Temperature and algal food quality jointly regulate seasonality of epidemics in a zooplankton-fungus disease system

Background/Question/Methods

Seasonal epidemics are commonplace. However, co-varying and interacting factors obscure how seasonality mechanistically drives and shapes epidemics. A case study illustrates this issue. In the Daphnia dentifera–Metschnikowia bucuspidata zooplankton-fungal disease system, seasonal epidemics begin in late summer and wane in early winter. During this period, lake water temperature decreases while algal food quality increases. We hypothesized that host nutrition constrains epidemics early in the season, while thermal physiology constrains epidemics late in the season. Thus, disease spread is maximized during the time that we observe epidemic peaks. First, we evaluated this hypothesis by analyzing natural epidemics in eighteen lakes over three years. Second, we conducted experiments manipulating each factor (resource quality and temperature) independently and measured their effects on specific host and parasite traits that affect the spread of disease. We then fit temperature-dependent and resource-dependent functions for the traits, and estimated the effect of each factor on R_0, a measure of disease spread. Finally, based on the covariation between temperature and food quality, we combined these thermal- and resource-based perspectives to predict their joint effect on disease spread over the season.

Results/Conclusions

Evidence from field data and lab experiments demonstrates that temperature is important for regulating disease seasonality. In natural populations, epidemic size was exponentially related to the water temperature when the epidemic starts, suggesting that warmer temperatures promote disease spread. We were able to capture key features of this pattern with a temperate-dependent model of disease parameterized from lab experiments. In the model, R₀ (a measure of disease spread) increases asymptotically with temperature over the relevant range. Sensitivity analysis revealed that this result is driven by transmission rate and spore production. These results provide further evidence that warmer temperatures fuel epidemics early in the season. However, this finding ignores simultaneous changes in food quality. Lab experiments found that spore production increased with food quality, while transmission rate was maximized at intermediate food quality. When the co-varying relationship between temperature and food quality is included in the model, R₀ is maximized at intermediate temperatures that more closely match the timing of observed epidemic peaks. These results suggest that the combined effects of temperature and algal resource quality regulate the size and timing of epidemics in our system.