Attention:The NSF Public Access Repository (PAR) system and access will be unavailable from 11:00 PM ET on Thursday, August 13 until 12:00 AM ET on Friday, August 14 due to maintenance. We apologize for the inconvenience.


Title: Host infection and disease‐induced mortality modify species contributions to the environmental reservoir
Abstract Environmental pathogen reservoirs exist for many globally important diseases and can fuel epidemics, influence pathogen evolution, and increase the threat of host extinction. Species composition can be an important factor that shapes reservoir dynamics and ultimately determines the outcome of a disease outbreak. However, disease‐induced mortality can change species communities, indicating that species responsible for environmental reservoir maintenance may change over time. Here we examine the reservoir dynamics ofPseudogymnoascus destructans, the fungal pathogen that causes white‐nose syndrome in bats. We quantified changes in pathogen shedding, infection prevalence and intensity, host abundance, and the subsequent propagule pressure imposed by each species over time. We find that highly shedding species are important during pathogen invasion, but contribute less over time to environmental contamination as they also suffer the greatest declines. Less infected species remain more abundant, resulting in equivalent or higher propagule pressure. More broadly, we demonstrate that high infection intensity and subsequent mortality during disease progression can reduce the contributions of high‐shedding species to long‐term pathogen maintenance.  more » « less
Award ID(s):
1911853
PAR ID:
10515806
Author(s) / Creator(s):
; ; ; ; ; ; ; ; ; ; ;
Publisher / Repository:
Ecological Society of America
Date Published:
Journal Name:
Ecology
Volume:
104
Issue:
10
ISSN:
0012-9658
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Environmental pathogen reservoirs exist for many globally important diseases and can fuel disease outbreaks, affect pathogen evolution, and increase the threat of host extinction. Differences in pathogen shedding among hosts can create mosaics of infection risk across landscapes by increasing pathogen contamination in high use areas. However, how the environmental reservoir establishes in multi-host communities and the importance of factors like host-specific infection and abundance in environmental contamination and transmission remain important outstanding questions. Here we examine how Pseudogymnoascus destructans, the fungal pathogen that causes white-nose syndrome in bats, invades and establishes in the environment. We quantified dynamic changes in pathogen shedding, infection intensities, host abundance, and the subsequent propagule pressure imposed by each species within the community. We find that the initial establishment of the pathogen reservoir is driven by different species within the community than those that are responsible for maintaining the reservoir over time. Our results also show that highly shedding species do not always contribute the most to pathogen reservoirs. More broadly, we demonstrate how individual host shedding rates scale to influence landscape-level pathogen contamination. 
    more » « less
  2. Abstract Host competence—the ability to acquire, harbour and transmit infections—drives pathogen spread and persistence in multi‐host communities. Evaluating species‐specific competence is critical for predicting transmission, particularly for generalist fungal pathogens likeBatrachochytrium dendrobatidis(Bd). Despite its central role in disease dynamics, we lack an epidemiologically grounded competence metric that rigorously accounts for how infection intensity affects a host's competence. This knowledge gap limits our ability to compare mechanisms across species and assess their roles in pathogen persistence. To address these challenges, we developed a novel, load‐dependent competence metric using host–pathogen Integral Projection Models (IPMs) that integrates variation in susceptibility, within‐host pathogen growth and pathogen shedding dynamics.We applied this metric to laboratory‐based challenge experiments with three common North American amphibians (Notophthalmus viridescens,Rana clamitansandRana catesbeianus) that persist endemically with Bd. Using dose–response assays and repeated pathogen shedding measurements across species, we asked: (i) is there a consistent, non‐linear relationship between infection intensity and pathogen shedding across species? and (ii) which load‐based traits best predict host competence? We quantified four of five components of host competence—susceptibility, pathogen growth, pathogen survival and load‐dependent shedding—and used these to parameterize species‐specific IPMs, integrating competence into a single relative metric across species.We found that Bd shedding increased non‐linearly with infection intensity, contradicting the standard assumption that Bd shedding is linearly related to infection intensity.Notophthalmus viridescensandR. catesbeianuswere the most competent hosts but through distinct pathways: high susceptibility inN. viridescensand elevated shedding rates inR. catesbeianus. In contrast, density‐dependent reductions in pathogen growth and shedding limitedR. clamitanscompetence. Thus, species‐level competence is not determined by a single trait, but emerges from interactions among multiple load‐based processes.Our results demonstrate that variation in competence emerges from distinct, species‐specific processes across multiple dimensions of competence. By linking individual infection dynamics to population‐level transmission potential, our integrative framework provides a more mechanistic approach to predicting host contributions to community‐level pathogen persistence. Read the freePlain Language Summaryfor this article on the Journal blog. 
    more » « less
  3. Disease outbreaks and pathogen introductions can have significant effects on host populations, and the ability of pathogens to persist in the environment can exacerbate disease impacts by fueling sustained transmission, seasonal epidemics, and repeated spillover events. While theory suggests that the presence of an environmental reservoir increases the risk of host declines and threat of extinction, the influence of reservoir dynamics on transmission and population impacts remains poorly described. Here we show that the extent of the environmental reservoir explains broad patterns of host infection and the severity of disease impacts of a virulent pathogen. We examined reservoir and host infection dynamics and the resulting impacts of Pseudogymnoascus destructans , the fungal pathogen that causes white-nose syndrome, in 39 species of bats at 101 sites across the globe. Lower levels of pathogen in the environment consistently corresponded to delayed infection of hosts, fewer and less severe infections, and reduced population impacts. In contrast, an extensive and persistent environmental reservoir led to early and widespread infections and severe population declines. These results suggest that continental differences in the persistence or decay of P. destructans in the environment altered infection patterns in bats and influenced whether host populations were stable or experienced severe declines from this disease. Quantifying the impact of the environmental reservoir on disease dynamics can provide specific targets for reducing pathogen levels in the environment to prevent or control future epidemics. 
    more » « less
  4. Anthropogenically driven environmental change has imposed substantial threats on biodiversity, including the emergence of infectious diseases that have resulted in declines of wildlife globally. In response to pathogen invasion, maintaining diversity within host populations across heterogenous environments is essential to facilitating species persistence. White-nose syndrome is an emerging fungal pathogen that has caused mass mortalities of hibernating bats across North America. However, in the northeast, peripheral island populations of the endangered northern myotis (Myotis septentrionalis) appear to be persisting despite infection while mainland populations in the core of the species range have experienced sharp declines. Thus, this study investigated host and environmental factors that may contribute to divergent population responses. We compared patterns of pathogen exposure and infection intensity between populations and documented the environmental conditions and host activity patterns that may promote survival despite disease invasion. For island populations, we found lower prevalence and less severe infections, possibly due to a shorter hibernation duration compared to the mainland, which may reduce the time for disease progression. The coastal region of the northern myotis range may serve as habitat refugia that enables this species to persist despite pathogen exposure; however, conservation efforts could be critical to supporting species survival in the long term. 
    more » « less
  5. Pedersen, Amy (Ed.)
    1. Resistance and tolerance are unique host defence strategies that can limit the impacts of a pathogen on a host. However, for most wildlife–pathogen systems, there are still fundamental uncertainties regarding (a) how changes in resistance and tolerance can affect disease outcomes and (b) the mechanisms underlying resistance and tolerance in host populations. 2.Here, we first compared observed patterns of resistance and tolerance and their effects on disease outcomes among salamander species that are susceptible to infection and mortality from the emerging fungal pathogen Batrachochytrium salamandrivorans (Bsal). We then tested whether two putative mechanisms that contribute to host resistance and tolerance, skin sloughing and skin lesion reduction, predicted reduced Bsal growth rate or increased host survival during infection, respectively. 3. We performed multi‐dose Bsal challenge experiments on four species of Salamandridae found throughout North America. We combined the laboratory experiments with dynamic models and sensitivity analysis to examine how changes in load‐dependent resistance and tolerance functions affected Bsal‐induced mortality risk. Finally, we used our disease model to test whether skin sloughing and lesion reduction predicted variability in infection outcomes not described by Bsal infection intensity. 4. We found that resistance and tolerance differed significantly among salamander species, with the most susceptible species being both less resistance and less tolerant of Bsal infection. Our dynamic model showed that the relative influence of resistance versus tolerance on host survival was species‐dependent—increasing resistance was only more influential than increasing tolerance for the least tolerant species where changes in pathogen load had a threshold‐like effect on host survival. Testing two candidate mechanisms of resistance and tolerance, skin sloughing and lesion reduction, respectively, we found limited support that either of these processes were strong mechanisms of host defense. 5. Our study contributes to a broader understanding of resistance and tolerance in host–pathogen systems by showing that differences in host tolerance can significantly affect whether changes in resistance or tolerance have larger effects on disease outcomes, highlighting the need for species and even population‐specific management approaches that target host defence strategies. 
    more » « less