Short-term temperature fluctuations increase disease in a Daphnia-parasite infectious disease system

Abstract

Climate change has profound effects on infectious disease dynamics, yet the impacts of increased short-term temperature fluctuations on disease spread remain poorly understood. We empirically tested the theoretical prediction that short-term thermal fluctuations suppress endemic infection prevalence at the pathogen’s thermal optimum. This prediction follows from a mechanistic disease transmission model analyzed using stochastic simulations of the model parameterized with thermal performance curves (TPCs) from metabolic scaling theory and using nonlinear averaging, which predicts ecological outcomes consistent with Jensen’s inequality (i.e., reduced performance around concave-down portions of a thermal response curve). Experimental observations of replicated epidemics of the microparasite Ordospora colligata in Daphnia magna populations indicate that temperature variability had the opposite effect of our theoretical predictions and instead increase endemic infection prevalence. This positive effect of temperature variability is qualitatively consistent with a published hypothesis that parasites may acclimate more rapidly to fluctuating temperatures than their hosts; however, incorporating hypothetical effects of delayed host acclimation into the mechanistic transmission model did not fully account for the observed pattern. The experimental data indicate that shifts in the distribution of infection burden underlie the positive effect of temperature fluctuations on endemic prevalence. The increase in disease risk associated with climate fluctuations may therefore result from disease processes interacting across scales, particularly within-host dynamics, that are not captured by combining standard transmission models with metabolic scaling theory.

Environmental variability can promote parasite diversity within hosts and transmission among hosts

“…Similarly, using nonlinear averaging to assess the response of a nonlinear process to variability is contentious. While many theoretical works and some empirical studies support the use of nonlinear averaging and find evidence for Jensen’s inequality, borne out as disproportionate effects of thermal variability on performance, many empirical studies have contested an implicit assumption of nonlinear averaging: that traits should respond instantaneously to change, without acclimation (Bernhardt et al, 2018; Estay et al, 2011; Krichel et al, 2023; Paaijmans et al, 2010; Sinclair et al, 2016). Thermal acclimation through phenotypic plasticity alters thermal performance curves, and as such, produces a more complex relationship between biological rates and temperature that may not be well-characterized by nonlinear averaging (Altman et al, 2016; Schulte et al, 2011; Sckrabulis et al, 2022).…”

Extreme heat reduces host and parasite performance in a butterfly–parasite interaction

“…Both monarchs and OE spores are known to survive in habitats where midday temperatures surpass 34°C [44,84,85], likely because they experience relief from the heat at night, and through behavioural thermoregulation where caterpillars seek shade, thus altering the internal temperature environment experienced by OE [86]. Future studies should therefore use fluctuating temperatures, simulated heatwaves, or shorter pulses of extreme temperatures to assess impacts on infection outcomes [15,44,[87][88][89]. Additionally, experiments should assess whether parasite strains from different locations or infecting different host populations (e.g.…”