Host identity matters in the amphibian-Batrachochytrium dendrobatidis system: fine-scale patterns of variation in responses to a multi-host pathogen

Abstract

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.

Figure 1. Box plots showing pathogen infection load (log genome equivalents +1) of larval and post-metamorphic amphibians across species, treatments, and sampling time-points.

We examined infection load of larval (a.) and post-metamorphic (b.) amphibians of three species (Pseudacris regilla, Rana cascadae, and Anaxyrus boreas) exposed to a High (H), Intermediate (I), or Low (L), inoculation dose treatment and sampled either on day 8 or day 15 of the experiment. Only live animals were sampled at each time-point. Low sample sizes (1 individual) are indicated with a bar and represent a low number of Bd-positive animals or low sample size due to mortality. Lines in the boxes represent the “mean” infection load. Bars are 2 SE of the mean (+/−) and outliers are represented by black dots.

Figure 2. Kaplan-meier survival curves for among treatment responses of post-metamorphic animals to Batrachochytrium dendrobatidis treatments.

For P. regilla (a.) the rate of mortality was significantly different among all three pathogen treatments (low, intermediate, and high inoculation dose). There were no significant differences between rates of mortality in the control versus the low inoculation dose treatment. For R. cascadae (b.) the rate of mortality was significantly greater in the high inoculation dose treatment compared to the low inoculation dose and control treatments. All other between treatment comparisons were non-significant. For A. boreas (c.) there were no significant differences in rate of mortality among the three pathogen treatments. Absolute mortality out the total number animals in each treatment is given in the in the figure legend boxes.