Impacts of thermal mismatches on chytrid fungus Batrachochytrium dendrobatidis prevalence are moderated by life stage, body size, elevation and latitude

Abstract

Global climate change is increasing the frequency of unpredictable weather conditions; however, it remains unclear how species‐level and geographic factors, including body size and latitude, moderate impacts of unusually warm or cool temperatures on disease. Because larger and lower‐latitude hosts generally have slower acclimation times than smaller and higher‐latitude hosts, we hypothesised that their disease susceptibility increases under ‘thermal mismatches’ or differences between baseline climate and the temperature during surveying for disease. Here, we examined how thermal mismatches interact with body size, life stage, habitat, latitude, elevation, phylogeny and International Union for Conservation of Nature (IUCN) conservation status to predict infection prevalence of the chytrid fungus Batrachochytrium dendrobatidis (Bd) in a global analysis of 32 291 amphibian hosts. As hypothesised, we found that the susceptibility of larger hosts and hosts from lower latitudes to Bd was influenced by thermal mismatches. Furthermore, hosts of conservation concern were more susceptible than others following thermal mismatches, suggesting that thermal mismatches might have contributed to recent amphibian declines.

Understanding how temperature shifts could impact infectious disease

“…The predictions of the TMH, specifically that cold-and warm-adapted hosts should have peak disease prevalence at relatively warm and cool temperatures, respectively, have been broadly supported using (1) continental-and global-scale analyses of outbreaks of the fungal pathogen Bd across 394 amphibian host species and 1,396 host populations [46,48]; (2) experiments on hosts that can [53] and cannot thermoregulate [46]; and (3) a meta-analysis on host mortality risk from infection across laboratory studies ( [54]; Fig 1C). Moreover, TMH better explained the timing and location of >66 declines in the genus Atelopus putatively caused by Bd than Bd growth in culture, temperature variability, mean climate alone, climate change alone, or the introduction and spread of Bd [4].…”

“…The thermal mismatch hypothesis (TMH), motivated by cases where host and parasite fitness peak at different temperatures under experimental settings [35,46,47], presents a way to explain how changing temperatures impact infection outcomes ( Fig 1C). Ultimately, the TMH posits that as environmental conditions shift away from those typically experienced by hosts and parasites (but remain within the threshold density of hosts), parasites often outperform hosts ( [4,46,48]; Fig 3). Thus, TMH predicts that parasites reach their highest abundance in hosts in nature at the temperatures they most outperform the host rather than at the temperature they perform best in isolation.…”

Temperature dependence of parasitic infection and gut bacterial communities in bumble bees

“…To determine the effects of environmental temperature on bumble bee gut microbiota and resistance to infection with trypanosomatid parasites, we measured gut bacterial community size and composition and infection intensity in bumble bees (Bombus impatiens) inoculated with the parasite Crithidia bombi, then incubated for 7 days at temperatures between 21 and 37 C. Because bumble and honey bee muscle performance (Gilmour and Ellington, 1993;Harrison and Fewell, 2002), bumble bee respiration rate (Kammer and Heinrich, 1974) and bacterial gut symbiont performance all have higher temperatures of peak performance than does the parasite C. bombi (Palmer-Young et al, 2018b), we predicted that infection would decrease across the temperature range previously recorded in wild bees (Heinrich, 1972). Based on metabolic theory and the concept of thermal mismatches (Cohen et al, 2019) which predict that high temperatures improve performance of the host immune system and antiparasitic bacterial symbionts relative to performance of parasiteswe also predicted that the temperature of peak infection in bees would be lower than the temperature of peak growth rate for parasite cell cultures. Finally, we predicted that higher temperatures would lead to lower absolute quantities of gut bacteria, due to elevation of per capita metabolic rates and consequent reduction of the gut ecosystem's carrying capacity at higher temperatures (Bernhardt et al, 2018;Lemoine, 2019).…”

“…One context in which the effect of temperature on species interactions has been repeatedly demonstrated to reflect the predictions of metabolic theory is that of host-parasite interactions (Raffel et al, 2013;Kirk et al, 2018;Cohen et al, 2019). Metabolic theory predicts that the success of parasites at any given temperature reflects the relative performance of hosts and parasites at that temperature, rather than the absolute performance of either in isolation (Cohen et al, 2017).…”

“…These febrile behaviours can allow hosts to achieve body temperatures in which the host immune system has a relative advantage over parasites (Casadevall, 2016). Consequently, fever can improve the health of individual hosts, with consequences that may be reflected at the landscape scale (Daskin et al, 2011;Cohen et al, 2019). In bees, particularly social bees that thermoregulate their nests, relatively high temperatures have been shown to ameliorate infections with microsporidia, other fungi, and viruses in both adults and larvae (Martín-Hernández et al, 2009;Di Prisco et al, 2011;Xu and James, 2012;Dalmon et al, 2019;Li et al, 2019).…”