Can hot temperatures limit disease transmission? A test of mechanisms in a zooplankton-fungus system

Abstract

ABSTRACTunimodally to temperature, i.e., be maximized at intermediate temperatures and constrained at extreme low and high temperatures. However, empirical evidence linking hot temperatures to decreased transmission in nature remains limited.We tested the hypothesis that hot temperatures constrain transmission in a zooplankton-fungus (Daphnia dentifera-Metschnikowia bicuspidata) disease system where autumnal epidemics typically start after lakes cool from their peak summer temperatures. This pattern suggested that maximally hot summer temperatures could be inhibiting disease spread.Using a series of lab experiments, we examined the effects of high temperatures on five mechanistic components of transmission. We found that (1) high temperatures increased exposure to parasites by speeding up foraging rate but (2) did not alter infection success post-exposure. (3) High temperatures lowered parasite production (due to faster host death and an inferred delay in parasite growth). (4) Parasites made in hot conditions were less infectious to the next host (instilling a parasite ‘rearing’ or ‘trans-host’ effect of temperature during the prior infection). (5) High temperatures in the free-living stage also reduce parasite infectivity, either by killing or harming parasites.We then assembled the five mechanisms into an index of disease spread. The resulting unimodal thermal response was most strongly driven by the rearing effect. Transmission peaked at intermediate-hot temperatures (25-26°C) and then decreased at maximally hot temperatures (30-32°C). However, transmission at these maximally hot temperatures only trended slightly lower than the baseline control (20°C), which easily sustains epidemics in laboratory conditions and in nature. Overall, we conclude that while exposure to hot epilimnetic temperatures does somewhat constrain disease, we lack evidence that this effect fully explains the lack of summer epidemics in this natural system. This work demonstrates the importance of experimentally testing hypothesized mechanisms of thermal constraints on disease transmission. Furthermore, it cautions against drawing conclusions based on field patterns and theory alone.