibrium and paralysis, suffered abnormalities and edemas, and eventually died. The observed effects increased with both concentration and time, and there were significant differences in sensitivity among species. Ambrystoma gracile displayed the highest acute effect in water with nitrate and nitrite. The three ranid species had acute effects in water with nitrite. In chronic exposures, R. pretiosa was the most sensitive species to nitrates and nitrites. All species showed 15-d LC50s lower than 2 mg N-NO2 /L. For both N ions, B. boreas was the least sensitive amphibian. All species showed a high mortality at the U.S. Environmental Protection Agency- recommended limits of nitrite for warm-water fishes (5 mg N-NO2 /L) and a significant larval mortality at the recommended limits of nitrite concentration for drinking water (1 mg N-NO2 The recommended levels of nitrate for warm-water fishes (90 mg N- NO3 /L) were highly toxic for R. pretiosa and A. gracile larvaePeer reviewe

Projected climate-induced faunal change in the western hemisphere

Climate change is predicted to be one of the greatest drivers of ecological change in the coming century. Increases in temperature over the last century have clearly been linked to shifts in species distributions. Given the magnitude of projected future climatic changes, we can expect even larger range shifts in the coming century. These changes will, in turn, alter ecological communities and the functioning of ecosystems. Despite the seriousness of predicted climate change, the uncertainty in climate-change projections makes it difficult for conservation managers and planners to proactively respond to climate stresses. To address one aspect of this uncertainty, we identified predictions of faunal change for which a high level of consensus was exhibited by different climate models. Specifically, we assessed the potential effects of 30 coupled atmosphere–ocean general circulation model (AOGCM) future-climate simulations on the geographic ranges of 2954 species of birds, mammals, and amphibians in the Western Hemisphere. Eighty percent of the climate projections based on a relatively low greenhouse-gas emissions scenario result in the local loss of at least 10% of the vertebrate fauna over much of North and South America. The largest changes in fauna are predicted for the tundra, Central America, and the Andes Mountains where, assuming no dispersal constraints, specific areas are likely to experience over 90% turnover, so that faunal distributions in the future will bear little resemblance to those of today

Effects of the pathogenic water mold Saprolegnia ferax on survival of amphibian larvae

Infectious diseases are a significant threat to worldwide biodiversity. Amphibian declines, a significant part of current biodiversity losses, are in many cases associated with infectious disease. Water molds are one group of pathogens affecting amphibians on a worldwide basis. Although water molds have been studied extensively for their effects on host embryos, little information is available about how they affect post-embryonic amphibians. We tested the effects of one species of water mold, Saprolegnia ferax, in a comparative study of larvae of 4 amphibian species: Pseudacris regilla (Pacific treefrog), Rana cascadae (Cascades frog), Ambystoma macrodactylum (long-toed salamander), and R. aurora (red-legged frog). S. ferax can kill amphibians at the embryonic and juvenile life history stages, depending on the amphibian species. In the present study, a 1 wk exposure to S. ferax killed P. regilla larvae and a 2 wk exposure killed R. aurora larvae. Larvae of the other host species were unaffected after 1 wk of exposure to S. ferax. Our results suggest that S. ferax can kill amphibian larvae and further suggest that evaluation of how pathogens affect amphibians at the population level requires investigation at various life stages

Predation by zooplankton on Batrachochytrium dendrobatidis: Biological control of the deadly amphibian chytrid fungus?

Batrachochytrium dendrobatidis (hereafter Batrachochytrium), a fungal pathogen of amphibians, causes the disease chytridiomycosis which is responsible for unprecedented population declines and extinctions globally. Host defenses against chytridiomycosis include cutaneous symbiotic bacteria and anti-microbial peptides, and proposed treatment measures include use of fungicides and bioaugmentation. Efforts to eradicate the fungus from localized areas of disease outbreak have not been successful. Instead, control measures to mitigate the impacts of the disease on host populations, many of which are already persisting with Batrachochytrium in an endemic state, may be more realistic. The infective stage of the fungus is an aquatic zoospore, 3-5µm in diameter. Here we show that zoospores of Batrachochytrium are consumed by the zooplankter Daphnia magna. This species inhabits amphibian breeding sites where Batrachochytrium transmission occurs, and consumption of Batrachochytrium zoospores may lead to effective biological control of Batrachochytrium.KEYWORDS: Batrachochytrium dendrobatidis, Biological control, Zooplankton, Amphibian chytrid fungus, Daphnia magnaThis is the authors’ post-peer review version of the final article. The final published version is copyrighted by Springer and can be found at: http://www.springer.com/life+sciences/evolutionary+%26+developmental+biology/journal/10531Keywords: Batrachochytrium dendrobatidis, Biological control, Zooplankton, Amphibian chytrid fungus, Daphnia magn

Does the agricultural fungicide Tebuconazole inhibit the growth of the amphibian chytrid fungus?

In the US, significant research is ongoing regarding the interactions of pesticides with species and processes within wetland ecosystems. For example, the effect of such pollutants on amphibian survival and physiology has been an area of focused research. Negative impacts of pesticides to non-target organisms (e.g. amphibians) have been observed. The effects of the fungal disease to amphibians that are also exposed to pesticides is complex, however the effects of pesticides on the free-living fungal pathogen has received little attention. We hypothesized that Tebuconazole would inhibit the growth of the amphibian chytrid fungus in culture. To test this hypothesis, we measured the growth of the fungus exposed to a high concentration of Tebuconazole (0.02mg/ml) over a 12 day period. We observed a rapid increase in fungal density in the first two days of the experiment, followed by a steady decrease in the density. We conclude that a high concentration (0.02 mg/ml) amphibian chytrid fungus growth appears to be inhibited by Tebuconazole, although exposure time appears to be an important factor in the response

Development and Infectious Disease in Hosts with Complex Life Cycles

Metamorphosis is often characterized by profound changes in morphology and physiology that can affect the dynamics of species interactions. For example, the interaction between a pathogen and its host may differ depending on the life stage of the host or pathogen. One pathogen that infects hosts with complex life cycles is the emerging fungal pathogen of amphibians, Batrachochytrium dendrobatidis (Bd). We sought to determine how conditions at the larval stage can affect variation in development and patterns of Bd infection across amphibian life stages. We used outdoor experimental mesocosms to simulate natural pond habitats and manipulated the presence of Bd, the larval density, and the number of host species in larvae of two co-occurring amphibian species (Rana cascadae and Pseudacris regilla). We found that infection differed between species throughout development; P. regilla consistently had higher infection severity compared to R. cascadae. Additionally, while up to 100% of larvae were infected, only 18.2% of R. cascadae and 81.5% of P. regilla were infected after metamorphosis. This indicates that amphibians have the ability to recover from Bd infection as they undergo metamorphosis. Higher larval densities in P. regilla led to a shorter larval period, and individuals with a shorter larval period had lower infection severity. This led to a trend where P. regilla larvae reared at high densities tended to have lower infection prevalence after metamorphosis. We also found that exposure to Bd increased larval mortality and prolonged the larval period in P. regilla, indicating that P. regilla are susceptible to the negative effects of Bd as larvae. This study demonstrates that host density, species composition, and pathogen exposure may all interact to influence development and infection in hosts with complex life cycles

Effects of Ultraviolet Radiation on Amphibians: Field Experiments

Numerous reports suggest that populations of amphibians from a wide variety of locations are experiencing population declines and/or range reductions. In some cases, unusually high egg mortality has been reported. Field experiments have been used with increasing frequency to investigate ultraviolet radiation as one of the potential factors contributing to these declines. Results from field experiments illustrate that hatching success of eggs is hampered by ultraviolet radiation in a number of species, while other species appear to be unaffected. Continued mortality in early life-history stages may ultimately contribute to a population decline. Although UV-B radiation may not contribute to the population declines of all species, it may play a role in the population decline of some species, especially those that lay eggs in open shallow water subjected to solar radiation and in those that have a poor ability to repair UV-induced DNA damage.Peer reviewe

Host Identity Matters in the Amphibian-Batrachochytrium dendrobatidis System: Fine-Scale Patterns of Variation in Responses to a Multi-Host Pathogen

Species composition within ecological assemblages can drive disease dynamics including pathogen invasion, spread, and persistence. In multi-host pathogen systems, interspecific variation in responses to infection creates important context dependency when predicting the outcome of disease. Here, we examine the responses of three sympatric host species to a single fungal pathogen, Batrachochytrium dendrobatidis, which is associated with worldwide amphibian population declines and extinctions. Using an experimental approach, we show that amphibian species from three different genera display significant differences in patterns of pathgen-induced mortality as well as the magnitude and temporal dynamics of infection load. We exposed amphibians to one of four inoculation dose treatments at both larval and post- metamorphic stages and quantified infection load on day 8 and day 15 post-inoculation. Of the three species examined, only one (the Pacific treefrog; Pseudacris regilla) displayed "dose-dependent" responses; survival was reduced and infection load was elevated as inoculation dose was increased. We observed a reduction in survival but no differences in infection load across pathogen treatments in Cascades frogs (Rana cascadae). Western toads (Anaxyrus boreas) displayed differences in infection load but no differences in survival across pathogen treatments. Within species, responses to the pathogen varied with life history stage, and the most heavily infected species at the larval stage was different from the most heavily infected species at the post-metamorphic stage. Temporal changes in infection load were species and life history stage-specific. We show that variation in susceptibility to this multi-host pathogen is complex when viewed at a fine-scale and may be mediated through intrinsic host traits

Influence of ultraviolet-B radiation on growth, prevalence of deformities, and susceptibility to predation in Cascades frog (Rana cascadae) larvae

Abstract Ambient levels of ultraviolet-B radiation (UVB) have a variety of detrimental effects on aquatic organisms. These include death and effects on growth, development, physiology, and behavior. Amphibians show all of these effects. However, the effects vary with species, life history stage, and ecological context. Little is known about the implications of the detrimental effects of UVB on ecological dynamics. Our study was designed to test how UVB may affect predator-prey interactions, an important ecological dynamic. Specifically, we tested the effect of UVB on the susceptibility of Cascades frog (Rana cascadae) larvae to predation by roughskinned newts (Taricha granulosa). We also further examined the sublethal effects of UVB on growth and development in Cascades frog larvae. We found no direct effect of UVB exposure on survival. However, UVB-exposed frog larvae displayed decreased growth and increased prevalence of deformities. UVB also caused increased susceptibility to predation, but there was a significant treatment-block interaction. UVB increased susceptibility to predation in two out of five blocks of Cascades frogs. The other three blocks did not show an effect of UVB on susceptibility to predation. Our study suggests that UVB can alter susceptibility to predation in at least one amphibian species. UVB-induced alteration of predator-prey interactions could potentially lead to changes at the population, community, and ecosystem levels