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Rohr, J. R.

Publications and source records attributed to Rohr, J. R..

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The influence of landscape and environmental factors on ranavirus epidemiology in amphibian assemblages

AimTo quantify the influence of a suite of landscape, abiotic, biotic, and host-level variables on ranavirus disease dynamics in amphibian assemblages at two biological levels (site and host-level).\n\nLocationWetlands within the East Bay region of California, USA.\n\nMethodsWe used competing models, multimodel inference, and variance partitioning to examine the influence of 16 landscape and environmental factors on patterns in site-level ranavirus presence and host-level ranavirus infection in 76 wetlands and 1,377 amphibian hosts representing five species.\n\nResultsThe landscape factor explained more variation than any other factors in site-level ranavirus presence, but biotic and host-level factors explained more variation in host-level ranavirus infection. At both the site- and host-level, the probability of ranavirus presence correlated negatively with distance to nearest ranavirus-positive wetland. At the site-level, ranavirus presence was associated positively with taxonomic richness. However, infection prevalence within the amphibian population correlated negatively with vertebrate richness. Finally, amphibian host species differed in their likelihood of ranavirus infection: American Bullfrogs had the weakest association with infection while Western Toads had the strongest. After accounting for host species effects, hosts with greater snout-vent length had a lower probability of infection.\n\nMain conclusionsStrong spatial influences at both biological levels suggest that mobile taxa (e.g., adult amphibians, birds, reptiles) may facilitate the movement of ranavirus among hosts and across the landscape. Higher taxonomic richness at sites may provide more opportunities for colonization or the presence of reservoir hosts that may influence ranavirus presence. Higher host richness correlating with higher ranavirus infection is suggestive of a dilution effect that has been observed for other amphibian disease systems and warrants further investigation. Our study demonstrates that an array of landscape, environmental, and host-level factors were associated with ranavirus epidemiology and illustrates that their importance vary with biological level.

ecology

Shifts in temperature influence how Batrachochytrium dendrobatidis infects amphibian larvae

Many climate change models predict increases in mean temperature, and increases in frequency and magnitude of temperature fluctuations. These potential shifts may impact ectotherms in several ways, including how they are affected by disease. Shifts in temperature may especially affect amphibians, a group with populations that have been challenged by several pathogens. Because amphibian hosts invest more in immunity at warmer than cooler temperatures and parasites may acclimate to temperature shifts faster than hosts (creating lags in optimal host immunity), researchers have hypothesized that a temperature shift from cold-to-warm might result in increased amphibian sensitivity to pathogens, whereas a shift from warm-to-cold might result in decreased sensitivity. Support for components of this climate-variability based hypothesis have been provided by prior studies of the fungus Batrachochytrium dendrobatidis (Bd) that causes the disease chytridiomycosis in amphibians. We experimentally tested whether temperature shifts before Bd exposure alter susceptibility to Bd in the larval stage of two amphibian species - western toads (Anaxyrus boreas) and northern red legged frogs (Rana aurora). Both host species harbored elevated Bd infection intensities under constant cold (15{degrees} C) temperature in comparison to constant warm (20{degrees} C) temperature. Additionally, both species experienced an increase in Bd infection abundance when shifted to 20{degrees} C from 15{degrees} C, compared to a constant 20{degrees} C but they experienced a decrease in Bd when shifted to 15{degrees} C from 20{degrees} C, compared to a constant 15{degrees} C. These results are in contrast to prior studies of adult amphibians that found increased susceptibility to Bd infection after a temperature shift in either direction, highlighting the potential for species and stage differences in the temperature-dependence of chytridiomycosis.

zoology

The Influence of Pesticide Use on Amphibian Chytrid Fungal Infections Varies with Host Life Stage

AimPesticides are widespread and may alter host-pathogen interactions, ultimately influencing pathogen distributions across landscapes. Previous laboratory research supports two hypotheses regarding the effects of pesticides on interactions between amphibians and the predominately aquatic fungal pathogen Batrachochytrium dendrobatidis (Bd): 1) pesticides can be directly toxic to Bd reducing infection risk of aquatic larval amphibians, and 2) exposure to pesticides at formative stages of amphibian development can have long-term consequences on defenses, increasing disease risk after metamorphosis. It remains equivocal whether these laboratory patterns are consistent across amphibian species and occur in the field across broad spatial scales. The aim of this research is to address this research gap on the impact of pesticides on Bd distributions.\n\nLocationContiguous United States.\n\nTime Period1998-2009.\n\nMajor Taxa StudiedAmphibian hosts and Bd.\n\nMethodsOur data included 3,946 individuals evaluated for Bd infection across 49 amphibian species, at 126 locations, which resulted in 199 estimates of Bd prevalence in populations. We used species distribution models and multimodel inference to assess the influence of 1) total pesticide use, 2) pesticide use by type (herbicide, insecticide, fungicide), and 3) the most commonly used pesticide compounds on Bd infection prevalence in amphibian populations across life stages, controlling for several factors previously documented to affect Bd's distribution.\n\nResultsConsistent with laboratory findings, our results indicate 36 that exposure to multiple herbicide compounds is associated with lowered infection risk in the aquatic larval stage but higher risk in the terrestrial post-metamorphic stage.\n\nMain ConclusionsOur study highlights the complex nature of the effects that pesticides can have on disease distributions and suggests that pesticides should be strongly considered at broad scales and across host species, especially in environments in which exposure is widespread. Accurate predictions of disease distributions may lead to more effective management strategies to limit disease spread.

ecology

Effects of agrochemicals on disease severity of Acanthostomum burminis infections (Digenea: Trematoda) in the Asian common toad, Duttaphrynus melanostictus

BackgroundAgrochemicals are widely used in many parts of the world posing direct and indirect threats to organisms. Xenobiotic-related disease susceptibility is a common phenomenon and a proposed cause of amphibian declines and malformations. For example, parasitic infections combined with pesticides generally pose greater risk to both tadpoles and adult frogs than either factor alone. Here, we report on experimental effects of lone and combined exposures to cercariae of the digenetic trematode Acanthostomum burminis and ecologically relevant concentrations of (0.5 ppm) four pesticides (insecticides: chlorpyrifos, dimethoate; herbicides: glyphosate, propanil) on the tadpoles and metamorphs of the Asian common toad, Duttaphrynus melanostictus.\n\nResultsAll 48 cercaraie successfully penetrated each host suggesting that the pesticides had no short-term detrimental effect on cercarial penetration abilities. When the two treatments were provided separately, both cercariae and pesticides significantly decreased the survival of tadpoles and metamorphs and increased developmental malformations, such as scoliosis, kyphosis, and skin ulcers. Exposure to cercariae and the two insecticides additively reduced host survival. In contrast, mortality associated with the combination of cercariae and herbicides was less than additive. The effect of cercariae on malformation incidence depended on the pesticide treatment; dimethoate, glyphosate, and propanil reduced the number of cercarial-induced malformations relative to both the control and chlorpyrifos treatments.\n\nConclusionsThese results show that ecologically relevant concentrations of the tested agrochemicals had minimal effects on trematode infections, in contrast to others studies which showed that these same treatments increased the adverse effects of these infections on tadpoles and metamorphs of the Asian common toad. These findings reinforce the importance of elucidating the complex interactions among xenobiotics and pathogens on sentinel organisms that may be indicators of risk to other biota.

ecology

Atrazine and amphibians: Data re-analysis and a summary of the controversy

The herbicide atrazine is one of the most commonly used, well studied, and controversial pesticides on the planet. Much of the controversy involves the effects of atrazine on wildlife, particularly amphibians and their non-infectious and infectious diseases, including diseases caused by trematode infections. Here I re-analyze data from authors that were funded by Syngenta Crop Protection, Inc., the company that produces atrazine, and show that even these authors revealed that increasing concentrations of atrazine applied to outdoor mesocosms increases the population growth rate of snails that can transmit trematode parasites to amphibians. These researchers missed this finding in their data because they never calculated population growth rates for the snail populations before they reached a carrying capacity or crashed. These results demonstrate that both Syngenta-funded and non-Syngenta-funded researchers have provided evidence that ecologically relevant concentrations of atrazine are capable of increasing snail populations. Given the controversy surrounding the effects of atrazine on amphibians, I follow this re-analysis with a timeline of some of the most salient events in the history of the atrazine-amphibian controversy.

ecology

A global synthesis of phenological responses to climate change

Phenology, or the timing of seasonal activities, is shifting with climate change, resulting in disruptions to the timing of migration and breeding and in emerging asynchronies between interacting species1-5. Recent syntheses have concluded that trophic level1, latitude6, and how phenological responses are measured7 are key to determining the strength of phenological responses to climate change. However, despite these insights, researchers still lack a comprehensive framework that can predict responses to climate change globally and across diverse taxa. For example, little is known about whether phenological shifts are driven by different climatic factors across regions or which ecologically important species characteristics (e.g., body size) predict the strength of phenological responses. Here, we address these questions by synthesizing hundreds of published time series of animal phenology from across the planet. We find that temperature drives phenological responses at mid-latitudes, but precipitation is more important at lower latitudes, likely because these climate factors often drive seasonality in each of these regions. Body size is also negatively associated with the strength of phenological shift, suggesting emerging asynchronies between interacting species that differ in size, such as hosts and ectoparasites and predators and prey. Finally, although there are many compelling biological explanations for spring phenological delays, some examples of delays are associated with short annual records prone to sampling error. As climate change intensifies, our findings arm biologists with predictions concerning which climatic variables and organismal traits drive phenological shifts.

ecology

Thermal mismatches explain how climate change and infectious disease drove widespread amphibian extinctions

Global temperatures and infectious disease outbreaks are simultaneously increasing, but linking climate change and infectious disease to modern extinctions remains difficult. The thermal mismatch hypothesis predicts that hosts should be vulnerable to disease at temperatures where the performance gap between themselves and parasites is greatest. This framework could be used to identify species at risk from a combination of climate change and disease because it suggests that extinctions should occur when climatic conditions shift from historical baselines. We conducted laboratory experiments and analyses of recent extinctions in the amphibian genus Atelopus to show that species from the coldest environments experienced the greatest disease susceptibility and extinction risk when temperatures rapidly warmed, confirming predictions of the thermal mismatch hypothesis. Our work provides evidence that a modern mass extinction was likely driven by an interaction between climate change and infectious disease.

ecology

Are the adverse effects of stressors on amphibians mediated by their effects on stress hormones?

Adverse effects of anthropogenic changes on biodiversity might be mediated by their impacts on the stress response of organisms. To test this hypothesis we crossed exposure to metyrapone, a synthesis inhibitor of the stress hormone corticosterone, with exposure to the herbicide atrazine and the fungal pathogen Batrachochytrium dendrobatidis (Bd) to assess whether the effects of these stressors on tadpoles and post-metamorphic frogs were mediated by corticosterone. Metyrapone countered atrazine-and Bd-induced corticosterone elevations. However, atrazine-and Bd-induced reductions in body size were not mediated by corticosterone because they persisted despite metyrapone exposure. Atrazine lowered Bd abundance without metyrapone but increased Bd abundance with metyrapone for tadpoles and frogs. In contrast, atrazine reduced tolerance of Bd infections because frogs exposed to atrazine as tadpoles had reduced growth with Bd compared to solvent controls; this effect was not countered by metyrapone. Our results suggest that the adverse effects of atrazine and Bd on amphibian growth, development, and tolerance of infection are not mediated primarily by corticosterone. Instead, these effects are likely a function of energy lost from atrazine detoxification, defense against Bd, or repair from damage caused by atrazine and Bd. Additional studies are needed to evaluate how often the effects of anthropogenic stressors are mediated by stress hormones.

ecology

Agrochemical pollution increases risk of human exposure to schistosome parasites

Roughly 10% of the global population is at risk of schistosomiasis, a snail-borne parasitic disease that ranks among the most important water-based diseases of humans in developing countries1-3. Increased prevalence, infection intensity, and spread of human schistosomiasis to non-endemic areas has been consistently linked with water resource management related to agricultural expansion, such as dam construction, which has resulted in increased snail habitat1,4-6. However, the role of agrochemical pollution in human schistosome transmission remains unexplored, despite strong evidence of agrochemicals increasing snail-borne diseases of wildlife7-9 and a projected 2- to 5-fold increase in global agrochemical use by 205010 that will disproportionately occur in schistosome-endemic regions. Using a field mesocosm experiment, we show that environmentally relevant concentrations of fertilizer, the common herbicide atrazine, and the common insecticide chlorpyrifos, individually and as mixtures, increase densities of schistosome-infected snails by increasing the algae snails eat (fertilizer and atrazine) and decreasing densities of snail predators (chlorpyrifos). Epidemiological models indicate that these agrochemical effects can increase transmission of schistosomiasis. Hence, the rapid agricultural changes occurring in schistosome-endemic regions11,12 that are driving increased agrochemical use and pollution could potentially increase the burden of schistosomiasis in these areas. Identifying agricultural practices or agrochemicals that minimize disease risk will be critical to meeting growing food demands while improving human wellbeing13,14.

ecology

A pesticide paradox: Fungicides indirectly increase fungal infections

There are many examples where the use of chemicals have had profound unintended consequences, such as fertilizers reducing crop yields (paradox of enrichment) and insecticides increasing insect pests (by reducing natural biocontrol). Recently, the application of agrochemicals, such as agricultural disinfectants and fungicides, has been explored as an approach to curb the pathogenic fungus, Batrachochytrium dendrobatidis (Bd), which is associated with worldwide amphibian declines. However, the long-term, net effects of early-life exposure to these chemicals on amphibian disease risk have not been thoroughly investigated. Using a combination of laboratory experiments and analysis of data from the literature, we explored the effects of fungicide exposure on Bd infections in two frog species. Extremely low concentrations of the fungicides azoxystrobin, chlorothalonil, and mancozeb were directly toxic to Bd in culture. However, estimated environmental concentrations of the fungicides did not reduce Bd on Cuban tree frog (Osteopilus septentrionalis) tadpoles exposed simultaneously to any of these fungicides and Bd, and fungicide exposure actually increased Bd-induced mortality. Additionally, exposure to any of these fungicides as tadpoles resulted in higher Bd abundance and greater Bd-induced mortality when challenged with Bd post-metamorphosis, an average of 71 days after their last fungicide exposure. Analysis of data from the literature revealed that previous exposure to the fungicide itraconazole, which is commonly used to clear Bd infections, made the critically endangered booroolong frog (Litoria booroolongensis) more susceptible to Bd. Finally, a field survey revealed that Bd prevalence was positively associated with concentrations of fungicides in ponds. Although fungicides show promise for controlling Bd, these results suggest that, if fungicides do not completely eliminate Bd or if Bd re-colonizes, exposure to fungicides has the potential to do more harm than good. To ensure that fungicide applications have the intended consequence of curbing amphibian declines, researchers must identify which fungicides do not compromise the pathogen resistance mechanisms of amphibians.

ecology

Towards a Global Framework for Estimating Acclimation and Thermal Breadth that Predicts Risk from Climate Change

Thermal breadth, the range of body temperatures over which organisms perform well, and thermal acclimation, the ability to alter optimal performance temperature and critical thermal maximum or minimum with changing temperatures, reflect the capacity of organisms to respond to temperature variability and are thus crucial traits for coping with climate change. Although there are theoretical frameworks for predicting thermal breadths and acclimation, the predictions of these models have not been tested across taxa, latitudes, body sizes, traits, habitats, and methodological factors. Here, we address this knowledge gap using simulation modeling and empirical analyses of >2,000 acclimation strengths from >500 species using four datasets of ectotherms. After accounting for important statistical interactions, covariates, and experimental artifacts, we reveal that i) acclimation rate scales positively with body size contributing to a negative association between body size and thermal breadth across species and ii) acclimation capacity increases with body size, seasonality, and latitude (to mid-latitudinal regions) and is regularly underestimated for most organisms. Contrary to suggestions that plasticity theory and empirical work on thermal acclimation are incongruent, these findings are consistent with theory on phenotypic plasticity. We further validated our framework by demonstrating that it could predict global extinction risk to amphibian biodiversity from climate change.

ecology