Spatiotemporal heterogeneity decouples infection parameters of amphibian chytridiomycosis

Abstract

Emerging infectious diseases are responsible for declines in wildlife populations around the globe. Mass mortality events associated with emerging infectious diseases are often associated with high number of infected individuals (prevalence) and high pathogen loads within individuals (intensity). At the landscape scale, spatial and temporal variation in environmental conditions can alter the relationship between these infection parameters and blur the overall picture of disease dynamics. Quantitative estimates of how infection parameters covary with environmental heterogeneity at the landscape scale are scarce. If we are to identify wild populations at risk of disease epidemics, we must elucidate the factors that shape, and potentially decouple, the link between pathogen prevalence and intensity of infection over complex ecological landscapes. Using a network of 41 populations of the amphibian host Rana pipiens in Ontario, Canada, we present the spatial and temporal heterogeneity in pathogen prevalence and intensity of infection of the chytrid fungus Batrachochytrium dendrobatidis (Bd), across a 3‐year period. We then quantify how covariation between both infection parameters measured during late summer is modified by previously experienced spatiotemporal environmental heterogeneity across 14 repeat sampled populations. Late summer Bd infection parameters are governed, at least in part, by different environmental factors operating during separate host life‐history events. Our results provide evidence for a relationship between Bd prevalence and thermal regimes prior to host breeding at the site level, and a relationship between intensity of infection and aquatic conditions (precipitation, hydroshed size and river density) throughout host breeding period at the site level. This demonstrates that microclimatic variation within temporal windows can drive divergent patterns of pathogen dynamics within and across years, by effecting changes in host behaviour which interfere with the pathogen's ability to infect and re‐infect hosts. A clearer understanding of the role that spatiotemporal heterogeneity has upon infection parameters will provide valuable insights into host–pathogen epidemiology, as well as more fundamental aspects of the ecology and evolution of interspecific interactions.

Widespread occurrence of Batrachochytrium dendrobatidis in Ontario, Canada, and predicted habitat suitability for the emerging Batrachochytrium salamandrivorans

“…Although Bd was detected across our study area, chytridiomycosis was not-consistent with other studies from eastern North America showing persistent occurrence of Bd in the absence of disease. In southern Ontario, 28.9% of 2,223 L. pipiens tested positive for Bd, but no sick or dead specimens were observed (McMillan et al, 2020). On the east coast of Canada, Bd was detected in 26.9% of 115 sampled amphibians, but only a single, deceased L. sylvaticus exhibited clinical signs of disease (Forzán et al, 2010).…”

“…These detections could indicate a recent range expansion—but Bd was also detected in museum specimens from Quebec, Canada, collected as early as 1961 (Ouellet et al, 2005 ). Further sampling across Canada continues to detect Bd even with low sampling effort, and reported prevalence in samples from wild populations of Canadian amphibians ranges from 26.9% to 100% (Brunet et al, 2020 ; D’Aoust‐Messier et al, 2015 ; Forzán et al, 2010 ; Jongsma et al, 2019 ; McMillan et al, 2020 ; Schock et al, 2010 ). Taken together, these studies contradict the predictions of available SDMs and suggest Bd is established and enzootic in Canada, highlighting the importance of representative sampling to inform SDMs.…”

Amphibian Disease Ecology: Are We Just Scratching the Surface?

“…Ranaviruses and chytrid fungi may rely therefore on reservoirs, such as sublethally infected individuals, for long-term persistence in amphibian communities (Gray et al 2009;Blaustein et al 2011;Bosch et al 2015;Schmidt et al 2017;Brannelly et al 2018). In fact, the amphibian-reservoir hypothesis is strongly supported by reoccurring pathogen emergence in amphibian communities inhabiting semipermanent and ephemeral wetlands (Hunter et al 2010;Hall et al 2018;McMillan et al 2020), as well as after environmental chemical disinfection (Bosch et al 2015). Furthermore, Bd and ranaviruses can persist in overwintering individuals (Brunner et al 2004;Narayan et al 2014).…”

“…The scientific community has been alarmed by disease-associated declines in amphibian populations all over the world (Daszak et al 2003;Muths and Hero 2010;Grant et al 2016;Cohen et al 2019;Scheele et al 2019), but the true scale of declines is unknown and knowledge on the spatiotemporal pattern remains limited (Brunner et al 2015;Duffus et al 2015;Scheele et al 2019;McMillan et al 2020). A key finding emerging from the literature is that environmental heterogeneity can strongly shape interactions between pathogens and their potential hosts by physiologically limiting vital processes of both host and parasite including growth, dispersal, and survival (Ostfeld et al 2005;Altizer et al 2013;McMillan et al 2020), thus potentially driving disease outcomes in various ecological and evolutionary trajectories (Echaubard et al 2014;Savage et al 2015). However, the literature reveals multifaceted and even conflicting patterns (Smalling et al 2019), providing a complex framework often difficult to translate into actions for conservation management.…”

Temperature and duration of exposure drive infection intensity with the amphibian pathogen Batrachochytrium dendrobatidis

“…Important drivers of infection intensity include variation in immune response ( Nava-González et al, 2021 ), individual health status and susceptibility ( Beldomenico & Begon, 2010 ; Brunner et al, 2017 ), behavioural patterns ( Burrowes et al, 2017 ) and the environment in which infection occurs ( McMillan et al, 2020 ; Carter et al, 2021 ). Another reason for variation in infection intensity is heterogeneity in how pathogen exposure occurs and for how long it lasts ( Kumar et al, 2020 ).…”