Variation in thermal performance of a widespread pathogen, the amphibian chytrid fungus Batrachochytrium dendrobatidis

Abstract

Rates of growth and reproduction of the pathogens that cause emerging infectious diseases can be affected by local environmental conditions; these conditions can thus influence the strength and nature of disease outbreaks. An understanding of these relationships is important for understanding disease ecology and developing mitigation strategies. Widespread emergence of the fungal disease chytridiomycosis has had devastating effects on amphibian populations. The causative pathogen, Batrachochytriumdendrobatidis (Bd), is sensitive to temperature, but its thermal tolerances are not well studied. We examined the thermal responses of three Bd isolates collected across a latitudinal gradient in eastern Australia. Temperature affected all aspects of Bd growth and reproduction that we measured, in ways that often differed among Bd isolates. Aspects of growth, reproduction, and their relationships to temperature that differed among isolates included upper thermal maxima for growth (26, 27, or 28 °C, depending on the isolate), relationships between zoospore production and temperature, and zoospore activity and temperature. Two isolates decreased zoospore production as temperature increased, whereas the third isolate was less fecund overall, but did not show a strong response to temperature until reaching the upper limit of its thermal tolerance. Our results show differentiation in life-history traits among isolates within Australia, suggesting that the pathogen may exhibit local adaptation. An understanding of how environmental temperatures can limit pathogens by constraining fitness will enhance our ability to assess pathogen dynamics in the field, model pathogen spread, and conduct realistic experiments on host susceptibility and disease transmission.

Figure 1. The locations of field sites from which Bd isolates were collected (stars), along with mean monthly maximum (red lines) and minimum (blue lines) air temperatures (from [45]).

Bd was first reported from the Queensland site in 1990, the New South Wales site in 1997, and the Tasmania site in 2004. The temperature range tested that produced maximum growth is shaded for each isolate.

Figure 2. Patterns of growth of Bd (measured as optical density) over time (days) at constant temperatures ranging from 13–28°C, shown for isolates from (a) Queensland (QLD), (b) New South Wales (NSW), and (c) Tasmania (TAS), Australia.

Shown are mean optical densities of Bd grown at an initial concentration of 0.575x10⁶ zoospores per ml.

Figure 3. Representative photographs of three Batrachochytrium dendrobatidis (Bd) isolates (from Queensland, New South Wales, and Tasmania, Australia) at 13, 17, 21, 25 and 27°C.

Photographs were taken on the day of maximum zoospore release.

Figure 4. Box plots showing distributions of the optical density of Batrachochytrium dendrobatidis (Bd) during the logarithmic growth phase (Day 5 [Panels A-C]) and the stationary phase (Day 14 [Panels D–F]), under constant temperatures, ranging from 13–28°C, for isolates from (a, d) Queensland (QLD), (b, e) New South Wales (NSW), and (c, f) Tasmania (TAS), Australia.

Shown are mean optical densities of Bd grown at a concentration of 0.575x10⁶ zoospores per ml. Horizontal lines indicate sets of temperatures that did not differ significantly; letters indicate groupings. Any temperature regime not included in a group differed significantly from all other temperature regimes for that isolate. See Appendix S2 for P-values.

Figure 5. The relationships of reproductive characteristics of Batrachochytrium dendrobatidis (Bd), including a) days to initial zoospore production, b) days to maximum zoospore production, c) zoospore longevity, and d) maximum zoospore density.

B. dendrobatidis followed similar trends across temperature treatments, but differed among the isolates. Note that in some cases the data points for different isolates are overlapping.

Figure 6. The relationships of Batrachochytrium dendrobatidis (Bd) zoosporangia sizes with a) temperature, and b) zoospore density.

Figure 7. Patterns of growth of Batrachochytrium dendrobatidis (Bd) (measured as optical density) over time (days) at constant temperatures ranging from 26–28°C for 14 days, and maintained at 23°C thereafter, shown for isolates from (a) Queensland (QLD), (b) New South Wales (NSW), and (c) Tasmania (TAS), Australia.

Shown are mean optical densities of Bd grown at an initial concentration of 0.575x10⁶ zoospores per ml.