Parasite rearing and infection temperatures jointly influence disease transmission and shape seasonality of epidemics

Abstract

Seasonal epidemics erupt commonly in nature and are driven by numerous mechanisms. Here, we suggest a new mechanism that could determine the size and timing of seasonal epidemics: rearing environment changes the performance of parasites. This mechanism arises when the environmental conditions in which a parasite is produced impact its performance-independently from the current environment. To illustrate the potential for "rearing effects", we show how temperature influences infection risk (transmission rate) in a Daphnia-fungus disease system through both parasite rearing temperature and infection temperature. During autumnal epidemics, zooplankton hosts contact (eat) fungal parasites (spores) reared in a gradually cooling environment. To delineate the effect of rearing temperature from temperature at exposure and infection, we used lab experiments to parameterize a mechanistic model of transmission rate. We also evaluated the rearing effect using spores collected from epidemics in cooling lakes. We found that fungal spores were more infectious when reared at warmer temperatures (in the lab and in two of three lakes). Additionally, the exposure (foraging) rate of hosts increased with warmer infection temperatures. Thus, both mechanisms cause transmission rate to drop as temperature decreases over the autumnal epidemic season (from summer to winter). Simulations show how these temperature-driven changes in transmission rate can induce waning of epidemics as lakes cool. Furthermore, via thermally dependent transmission, variation in environmental cooling patterns can alter the size and shape of epidemics. Thus, the thermal environment drives seasonal epidemics through effects on hosts (exposure rate) and the infectivity of parasites (a rearing effect). Presently, the generality of parasite rearing effects remains unknown. Our results suggest that they may provide an important but underappreciated mechanism linking temperature to the seasonality of epidemics.

Temperature and host diet jointly influence the outcome of infection in a Daphnia‐fungal parasite system

“…Especially high levels of mortality were observed at 23°C, both in infected and uninfected hosts. This phenomenon might be attributed to increased filtering rates at high temperatures (Shocket et al, ), which aggravate clogging of the host's filtering apparatus by the filamentous cyanobacterium, thereby limiting proper nutrition. Interestingly, the Microcystis diet supported parasite growth in one of two tested clones; under elevated temperature, this diet even resulted in highest parasite output.…”

“…The absence of a general effect of temperature was surprising, as elevated temperatures are associated with an increase in metabolic rates (O’Connor & Bernhardt, ). Thus, high temperatures may increase the filtration rate of zooplankton, thereby facilitating the uptake of fungal spores (Shocket et al, ). Based on such findings, we expected both Daphnia genotypes to display increased susceptibility to the fungal parasite at 23°C.…”

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

“…However, in the planktonic system here, the 7‐day result likely exaggerates the thermal constraint. While difficult to quantify, physical sinking, consumption (Civitello, Pearsall, Duffy, & Hall, ; Penczykowski, Hall, et al, ; Shocket, Vergara, et al, ; Strauss, Civitello, Cáceres, & Hall, ) and damage from radiation (Overholt et al, ) likely remove most spores before 7 days. To acknowledge this mortality, we weighted this component of infectivity ( φ ) using a model of spore longevity.…”

“…We measured foraging rate of hosts by comparing the fluorescence of ungrazed and grazed algae (Penczykowski, Lemanski, et al, 2014;Sarnelle & Wilson, 2008). We added estimates of foraging rate at 30°C to those at 20 and 25°C presented elsewhere using the same methods (Shocket, Vergara, et al, 2018). In both experiments, we measured foraging rate across a gradient of host body size (Kooijman, 2009) to index foraging at a common size among experiments (1.5 mm).…”

“…This decrease could stem from slower host growth rate (since parasite production often scales with host growth: Hall, Knight, et al, 2009;Hall, Simonis, Nisbet, Tessier, & Cáceres, 2009), slower parasite growth independent from host growth or enhanced mortality of infected hosts (truncating production time; Auld, Hall, Housley Ochs, Sebastian, & Duffy, 2014;Civitello, Forys, Johnson, & Hall, 2012). Fourth, hot temperatures could lower the quality of parasite spores released from dead hosts into the environment (Shocket, Vergara, et al, 2018). Finally, these free-living spores could be harmed or killed by hot temperatures.…”