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

Abstract

Thermal ecology theory predicts that transmission of infectious diseases should respond unimodally to temperature, that is 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 laboratory experiments, we examined the effects of high temperatures on five mechanistic components of transmission. We found that (a) high temperatures increased exposure to parasites by speeding up foraging rate but (b) did not alter infection success post‐exposure. (c) High temperatures lowered parasite production (due to faster host death and an inferred delay in parasite growth). (d) 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). (e) 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. A free Plain Language Summary can be found within the Supporting Information of this article.

Prevalence of ‘milky disease’ caused by Metschnikowia bicuspidata in Eriocheir sinensis in Panjin city, China

“…The infection rates were inhibited in summer, while they increased after the weather turned cool (Cáceres et al, 2006). Nevertheless, Shocket et al (2019) found that although high temperatures decreased the yield of spores and harmed the free living spores of M. bicuspidata, this effect did not fully explain the lack of summer epidemics in a Daphnia zooplankton host. Dallas and Drake (2016) found that temperature fluctuations can reduce the spread of M. bicuspidata.…”

Warmer temperatures reduce the transmission of a virus in a gregarious forest insect

“…A recent study on a freshwater invertebrate–pathogen system measured different components of disease transmission at several temperatures and found that the most important impacts were on the fungus itself. They demonstrated that the spores of the fungus Metschnikowia bicuspidata were most infectious when produced in the zooplankton hosts at an intermediate temperature and declined in infectiousness when exposed to increasing temperatures as free‐living spores (Shocket et al, 2019). We did not test either of these scenarios, but as far as we are aware, there is no evidence of temperature sensitivity in baculoviruses.…”

“…While examples of temperature‐induced changes in disease prevalence in natural populations have already been identified, the mechanisms are poorly understood. Few empirical studies address how different components of disease transmission respond to thermal change (but see Shocket et al, 2019).…”

Thermal limits in the face of infectious disease: How important are pathogens?

“…shown to be more infectious to their subsequent host (Altman et al, 2016;Shocket, Vergara, et al, 2018), although hot temperatures prior to contacting a host can lead to a decrease in infectiousness (Shocket et al, 2019). How prior thermal experience affects host thermal limits during infection will therefore depend on the interaction between both host and pathogen thermal plasticity; something which models of disease dynamics parameterized from constant temperature experiments will not be able to account for (see also Raffel et al, 2013).…”