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USGS2014

Using cure models for analyzing the influence of pathogens on salmon survival

Parasites and pathogens influence the size and stability of wildlife populations, yet many population models ignore the population-level effects of pathogens. Standard survival analysis methods (e.g., accelerated failure time models) are used to assess how survival rates are influenced by disease. However, they assume that each individual is equally susceptible and will eventually experience the event of interest; this assumption is not typically satisfied with regard to pathogens of wildlife populations. In contrast, mixture cure models, which comprise logistic regression and survival analysis components, allow for different covariates to be entered into each part of the model and provide better predictions of survival when a fraction of the population is expected to survive a disease outbreak. We fitted mixture cure models to the host–pathogen dynamics of Chinook Salmon Oncorhynchus tshawytscha and Coho Salmon O. kisutch and the myxozoan parasite Ceratomyxa shasta . Total parasite concentration, water temperature, and discharge were used as covariates to predict the observed parasite-induced mortality in juvenile salmonids collected as part of a long-term monitoring program in the Klamath River, California. The mixture cure models predicted the observed total mortality well, but some of the variability in observed mortality rates was not captured by the models. Parasite concentration and water temperature were positively associated with total mortality and the mortality rate of both Chinook Salmon and Coho Salmon. Discharge was positively associated with total mortality for both species but only affected the mortality rate for Coho Salmon. The mixture cure models provide insights into how daily survival rates change over time in Chinook Salmon and Coho Salmon after they become infected with C. shasta .

Oregon, California↗

USGS2019

Epidemic growth rates and host movement patterns shape management performance for pathogen spillover at the wildlife-livestock interface

Managing pathogen spillover at the wildlife–livestock interface is a key step towards improving global animal health, food security and wildlife conservation. However, predicting the effectiveness of management actions across host–pathogen systems with different life histories is an on-going challenge since data on intervention effectiveness are expensive to collect and results are system-specific. We developed a simulation model to explore how the efficacies of different management strategies vary according to host movement patterns and epidemic growth rates. The model suggested that fast-growing, fast-moving epidemics like avian influenza were best-managed with actions like biosecurity or containment, which limited and localized overall spillover risk. For fast-growing, slower-moving diseases like foot-and-mouth disease, depopulation or prophylactic vaccination were competitive management options. Many actions performed competitively when epidemics grew slowly and host movements were limited, and how management efficacy related to epidemic growth rate or host movement propensity depended on what objective was used to evaluate management performance. This framework offers one means of classifying and prioritizing responses to novel pathogen spillover threats, and evaluating current management actions for pathogens emerging at the wildlife–livestock interface.

Philosophical Transactions of the Royal Society A:↗

USGS2018

Inferring epidemiologic dynamics from viral evolution: 2014–2015 Eurasian/North American highly pathogenic avian influenza viruses exceed transmission threshold, R0 = 1, in wild birds and poultry in North America

Highly pathogenic avian influenza virus (HPAIV) is a multihost pathogen with lineages that pose health risks for domestic birds, wild birds, and humans. One mechanism of intercontinental HPAIV spread is through wild bird reservoirs, and wild birds were the likely sources of a Eurasian (EA) lineage HPAIV into North America in 2014. The introduction resulted in several reassortment events with North American (NA) lineage low-pathogenic avian influenza viruses and the reassortant EA/NA H5N2 went on to cause one of the largest HPAIV poultry outbreaks in North America. We evaluated three hypotheses about novel HPAIV introduced into wild and domestic bird hosts: (i) transmission of novel HPAIVs in wild birds was restricted by mechanisms associated with highly pathogenic phenotypes; (ii) the HPAIV poultry outbreak was not self-sustaining and required viral input from wild birds; and (iii) reassortment of the EA H5N8 generated reassortant EA/NA AIVs with a fitness advantage over fully Eurasian lineages in North American wild birds. We used a time-rooted phylodynamic model that explicitly incorporated viral population dynamics with evolutionary dynamics to estimate the basic reproductive number ( R 0 ) and viral migration among host types in domestic and wild birds, as well as between the EA H5N8 and EA/NA H5N2 in wild birds. We did not find evidence to support hypothesis (i) or (ii) as our estimates of the transmission parameters suggested that the HPAIV outbreak met or exceeded the threshold for persistence in wild birds ( R 0 > 1) and poultry ( R 0 ≈ 1) with minimal estimated transmission among host types. There was also no evidence to support hypothesis (iii) because R 0 values were similar among EA H5N8 and EA/NA H5N2 in wild birds. Our results suggest that this novel HPAIV and reassortments did not encounter any transmission barriers sufficient to prevent persistence when introduced to wild or domestic birds.

Evolutionary Applications↗

USGS2012

Gene flow and pathogen transmission among bobcats (Lynx rufus) in a fragmented urban landscape

Urbanization can result in the fragmentation of once contiguous natural landscapes into a patchy habitat interspersed within a growing urban matrix. Animals living in fragmented landscapes often have reduced movement among habitat patches because of avoidance of intervening human development, which potentially leads to both reduced gene flow and pathogen transmission between patches. Mammalian carnivores with large home ranges, such as bobcats (Lynx rufus), may be particularly sensitive to habitat fragmentation. We performed genetic analyses on bobcats and their directly transmitted viral pathogen, feline immunodeficiency virus (FIV), to investigate the effects of urbanization on bobcat movement. We predicted that urban development, including major freeways, would limit bobcat movement and result in genetically structured host and pathogen populations. We analysed molecular markers from 106 bobcats and 19 FIV isolates from seropositive animals in urban southern California. Our findings indicate that reduced gene flow between two primary habitat patches has resulted in genetically distinct bobcat subpopulations separated by urban development including a major highway. However, the distribution of genetic diversity among FIV isolates determined through phylogenetic analyses indicates that pathogen genotypes are less spatially structured--exhibiting a more even distribution between habitat fragments. We conclude that the types of movement and contact sufficient for disease transmission occur with enough frequency to preclude structuring among the viral population, but that the bobcat population is structured owing to low levels of effective bobcat migration resulting in gene flow. We illustrate the utility in using multiple molecular markers that differentially detect movement and gene flow between subpopulations when assessing connectivity.

California↗

USGS2011

Forest species diversity reduces disease risk in a generalist plant pathogen invasion

Empirical evidence suggests that biodiversity loss can increase disease transmission, yet our understanding of the 'diversity-disease hypothesis' for generalist pathogens in natural ecosystems is limited. We used a landscape epidemiological approach to examine two scenarios regarding diversity effects on the emerging plant pathogen Phytophthora ramorum across a broad, heterogeneous ecoregion: (1) an amplification effect exists where disease risk is greater in areas with higher plant diversity due to the pathogen's wide host range, or (2) a dilution effect where risk is reduced with increasing diversity due to lower competency of alternative hosts. We found evidence for pathogen dilution, whereby disease risk was lower in sites with higher species diversity, after accounting for potentially confounding effects of host density and landscape heterogeneity. Our results suggest that although nearly all plants in the ecosystem are hosts, alternative hosts may dilute disease transmission by competent hosts, thereby buffering forest health from infectious disease.

Ecology Letters↗

USGS2003

Pathogenic human viruses in coastal waters

This review addresses both historical and recent investigations into viral contamination of marine waters. With the relatively recent emergence of molecular biology-based assays, a number of investigations have shown that pathogenic viruses are prevalent in marine waters being impacted by sewage. Research has shown that this group of fecal-oral viral pathogens (enteroviruses, hepatitis A viruses, Norwalk viruses, reoviruses, adenoviruses, rotaviruses, etc.) can cause a broad range of asymptomatic to severe gastrointestinal, respiratory, and eye, nose, ear, and skin infections in people exposed through recreational use of the water. The viruses and the nucleic acid signature survive for an extended period in the marine environment. One of the primary concerns of public health officials is the relationship between the presence of pathogens and the recreational risk to human health in polluted marine environments. While a number of studies have attempted to address this issue, the relationship is still poorly understood. A contributing factor to our lack of progress in the field has been the lack of sensitive methods to detect the broad range of both bacterial and viral pathogens. The application of new and advanced molecular methods will continue to contribute to our current state of knowledge in this emerging and

Clinical Microbiology Reviews↗

USGS2021

Surveillance for diseases, pathogens, and toxicants of muskrat (Ondatra zibethicus) in Pennsylvania and surrounding regions

Using diagnostic data and contemporary sampling efforts, we conducted surveillance for a diversity of pathogens, toxicants, and diseases of muskrats ( Ondatra zibethicus ). Between 1977 and 2019, 26 diagnostic cases were examined from Kansas and throughout the Southeast and Mid-Atlantic, USA. We identified multiple causes of mortality in muskrats, but trauma (8/26), Tyzzer’s disease (5/6), and cysticercosis (5/26) were the most common. We also conducted necropsies, during November 2018—January 2019 Pennsylvania muskrat trapping season, on 380 trapper-harvested muskrat carcasses after the pelt was removed. Tissue samples and exudate were tested for presence of or exposure to a suite of pathogens and contaminants. Gastrointestinal tracts were examined for helminths. Intestinal helminths were present in 39.2% of necropsied muskrats, with Hymenolepis spp. (62%) and echinostome spp. (44%) being the most common Molecular testing identified a low prevalence of infection with Clostridium piliforme in the feces and Sarcocystis spp. in the heart. We detected a low seroprevalence to Toxoplasma gondii (1/380). No muskrats were positive for Francisella tularensis or Babesia spp. Cysticercosis was detected in 20% (5/26) of diagnostic cases and 15% (57/380) of our trapper-harvested muskrats. Toxic concentrations of arsenic, cadmium, lead, or mercury were not detected in tested liver samples. Copper, molybdenum, and zinc concentrations were detected at acceptable levels comparative to previous studies. Parasite intensity and abundance were typical of historic reports; however, younger muskrats had higher intensity of infection than older muskrats which is contradictory to what has been previously reported. A diversity of pathogens and contaminants have been reported from muskrats, but the associated disease impacts are poorly understood. Our data are consistent with historic reports and highlight the wide range of parasites, pathogens and contaminants harbored by muskrats in Pennsylvania. The data collected are a critical component in assessing overall muskrat health and serve as a basis for understanding the impacts of disease on recent muskrat population declines.

Pennsylvania↗

USGS2008

Recovery of a fish pathogenic bacterium, Aeromonas salmonicida, from ebonyshell mussels Fusconaia ebena using nondestructive sample collection procedures

Refugia are increasingly being used to maintain and propagate imperiled freshwater mussels for future population augmentations. Success for this endeavor is dependent on good husbandry, including a holistic program of resource health management. A significant aspect to optimal health is the prevention or control of infectious diseases. Describing and monitoring pathogens and diseases in mussels involves examination of tissues or samples collected from an appropriate number of individuals that satisfies a certain confidence level for expected prevalences of infections. In the present study, ebonyshell mussels Fusconaia ebena were infected with a fish pathogenic bacterium, Aeromonas salmonicida, through their cohabitation with diseased brook trout Salvelinus fontinalis. At a 100% prevalence of infection, the F. ebena were removed from the cohabitation tank to clean tanks that were supplied with pathogen-free water, which initiated their depuration of A. salmonicida. Three samples (nondestructive fluid, mantle, hemolymph) collected using nondestructive procedures were compared with fluids and soft tissue homogenates collected after sacrificing the mussels for recovery of the bacterium during this period of depuration. Nondestructive sample collections, especially ND fluid, provide a comparable alternative to sacrificing mussels to determine pathogen status.

Journal of Shellfish Research↗

USGS2012

AquaPathogen X--A template database for tracking field isolates of aquatic pathogens

AquaPathogen X is a template database for recording information on individual isolates of aquatic pathogens and is available for download from the U.S. Geological Survey (USGS) Western Fisheries Research Center (WFRC) website (http://wfrc.usgs.gov). This template database can accommodate the nucleotide sequence data generated in molecular epidemiological studies along with the myriad of abiotic and biotic traits associated with isolates of various pathogens (for example, viruses, parasites, or bacteria) from multiple aquatic animal host species (for example, fish, shellfish, or shrimp). The simultaneous cataloging of isolates from different aquatic pathogens is a unique feature to the AquaPathogen X database, which can be used in surveillance of emerging aquatic animal diseases and clarification of main risk factors associated with pathogen incursions into new water systems. As a template database, the data fields are empty upon download and can be modified to user specifications. For example, an application of the template database that stores the epidemiological profiles of fish virus isolates, called Fish ViroTrak (fig. 1), was also developed (Emmenegger and others, 2011).

Fact Sheet↗

USGS2003

Chapter A7. Section 7.3. Protozoan Pathogens

Protozoan pathogens are widely distributed in the aquatic environment. Cryptosporidium and Giardia are the principal protozoan pathogens that are known to affect the acceptability of water supplies for public use within the United States. A sampling program for protozoan pathogens should be conducted over an extended period of time because of cyclical and seasonal variations in their concentrations in the environment. This report provides information on the equipment, sampling protocols, and laboratory method that are in standard use by U.S. Geological Survey (USGS) personnel for the collection of data on protozoan pathogens. Each chapter of the National Field Manual is published separately and revised periodically. Newly published and revised chapters will be announced on the USGS Home Page on the World Wide Web under 'New Publications of the U.S. Geological Survey.'

Techniques of Water-Resources Investigations↗

USGS2020

A review of pathogens, diseases, and contaminants of muskrats (Ondatra zibethicus) in North America

Over the last 50 years, significant muskrat (Ondatra zibethicus) harvest declines have been observed throughout North America. Several theories for the decline have been proposed, including increased parasite infections and disease within muskrat populations. No existing wholistic review of muskrat exposure to pathogens, contaminants, and diseases exists. To address this knowledge gap, we conducted a thorough review of existing literature on muskrat pathogens, contaminants, and diseases across their natural range. This review is comprised of 129 articles from 1915-2019and from 27 U.S. states and 9 Canadian provinces. A wide diversity of contaminants, toxins, and pathogens were reported in muskrats, with the most common diseases being cysticercosis, tularemia, Tyzzer’s disease, and biotoxin poisoning from cyanobacteria. This review provides a summary of muskrat pathogens, contaminants, and disease over a century that has observed significant population declines throughout the species’ range in North America. Such data provides baseline data for understanding the potential role of disease in these declines. In addition, these data highlight critical knowledge gaps that warrant future research efforts.

Alaska, Alberta, British Columbia, Colorado, Idaho↗

USGS2019

Pathogen prevalence in American black bears (Ursus americanus) of the Jemez Mountains, New Mexico, USA

Informed management of American black bears ( Ursus americanus ) requires knowledge of the distribution and pathology of diseases affecting the species. Little information is available on pathogen prevalence from black bear populations in the Southwest, US, and it is unknown how these infections may influence black bear populations or disease transmission. We captured New Mexico black bears ( Ursus americanus amblyceps ) during 2016–17 as part of a long-term monitoring project and opportunistically collected 36 blood samples from 12 female and 17 male black bears. We wanted to determine prior exposure to canine distemper virus, canine parvovirus, Yersinia pestis , Francisella tularensis , West Nile virus, Toxoplasma gondii , and the tick-borne pathogens, Anaplasma spp., Ehrlichia spp., Borrelia burgdorferi , Rickettsia spp., and Babesia spp. Approximately half (55%, 16/29) of the individuals sampled had antibodies to Y. pestis , and 37% (10/27) had antibodies to T. gondii . Prevalence of antibodies to West Nile virus, F. tularensis , and canine parvovirus were lower (i.e., 11, 10, and 3%, respectively). We detected no antibodies to canine distemper, B. burgdorferi , Rickettsia spp., or Babesia spp. We documented changes in antibody titer levels for both sexes of several recaptured black bears. Our data will inform managers of pathogen prevalence and distribution in black bears in north-central New Mexico and provide a vital baseline dataset for future pathogen monitoring. Additionally, these data support actions to minimize exposure through handling wild individuals or through hunter harvest activities.

New Mexico↗

USGS2008

Pathogens associated with native and exotic trout populations in Shenandoah National Park and the relationships to fish stocking practices

Restrictive fish stocking policies in National Parks were developed as early as 1936 in order to preserve native fish assemblages and historic genetic diversity. Despite recent efforts to understand the effects of non-native or exotic fish introductions, park managers have limited information regarding the effects of these introductions on native fish communities. Shenandoah National Park was established in 1936 and brook trout (Salvelinus fontinalis) restoration within selected streams in the park began in 1937 in collaboration with the Virginia Department of Game and Inland Fisheries (VDGIF). An analysis of tissue samples from brook, brown (Salmo trutta), and rainbow trout (Oncorhynchus mykiss) from 29 streams within the park from 1998–2002 revealed the presence of Renibacterium salmoninarum, Yersinia ruckeri, and infectious pancreatic necrosis virus (IPNv). In order to investigate the relationships of the occurrence of fish pathogens with stocking histories we classified the streams into three categories: 1) streams with no record of stocking, 2) streams that are known to have been stocked historically, and 3) streams that were historically stocked within the park and continue to be stocked downstream of the park boundary. The occurrences of pathogens were summarized relative to this stocking history. Renibacterium salmoninarum, the causative agent of bacterial kidney disease, was the most prevalent pathogen found, occurring in all three species and stream stocking categories, and appears to be endemic to the park. Two other pathogens, Yersinia ruckeri and infectious pancreatic necrosis virus were also described from brook trout populations within the park. IPNv was only found in brook trout populations in streams with prior stocking histories. Yersinia ruckeri was only found in brook trout in steams that have never been stocked and like R. salmoninarum, is likely endemic.

Virginia↗

USGS2017

Design- and model-based recommendations for detecting and quantifying an amphibian pathogen in environmental samples

Accurate pathogen detection is essential for developing management strategies to address emerging infectious diseases, an increasingly prominent threat to wildlife. Sampling for free-living pathogens outside of their hosts has benefits for inference and study efficiency, but is still uncommon. We used a laboratory experiment to evaluate the influences of pathogen concentration, water type, and qPCR inhibitors on the detection and quantification of Batrachochytrium dendrobatidis ( Bd ) using water filtration. We compared results pre- and post-inhibitor removal, and assessed inferential differences when single versus multiple samples were collected across space or time. We found that qPCR inhibition influenced both Bd detection and quantification in natural water samples, resulting in biased inferences about Bd occurrence and abundance. Biases in occurrence could be mitigated by collecting multiple samples in space or time, but biases in Bd quantification were persistent. Differences in Bd concentration resulted in variation in detection probability, indicating that occupancy modeling could be used to explore factors influencing heterogeneity in Bd abundance among samples, sites, or over time. Our work will influence the design of studies involving amphibian disease dynamics and studies utilizing environmental DNA (eDNA) to understand species distributions.

Ecolology and Evolution↗

USGS2021

Genomic association with pathogen carriage in bighorn sheep (Ovis canadensis)

Genetic composition can influence host susceptibility to, and transmission of, pathogens, with potential population‐level consequences. In bighorn sheep ( Ovis canadensis ), pneumonia epidemics caused by Mycoplasma ovipneumoniae have been associated with severe population declines and limited recovery across North America. Adult survivors either clear the infection or act as carriers that continually shed M. ovipneumoniae and expose their susceptible offspring, resulting in high rates of lamb mortality for years following the outbreak event. Here, we investigated the influence of genomic composition on persistent carriage of M. ovipneumoniae in a well‐studied bighorn sheep herd in the Wallowa Mountains of Oregon, USA. Using 10,605 SNPs generated using RADseq technology for 25 female bighorn sheep, we assessed genomic diversity metrics and employed family‐based genome‐wide association methodologies to understand variant association and genetic architecture underlying chronic carriage. We observed no differences among genome‐wide diversity metrics (heterozygosity and allelic richness) between groups. However, we identified two variant loci of interest and seven associated candidate genes, which may influence carriage status. Further, we found that the SNP panel explained ~55% of the phenotypic variance (SNP‐based heritability) for M. ovipneumoniae carriage, though there was considerable uncertainty in these estimates. While small sample sizes limit conclusions drawn here, our study represents one of the first to assess the genomic factors influencing chronic carriage of a pathogen in a wild population and lays a foundation for understanding genomic influence on pathogen persistence in bighorn sheep and other wildlife populations. Future research should incorporate additional individuals as well as distinct herds to further explore the genomic basis of chronic carriage.

Oregon↗

USGS2020

Possible control of acute outbreaks of a marine fungal pathogen by nominally herbivorous tropical reef fish

Primary producers in terrestrial and marine systems can be affected by fungal pathogens threatening the provision of critical ecosystem services. Crustose coralline algae (CCA) are ecologically important members of tropical reef systems and are impacted by coralline fungal disease (CFD) which manifests as overgrowth of the CCA crust by fungal lesions causing partial to complete mortality of the CCA host. No natural controls for CFD have been identified, but nominally herbivorous fish could play a role by consuming pathogenic fungi. We documented preferential grazing on fungal lesions by adults of six common reef-dwelling species of herbivorous Acanthuridae and Labridae, (surgeonfish and parrotfish) which collectively demonstrated an ~ 80-fold higher grazing rate on fungal lesions relative to their proportionate benthic coverage, and a preference for lesions over other palatable substrata (e.g. live scleractinian coral, CCA, or algae). Furthermore, we recorded a ~ 600% increase in live CFD lesion size over an approximately 2-week period when grazing by herbivorous fish was experimentally excluded suggesting that herbivorous reef fish could control CFD progression by directly reducing biomass of the fungal pathogen. Removal rates may be sufficient to allow CCA to recover from infection and explain historically observed natural waning behaviour after an outbreak. Thus, in addition to their well-known role as determinants of macroalgal overgrowth of reefs, herbivorous fish could thus also be important in control of diseases affecting crustose coralline algae that stabilize the foundation of coral reef substrata.

Palmyra Atoll National Wildlife Refuge↗

USGS2022

Environmental monitoring for invasive fungal pathogens of ʽŌhiʽa (Metrosideros polymorpha) on the Island of Hawaiʽi

The invasive rust Austropuccina psidii was detected in the Hawaiian Islands in 2005 and has become widely established throughout the archipelago in both native and introduced species of Myrtaceae. Initial predictions about the impacts of the fungus on native ʽōhiʽa lehua ( Metrosideros polymorpha ), a keystone native tree, have not materialized, but there is ongoing concern that introductions of new genotypes of the fungus could lead to widespread mortality with catastrophic effects on native ecosystems. By contrast, two recently emergent Ascomycete pathogens, Ceratocystis lukuohia ( Ceratocystis wilt of ‘ōhi‘a) and C. huliohia ( Ceratocystis canker of ‘ōhi‘a), collectively known to cause Rapid ʽŌhiʽa Death (ROD), are causing significant mortality in native forests on Hawaiʻi and Kauaʻi Islands, but pathways of spread are still incompletely understood. We used a network of passive environmental samplers for collecting windblown urediniospores of Austropuccina to evaluate the effectiveness of environmental monitoring to detect seasonal and landscape-scale differences in airborne propagules of this rust on Hawai`i Island. The samplers were also used to determine if windborn ambrosia beetle frass or spores of Ceratocystis can spread long distances. We found frequent detections and regional and seasonal differences in numbers of samplers that were positive for urediniospores of Austropuccinia , but little evidence of long-distance airborne dispersal of the ROD-causing fungi. The simple, inexpensive platform for sampling airborne fungal spores that we used may have value as a monitoring tool for detecting spread of airborne fungal pathogens, evaluating habitats for suitability for restoration efforts, and for detecting new pathogen introductions, particularly new Austropuccinia genotypes both in Hawaiʻi and other parts of the world.

Hawaii↗

USGS2019

Contrasting demographic responses of toad populations to regionally synchronous pathogen (Batrachochytrium dendrobatidis) dynamics

Batrachochytrium dendrobatidis (Bd), a fungal pathogen that causes amphibian chytridiomycosis, has been implicated in population declines globally. To better understand how Bd affects survival and how threats vary spatially and temporally, we conducted long-term (range: 9–13 yrs) capture-recapture studies of boreal toads ( Anaxyrus boreas ) from three similar communities in western Montana. We also estimated temporal and spatial variation in population-level Bd prevalence among populations and the potential role of co-occurring Columbia spotted frogs ( Rana luteiventris ) in driving infection dynamics. Hierarchical models that accounted for detection uncertainty revealed Bd reduced apparent survival in one population that declined, was unassociated with survival in one stationary population, and was associated with increased survival in one population that is near extirpation. Despite different effects of Bd on hosts, pathogen prevalence was similar and synchronous across the populations separated by 111–176 km. Variation in Bd prevalence was driven partly by seasonal temperatures, but opposite the direction expected. Bd prevalence also decreased sharply over time across all populations, unrelated to trends in temperature, boreal toad survival, or infection dynamics of co-occurring Columbia spotted frogs. Toad Bd prevalence increased when frog abundance was high, consistent with an amplification effect. However, Bd prevalence of toads decreased as Bd prevalence of spotted frogs increased, consistent with a dilution effect. Our results reveal surprising variation in responses to Bd and show pathogen prevalence is not predictive of survival or population risk, and they illustrate the complexity in understanding disease dynamics across multiple populations.

Western Montana↗