Daily fluctuating temperatures decrease growth and reproduction rate of a lethal amphibian fungal pathogen in culture

Abstract

Background: Emerging infectious diseases (EIDs) are contributing to species die-offs worldwide. We can better understand EIDs by using ecological approaches to study pathogen biology. For example, pathogens are exposed to variable temperatures across daily, seasonal, and annual scales. Exposure to temperature fluctuations may reduce pathogen growth and reproduction, which could affect pathogen virulence, transmission, and environmental persistence with implications for disease. We examined the effect of a variable thermal environment on reproductive life history traits of the fungal pathogen Batrachochytrium dendrobatidis (Bd). Bd causes chytridiomycosis, an emerging infectious disease of amphibians. As a pathogen of ectothermic hosts, Bd can be exposed to large temperature fluctuations in nature. To determine the effect of fluctuating temperatures on Bd growth and reproduction, we collected temperature data from breeding pools of the Yosemite toad (Anaxyrus canorus), a federally threatened species that is susceptible to chytridiomycosis. We cultured Bd under a daily fluctuating temperature regime that simulated Yosemite toad breeding pool temperatures and measured Bd growth, reproduction, fecundity, and viability. Results: We observed decreased Bd growth and reproduction in a diurnally fluctuating thermal environment as compared to cultures grown at constant temperatures within the optimal Bd thermal range. We also found that Bd exhibits temperature-induced trade-offs under constant low and constant high temperature conditions. Conclusions: Our results provide novel insights on variable responses of Bd to dynamic thermal conditions and highlight the importance of incorporating realistic temperature fluctuations into investigations of pathogen ecology and EIDs.

Thermal Performance Curves of Multiple Isolates of Batrachochytrium dendrobatidis, a Lethal Pathogen of Amphibians

“…Furthermore, the fecundity of Bd was highest in low temperatures for every isolate. These findings are in line with those from previous studies that suggest understanding Bd responses (particularly zoospore production) in low temperatures is important to resolving the complexities of the fundamental niche and the disease ecology of Bd (42,49,62).…”

“…Environmental influences on Bd traits such as growth and reproduction may ultimately influence the disease outcomes of chytridiomycosis (42,44). For example, temperature conditions within local environments may increase viability, zoospores densities, fecundity, growth rates, or carrying capacities of Bd, leading to higher infectivity, and greater threat of disease for vulnerable amphibians (49). The threat of biodiversity loss for amphibian communities may be exacerbated from diseases like chytridiomycosis in the coming decades (63).…”

“…Because we used only zoospores to start the growth experiments, we were able to track and quantify several parts of the Bd life cycle as they occurred at different time points in these different temperature conditions. Specifically, by tracking cultures for multiple successive days, we were able to measure the change in population growth, time to maximum zoospore densities, zoospore densities, and calculate fecundity (49). At multiple time points following experimental set up (Day 0), we randomly selected five wells (N = 5) for each of two destructive measures: zoospore counts and viability assays (49).…”

“Heat waves” experienced during larval life have species-specific consequences on life-history traits and sexual development in anuran amphibians

“…These two species are common in Europe, they inhabit various types of water bodies, have different thermal optima (Morand et al 1997) and represent two globally widespread families (Bufonidae and Ranidae). The temperatures we applied occur during heat waves in aquatic habitats of amphibian larvae in the temperate climate zone (Lambert et al 2018, Lindauer et al 2020 and are also recommended for thermal treatment of diseased amphibians (Chatfield and Richards-Zawacki 2011, McMahon et al 2014, Cohen et al 2017, Hettyey et al 2019). Thus, our aim was twofold: to reveal developmental effects of heat waves that may occur in natural habitats, and to assess possible negative consequences of thermal treatment applied against cold-adapted pathogens.…”

Environmental suitability of bare-nosed wombat burrows for Sarcoptes scabiei

“…Notwithstanding the importance of model choice, the stability of environmental conditions is important for fomite survival ( Lindauer et al, 2020 ; Stevenson et al, 2013 ). We found that the temperature and relative humidity conditions within wombat burrows were different from those outside of burrows.…”