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

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

Projecting the Global Distribution of the Emerging Amphibian Fungal Pathogen, <i>Batrachochytrium dendrobatidis</i>, Based on IPCC Climate Futures

<div><p>Projected changes in climate conditions are emerging as significant risk factors to numerous species, affecting habitat conditions and community interactions. Projections suggest species range shifts in response to climate change modifying environmental suitability and is supported by observational evidence. Both pathogens and their hosts can shift ranges with climate change. We consider how climate change may influence the distribution of the emerging infectious amphibian chytrid fungus, <i>Batrachochytrium dendrobatidis</i> (<i>Bd</i>), a pathogen associated with worldwide amphibian population losses. Using an expanded global <i>Bd</i> database and a novel modeling approach, we examined a broad set of climate metrics to model the <i>Bd</i>-climate niche globally and regionally, then project how climate change may influence <i>Bd</i> distributions. Previous research showed that <i>Bd</i> distribution is dependent on climatic variables, in particular temperature. We trained a machine-learning model (random forest) with the most comprehensive global compilation of <i>Bd</i> sampling records (~5,000 site-level records, mid-2014 summary), including 13 climatic variables. We projected future <i>Bd</i> environmental suitability under IPCC scenarios. The learning model was trained with combined worldwide data (non-region specific) and also separately per region (region-specific). One goal of our study was to estimate of how <i>Bd</i> spatial risks may change under climate change based on the best available data. Our models supported differences in <i>Bd-</i>climate relationships among geographic regions. We projected that <i>Bd</i> ranges will shift into higher latitudes and altitudes due to increased environmental suitability in those regions under predicted climate change. Specifically, our model showed a broad expansion of areas environmentally suitable for establishment of <i>Bd</i> on amphibian hosts in the temperate zones of the Northern Hemisphere. Our projections are useful for the development of monitoring designs in these areas, especially for sensitive species and those vulnerable to multiple threats.</p></div

Predicted change in occurrence probability of amphibian chytrid fungus (<i>Batrachochytrium dendrobatidis</i>) based on future climate conditions using data combined from region-specific models.

<p>Predicted change in occurrence probability of <i>Batrachochytrium dendrobatidis</i> determined using data combined from region-specific global models with future climate conditions forecasted for 2100 in the RCP 2.6, 6.0 and 8.5 scenarios.Predicted future occurrence of <i>Batrachochytrium dendrobatidis</i> determined using the non-region-specific global model based on future climate conditions forecasted for 2100 in the RCP 2.6, 6.0 and 8.5 scenarios. Predicted future occurrence of <i>Batrachochytrium dendrobatidis</i> determined using the non-region-specific global model based on future climate conditions forecasted for 2100 in the RCP 2.6, 6.0 and 8.5 scenarios.</p

Average infection severity in <i>Rana cascadae</i> (“Rc”) was lower than <i>Pseudacris regilla</i> (“Pr”) at all time points (±SE).

<p>Whole larval mouthparts were used for time point 1 (after laboratory infection), oral swabs for larvae at time point 2 (when animals were in the mesocosms) and skin swabs for time point 3 (after metamorphosis). Only animals that tested positive for infection are shown.</p

Correlograms of global amphibian chytrid fungus (<i>Batrachochytrium dendrobatidis</i>) data.

<p><i>Batrachochytrium dendrobatidis</i> correlograms indicate positive spatial autocorrelation in chytrid presence between sampled sites: a) in full dataset; b) 50% sampled training data; c) predictions generated by the random forest model. However, spatial autocorrelation is absent in residuals from the random forest model (d).</p

Predicted change in occurrence probability of amphibian chytrid fungus (<i>Batrachochytrium dendrobatidis</i>) based on future climate conditions using a non-region-specific global model.

<p>Predicted change in occurrence probability of <i>Batrachochytrium dendrobatidis</i> determined using the non-region-specific global model with future climate conditions forecasted for 2100 using RCP 2.6, 6.0 and 8.5 scenarios.</p

Relationship between A) mass at metamorphosis and B) larval period on log-transformed post-metamorphic infection severity in <i>Pseudacris regilla</i>.

<p>Only animals that tested positive for infection are included.</p

Summary of statistical findings.

1<p>Post-metamorphic infection prevalence was analyzed using a binomial GLM with the density and species treatments as predictors.</p>2<p>Proportion of animals in each mesocosm surviving to metamorphosis was analyzed using a binomial GLM with Bd treatment and density and species treatments as predictors.</p>3<p>Larval period was analyzed using a mixed effects model with Bd treatment and density and species treatments as predictors with individuals nested by mesocosm.</p>4<p>Post-metamorphic infection severity was analyzed using a mixed effects model with density and species treatments, mass at metamorphosis and larval period as predictors with individuals nested by mesocosm.</p

Relative importance of input features based on non-region specific (global) model of amphibian chytrid fungus (<i>Batrachochytrium dendrobatidis</i>) occurrence.

<p>Relative importance of an input feature for global <i>Batrachochytrium dendrobatidis</i> occurrence was estimated as an increase in out-of-bag error if training values for that feature were permutated. Plots indicate one standard deviation to show variation between trees in the random forest.</p