Cheryl J. Briggs

Most hosts contain few parasites, whereas few hosts contain many. This pattern, known as aggregation, is well-documented in macroparasites where parasite intensity distribution among hosts affects host–parasite dynamics. Infection intensity also drives fungal disease dynamics, but we lack a basic understanding of host–fungal aggregation patterns, how they compare with macroparasites and if they reflect biological processes. To begin addressing these gaps, we characterized aggregation of the fungal pathogen Batrachochytrium dendrobatidis (Bd) in amphibian hosts. Utilizing the slope of Taylor’s Power law, we found Bd intensity distributions were more aggregated than many macroparasites, conforming closely to lognormal distributions. We observed that Bd aggregation patterns are strongly correlated with known biological processes operating in amphibian populations, such as epizoological phase (i.e. invasion, post-invasion and enzootic), and intensity-dependent disease mortality. Using intensity-dependent mathematical models, we found evidence of evolution of host resistance based on aggregation shifts in systems persisting with Bd following disease-induced declines. Our results show that Bd aggregation is highly conserved across disparate systems and contains signatures of potential biological processes of amphibian–Bd systems. Our work can inform future modelling approaches and be extended to other fungal pathogens to elucidate host–fungal interactions and unite host–fungal dynamics under a common theoretical framework.

Batrachochytrium dendrobatidis (Bd) is an aquatic chytrid fungus that infects amphibians and has the potential to remain viable outside of hosts. However, the role of aquatic microbiota in influencing Bd growth and survival remains insufficiently understood. In this study, we demonstrated that in the absence of amphibian hosts, aquatic environmental (AE) biofilms supported the development of Bd, allowing it to complete its life cycle for a short period; whereas aquatic planktonic microorganisms did not. However, exposure of Bd zoospores to AE biofilms or planktonic microorganisms resulted in a significant reduction in Bd DNA within a week. These results suggest a dual role of aquatic biofilms in both supporting Bd growth and inhibiting it simultaneously. Moreover, Bd monolayers, composed mainly of zoosporangia, rapidly declined when exposed to AE planktonic microorganisms. Laboratory-formulated nutrients further enhanced the Bd-inhibitory effect of AE microbiota, suggesting that competition for shared nutrients plays a role in this interaction. This study advances our understanding of the complex interactions between Bd and aquatic microbial communities, underscores the ecological significance of biofilm-associated environments, and supports the potential of microbiota-informed interventions for controlling chytridiomycosis in amphibians.

The recently-emerged amphibian chytrid fungus Batrachochytrium dendrobatidis (Bd) has had an unprecedented impact on global amphibian populations, and highlights the urgent need to develop effective mitigation strategies against this pathogen. We conducted field antifungal treatment experiments in populations of the endangered mountain yellow-legged frog during or immediately after Bd-caused mass die-off events. The objective of the treatments was to reduce Bd infection intensity (“load”) and in doing so alter frog-Bd dynamics and increase the probability of frog population persistence despite ongoing Bd infection. Experiments included treatment of early life stages (tadpoles and subadults) with the antifungal drug itraconazole, treatment of adults with itraconazole, and augmentation of the skin microbiome of subadults with Janthinobacterium lividum , a commensal bacterium with antifungal properties. All itraconazole treatments caused immediate reductions in Bd load, and produced longer-term effects that differed between life stages. In experiments focused on early life stages, Bd load was reduced in the two months immediately following treatment and was associated with increased survival of subadults. However, Bd load and frog survival returned to pre-treatment levels in less than one year, and treatment had no effect on population persistence. In adults, treatment reduced Bd load and increased frog survival over the three-year post-treatment period, consistent with frogs having developed an effective adaptive immune response against Bd. Despite this protracted period of reduced impacts of Bd on adults, recruitment of new individuals into the adult population was limited and the population eventually declined to near-extirpation. In the microbiome augmentation experiment, bathing frogs in a J. lividum solution after Bd load reduction with itraconazole increased concentrations of this bacterium on frogs, but concentrations declined to baseline levels within one month and did not have a protective effect against Bd infection. Collectively, these results suggest that Bd mitigation efforts focused on frog populations that have recently declined due to Bd emergence are ineffective in causing long-term changes in frog-Bd dynamics and increasing population persistence, due largely to the inability of early life stages to mount an effective immune response against Bd and resulting high susceptibility. This results in repeated recruitment failure and a low probability of population persistence in the face of ongoing Bd infection.

Emerging infectious diseases have caused many species declines, changes in communities and even extinctions. There are also many species that persist following devastating declines due to disease. The broad mechanisms that enable host persistence following declines include evolution of resistance or tolerance, changes in immunity and behaviour, compensatory recruitment, pathogen attenuation, environmental refugia, density‐dependent transmission and changes in community composition. Here we examine the case of chytridiomycosis, the most important wildlife disease of the past century. We review the full breadth of mechanisms allowing host persistence, and synthesise research on host, pathogen, environmental and community factors driving persistence following chytridiomycosis‐related declines and overview the current evidence and the information required to support each mechanism. We found that for most species the mechanisms facilitating persistence have not been identified. We illustrate how the mechanisms that drive long‐term host population dynamics determine the most effective conservation management strategies. Therefore, understanding mechanisms of host persistence is important because many species continue to be threatened by disease, some of which will require intervention. The conceptual framework we describe is broadly applicable to other novel disease systems.

World‐wide, infectious diseases represent a major source of mortality in humans and livestock. For wildlife populations, disease‐induced mortality is likely even greater, but remains notoriously difficult to estimate—especially for endemic infections. Approaches for quantifying wildlife mortality due to endemic infections have historically been limited by an inability to directly observe wildlife mortality in nature. Here we address a question that can rarely be answered for endemic pathogens of wildlife: what are the population‐ and landscape‐level effects of infection on host mortality? We combined laboratory experiments, extensive field data and novel mathematical models to indirectly estimate the magnitude of mortality induced by an endemic, virulent trematode parasite (Ribeiroia ondatrae) on hundreds of amphibian populations spanning four native species. We developed a flexible statistical model that uses patterns of aggregation in parasite abundance to infer host mortality. Our model improves on previous approaches for inferring host mortality from parasite abundance data by (i) relaxing restrictive assumptions on the timing of host mortality and sampling, (ii) placing all mortality inference within a Bayesian framework to better quantify uncertainty and (iii) accommodating data from laboratory experiments and field sampling to allow for estimates and comparisons of mortality within and among host populations. Applying our approach to 301 amphibian populations, we found that trematode infection was associated with an average of between 13% and 40% population‐level mortality. For three of the four amphibian species, our models predicted that some populations experienced >90% mortality due to infection, leading to mortality of thousands of amphibian larvae within a pond. At the landscape scale, the total number of amphibians predicted to succumb to infection was driven by a few high mortality sites, with fewer than 20% of sites contributing to greater than 80% of amphibian mortality on the landscape. The mortality estimates in this study provide a rare glimpse into the magnitude of effects that endemic parasites can have on wildlife populations and our theoretical framework for indirectly inferring parasite‐induced mortality can be applied to other host–parasite systems to help reveal the hidden death toll of pathogens on wildlife hosts.

Moving animals on a landscape through translocations and reintroductions is an important management tool used in the recovery of endangered species, particularly for the maintenance of population genetic diversity and structure. Management of imperiled amphibian species rely heavily on translocations and reintroductions, especially for species that have been brought to the brink of extinction by habitat loss, introduced species, and disease. One striking example of amphibian declines and associated management efforts is in California's Sequoia and Kings Canyon National Parks with the mountain yellow‐legged frog species complex (Rana sierrae/muscosa ). Mountain yellow‐legged frogs have been extirpated from more than 93% of their historic range, and limited knowledge of their population genetics has made long‐term conservation planning difficult. To address this, we used 598 archived skin swabs from both extant and extirpated populations across 48 lake basins to generate a robust Illumina‐based nuclear amplicon data set. We found that samples grouped into three main genetic clusters, concordant with watershed boundaries. We also found evidence for historical gene flow across watershed boundaries with a north‐to‐south axis of migration. Finally, our results indicate that genetic diversity is not significantly different between populations with different disease histories. Our study offers specific management recommendations for imperiled mountain yellow‐legged frogs and, more broadly, provides a population genetic framework for leveraging minimally invasive samples for the conservation of threatened species.

Pathogen persistence in host communities is influenced by processes operating at the individual host to landscape‐level scale, but isolating the relative contributions of these processes is challenging. We developed theory to partition the influence of host species, habitat patches and landscape connectivity on pathogen persistence within metacommunities of hosts and pathogens. We used this framework to quantify the contributions of host species composition and habitat patch identity on the persistence of an amphibian pathogen across the landscape. By sampling over 11 000 hosts of six amphibian species, we found that a single host species could maintain the pathogen in 91% of observed metacommunities. Moreover, this dominant maintenance species contributed, on average, twice as much to landscape‐level pathogen persistence compared to the most influential source patch in a metacommunity. Our analysis demonstrates substantial inequality in how species and patches contribute to pathogen persistence, with important implications for targeted disease management.

Amphibians, the most threatened group of vertebrates, are seen as indicators of the sixth mass extinction on earth. Thousands of species are threatened with extinction and many have been affected by an emerging infectious disease, chytridiomycosis, caused by the fungal pathogen, Batrachochytrium dendrobatidis (Bd). However, amphibians exhibit different responses to the pathogen, such as survival and population persistence with infection, or mortality of individuals and complete population collapse after pathogen invasion. Multiple factors can affect host pathogen dynamics, yet few studies have provided a temporal view that encompasses both the epizootic phase (i.e. pathogen invasion and host collapse), and the transition to a more stable co-existence (i.e. recovery of infected host populations). In the Sierra Nevada mountains of California, USA, conspecific populations of frogs currently exhibit dramatically different host/ Bd-pathogen dynamics. To provide a temporal context by which present day dynamics may be better understood, we use a Bd qPCR assay to test 1165 amphibian specimens collected between 1900 and 2005. Our historical analyses reveal a pattern of pathogen invasion and eventual spread across the Sierra Nevada over the last century. Although we found a small number of Bd-infections prior to 1970, these showed no sign of spread or increase in infection prevalence over multiple decades. After the late 1970s, when mass die offs were first noted, our data show Bd as much more prevalent and more spatially spread out, suggesting epizootic spread. However, across the ~400km² area, we found no evidence of a wave-like pattern, but instead discovered multiple, nearly-simultaneous invasions within regions. We found that Bd invaded and spread in the central Sierra Nevada (Yosemite National Park area) about four decades before it invaded and spread in the southern Sierra Nevada (Sequoia and Kings Canyon National Parks area), and suggest that the temporal pattern of pathogen invasion may help explain divergent contemporary host pathogen dynamics.