Epidemiological modeling of SARS-CoV-2 in white-tailed deer (Odocoileus virginianus) reveals conditions for introduction and widespread transmission.

Emerging infectious diseases with zoonotic potential often have complex socioecological dynamics and limited ecological data, requiring integration of epidemiological modeling with surveillance. Although our understanding of SARS-CoV-2 has advanced considerably since its detection in late 2019, the factors influencing its introduction and transmission in wildlife hosts, particularly white-tailed deer (Odocoileus virginianus), remain poorly understood. We use a Susceptible-Infected-Recovered-Susceptible epidemiological model to investigate the spillover risk and transmission dynamics of SARS-CoV-2 in wild and captive white-tailed deer populations across various simulated scenarios. We found that captive scenarios pose a higher risk of SARS-CoV-2 introduction from humans into deer herds and subsequent transmission among deer, compared to wild herds. However, even in wild herds, the transmission risk is often substantial enough to sustain infections. Furthermore, we demonstrate that the strength of introduction from humans influences outbreak characteristics only to a certain extent. Transmission among deer was frequently sufficient for widespread outbreaks in deer populations, regardless of the initial level of introduction. We also explore the potential for fence line interactions between captive and wild deer to elevate outbreak metrics in wild herds that have the lowest risk of introduction and sustained transmission. Our results indicate that SARS-CoV-2 could be introduced and maintained in deer herds across a range of circumstances based on testing a range of introduction and transmission risks in various captive and wild scenarios. Our approach and findings will aid One Health strategies that mitigate persistent SARS-CoV-2 outbreaks in white-tailed deer populations and potential spillback to humans.

Quantitative support for the benefits of proactive management for wildlife disease control.

Finding effective pathogen mitigation strategies is one of the biggest challenges humans face today. In the context of wildlife, emerging infectious diseases have repeatedly caused widespread host morbidity and population declines of numerous taxa. In areas yet unaffected by a pathogen, a proactive management approach has the potential to minimize or prevent host mortality. However, typically critical information on disease dynamics in a novel host system is lacking, empirical evidence on efficacy of management interventions is limited, and there is a lack of validated predictive models. As such, quantitative support for identifying effective management interventions is largely absent, and the opportunity for proactive management is often missed. We considered the potential invasion of the chytrid fungus, Batrachochytrium salamandrivorans (Bsal), whose expected emergence in North America poses a severe threat to hundreds of salamander species in this global salamander biodiversity hotspot. We developed and parameterized a dynamic multistate occupancy model to forecast host and pathogen occurrence, following expected emergence of the pathogen, and evaluated the response of salamander populations to different management scenarios. Our model forecasted that taking no action is expected to be catastrophic to salamander populations. Proactive action was predicted to maximize host occupancy outcomes relative to wait-and-see reactive management, thus providing quantitative support for proactive management opportunities. The eradication of Bsal was unlikely under all the evaluated management options. Contrary to our expectations, even early pathogen detection had little effect on Bsal or host occupancy outcomes. Our results provide quantitative support that proactive management is the optimal strategy for promoting persistence of disease-threatened salamander populations. Our approach fills a critical gap by defining a framework for evaluating management options prior to pathogen invasion and can thus serve as a template for addressing novel disease threats that jeopardize wildlife and human health.

Apoyo cuantitativo para los beneficios de la gestión proactiva del control de enfermedades silvestres Resumen Uno de los mayores retos en la actualidad es encontrar estrategias eficaces de mitigación de patógenos. En el contexto de la fauna silvestre, las enfermedades infecciosas emergentes han causado en varias ocasiones una morbilidad generalizada de los hospedadores y el declive de las poblaciones de numerosos taxones. En zonas aún no afectadas por un patógeno, un enfoque de gestión proactivo tiene el potencial de minimizar o prevenir la mortalidad de los hospederos. Sin embargo, en general se carece de información crítica sobre la dinámica de la enfermedad en el nuevo sistema huésped, las pruebas empíricas sobre la eficacia de las intervenciones de gestión son limitadas y faltan modelos predictivos validados. Por lo tanto, no existe un apoyo cuantitativo para identificar intervenciones de gestión eficaces y a menudo se pierde la oportunidad de una gestión proactiva. Consideramos la posible invasión del hongo quitridio Batrachochytrium salamandrivorans (Bsal), cuya aparición prevista en América del Norte supone una grave amenaza para cientos de especies de salamandras en este punto caliente de la biodiversidad mundial de salamandras. Desarrollamos y parametrizamos un modelo dinámico de ocupación multiestado para predecir la presencia de hospederos y patógenos, tras la aparición esperada del patógeno, y evaluamos la respuesta de las poblaciones de salamandras a diferentes escenarios de gestión. Nuestro modelo predijo que no tomar ninguna medida sería catastrófico para las poblaciones de salamandras. También predijo que la acción proactiva maximizaría los resultados de ocupación de hospederos en relación con la gestión reactiva de esperar y ver, proporcionando así un apoyo cuantitativo a las oportunidades de gestión proactiva. La erradicación de Bsal fue improbable bajo todas las opciones de gestión evaluadas. Contrariamente a nuestras expectativas, incluso la detección temprana del patógeno tuvo poco efecto sobre los resultados de ocupación de Bsal o del hospedador. Nuestros resultados apoyan cuantitativamente a la gestión proactiva como la estrategia óptima para promover la persistencia de poblaciones de salamandras amenazadas por la enfermedad. Nuestro enfoque llena un vacío crítico al definir un marco para evaluar las opciones de gestión antes de la invasión de patógenos y, por lo tanto, puede servir como plantilla para hacer frente a nuevas amenazas de enfermedades que ponen en peligro la vida silvestre y la salud humana.

Reframing wildlife disease management problems with decision analysis.

Contemporary wildlife disease management is complex because managers need to respond to a wide range of stakeholders, multiple uncertainties, and difficult trade-offs that characterize the interconnected challenges of today. Despite general acknowledgment of these complexities, managing wildlife disease tends to be framed as a scientific problem, in which the major challenge is lack of knowledge. The complex and multifactorial process of decision-making is collapsed into a scientific endeavor to reduce uncertainty. As a result, contemporary decision-making may be oversimplified, rely on simple heuristics, and fail to account for the broader legal, social, and economic context in which the decisions are made. Concurrently, scientific research on wildlife disease may be distant from this decision context, resulting in information that may not be directly relevant to the pertinent management questions. We propose reframing wildlife disease management challenges as decision problems and addressing them with decision analytical tools to divide the complex problems into more cognitively manageable elements. In particular, structured decision-making has the potential to improve the quality, rigor, and transparency of decisions about wildlife disease in a variety of systems. Examples of management of severe acute respiratory syndrome coronavirus 2, white-nose syndrome, avian influenza, and chytridiomycosis illustrate the most common impediments to decision-making, including competing objectives, risks, prediction uncertainty, and limited resources.

Replanteamiento del manejo de problemas por enfermedades de fauna mediante el análisis de decisiones Resumen El manejo actual de las enfermedades de la fauna es complejo debido a que los gestores necesitan responder a una amplia gama de actores, varias incertidumbres y compensaciones difíciles que caracterizan los retos interconectados del día de hoy. A pesar de que en general se reconocen estas complejidades, el manejo de las enfermedades tiende a plantearse como un problema científico en el que el principal obstáculo es la falta de conocimiento. El proceso complejo y multifactorial de la toma decisiones está colapsado dentro de un esfuerzo científico para reducir la incertidumbre. Como resultado de esto, las decisiones contemporáneas pueden estar simplificadas en exceso, depender de métodos heurísticos simples y no considerar el contexto legal, social y económico más amplio en el que se toman las decisiones. De manera paralela, las investigaciones científicas sobre las enfermedades de la fauna pueden estar lejos de este contexto de decisiones, lo que deriva en información que puede no ser directamente relevante para las preguntas pertinentes de manejo. Proponemos replantear los obstáculos para el manejo de enfermedades de fauna como problemas de decisión y abordarlos con herramientas analíticas de decisión para dividir los problemas complejos en elementos más manejables de manera cognitiva. En particular, las decisiones estructuradas tienen el potencial de mejorar la calidad, el rigor y la transparencia de las decisiones sobre las enfermedades de la fauna en una variedad de sistemas. Ejemplos como el manejo del coronavirus del síndrome de respiración agudo tipo 2, el síndrome de nariz blanca, la influenza aviar y la quitridiomicosis ilustran los impedimentos más comunes para la toma de decisiones, incluyendo los objetivos en competencia, riesgos, incertidumbre en las predicciones y recursos limitados.

Assessing amphibian disease risk across tropical streams while accounting for imperfect pathogen detection.

Ecologists studying emerging wildlife diseases need to confront the realism of imperfect pathogen detection across heterogeneous habitats to aid in conservation decisions. For example, spatial risk assessments of amphibian disease caused by Batrachochytrium dendrobatidis (Bd) has largely ignored imperfect pathogen detection across sampling sites. Because changes in pathogenicity and host susceptibility could trigger recurrent population declines, it is imperative to understand how pathogen prevalence and occupancy vary across environmental gradients. Here, we assessed how Bd occurrence, prevalence, and infection intensity in a diverse Neotropical landscape vary across streams in relation to abiotic and biotic predictors using a hierarchical Bayesian model that accounts for imperfect Bd detection caused by qPCR error. Our model indicated that the number of streams harboring Bd-infected frogs is higher than observed, with Bd likely being present at ~ 43% more streams than it was detected. We found that terrestrial-breeders captured along streams had higher Bd prevalence, but lower infection intensity, than aquatic-breeding species. We found a positive relationship between Bd occupancy probability and stream density, and a negative relationship between Bd occupancy probability and amphibian local richness. Forest cover was a weak predictor of Bd occurrence and infection intensity. Finally, we provide estimates for the minimum number of amphibian captures needed to determine the presence of Bd at a given site where Bd occurs, thus, providing guidence for cost-effective disease risk monitoring programs.

Diverse genotypes of the amphibian-killing fungus produce distinct phenotypes through plastic responses to temperature.

Phenotypes are the target of selection and affect the ability of organisms to persist in variable environments. Phenotypes can be influenced directly by genes and/or by phenotypic plasticity. The amphibian-killing fungus Batrachochytrium dendrobatidis (Bd) has a global distribution, unusually broad host range, and high genetic diversity. Phenotypic plasticity may be an important process that allows this pathogen to infect hundreds of species in diverse environments. We quantified phenotypic variation of nine Bd genotypes from two Bd lineages (Global Pandemic Lineage [GPL] and Brazil) and a hybrid (GPL-Brazil) grown at three temperatures (12, 18 and 24°C). We measured five functional traits including two morphological traits (zoospore and zoosporangium sizes) and three life history traits (carrying capacity, time to fastest growth and exponential growth rate) in a phylogenetic framework. Temperature caused highly plastic responses within each genotype, with all Bd genotypes showing phenotypic plasticity in at least three traits. Among genotypes, Bd generally showed the same direction of plastic response to temperature: larger zoosporangia, higher carrying capacity, longer time to fastest growth and slower exponential growth at lower temperatures. The exception was zoospore size, which was highly variable. Our findings indicate that Bd genotypes have evolved novel phenotypes through plastic responses to temperature over very short timescales. High phenotypic variability likely extends to other traits and may facilitate the large host range and rapid spread of Bd.

Eco-evolutionary rescue promotes host-pathogen coexistence.

Emerging infectious pathogens are responsible for some of the most severe host mass mortality events in wild populations. Yet, effective pathogen control strategies are notoriously difficult to identify, in part because quantifying and forecasting pathogen spread and disease dynamics is challenging. Following an outbreak, hosts must cope with the presence of the pathogen, leading to host-pathogen coexistence or extirpation. Despite decades of research, little is known about host-pathogen coexistence post-outbreak when low host abundances and cryptic species make these interactions difficult to study. Using a novel disease-structured N-mixture model, we evaluate empirical support for three host-pathogen coexistence hypotheses (source-sink, eco-evolutionary rescue, and spatial variation in pathogen transmission) in a Neotropical amphibian community decimated by Batrachochytrium dendrobatidis (Bd) in 2004. During 2010-2014, we surveyed amphibians in Parque Nacional G. D. Omar Torríjos Herrera, Coclé Province, El Copé, Panama. We found that the primary driver of host-pathogen coexistence was eco-evolutionary rescue, as evidenced by similar amphibian survival and recruitment rates between infected and uninfected hosts. Average apparent monthly survival rates of uninfected and infected hosts were both close to 96%, and the expected number of uninfected and infected hosts recruited (via immigration/reproduction) was less than one host per disease state per 20-m site. The secondary driver of host-pathogen coexistence was spatial variation in pathogen transmission as we found that transmission was highest in areas of low abundance but there was no support for the source-sink hypothesis. Our results indicate that changes in the host community (i.e., through genetic or species composition) can reduce the impacts of emerging infectious disease post-outbreak. Our disease-structured N-mixture model represents a valuable advancement for conservation managers trying to understand underlying host-pathogen interactions and provides new opportunities to study disease dynamics in remnant host populations decimated by virulent pathogens.

Antifungal Bacteria on Woodland Salamander Skin Exhibit High Taxonomic Diversity and Geographic Variability.

Diverse bacteria inhabit amphibian skin; some of those bacteria inhibit growth of the fungal pathogen Batrachochytrium dendrobatidis Yet there has been no systematic survey of anti-B. dendrobatidis bacteria across localities, species, and elevations. This is important given geographic and taxonomic variations in amphibian susceptibility to B. dendrobatidis Our collection sites were at locations within the Appalachian Mountains where previous sampling had indicated low B. dendrobatidis prevalence. We determined the numbers and identities of anti-B. dendrobatidis bacteria on 61 Plethodon salamanders (37 P. cinereus, 15 P. glutinosus, 9 P. cylindraceus) via culturing methods and 16S rRNA gene sequencing. We sampled co-occurring species at three localities and sampled P. cinereus along an elevational gradient (700 to 1,000 meters above sea level [masl]) at one locality. We identified 50 anti-B. dendrobatidis bacterial operational taxonomic units (OTUs) and found that the degree of B. dendrobatidis inhibition was not correlated with relatedness. Five anti-B. dendrobatidis bacterial strains occurred on multiple amphibian species at multiple localities, but none were shared among all species and localities. The prevalence of anti-B. dendrobatidis bacteria was higher at Shenandoah National Park (NP), VA, with 96% (25/26) of salamanders hosting at least one anti-B. dendrobatidis bacterial species compared to 50% (7/14) at Catoctin Mountain Park (MP), MD, and 38% (8/21) at Mt. Rogers National Recreation Area (NRA), VA. At the individual level, salamanders at Shenandoah NP had more anti-B. dendrobatidis bacteria per individual (µ = 3.3) than those at Catoctin MP (µ = 0.8) and at Mt. Rogers NRA (µ = 0.4). All salamanders tested negative for B. dendrobatidis Anti-B. dendrobatidis bacterial species are diverse in central Appalachian Plethodon salamanders, and their distribution varied geographically. The antifungal bacterial species that we identified may play a protective role for these salamanders.IMPORTANCE Amphibians harbor skin bacteria that can kill an amphibian fungal pathogen, Batrachochytrium dendrobatidis Some amphibians die from B. dendrobatidis infection, whereas others do not. The bacteria that can kill B. dendrobatidis, called anti-B. dendrobatidis bacteria, are thought to influence the B. dendrobatidis infection outcome for the amphibian. Yet how anti-B. dendrobatidis bacterial species vary among amphibian species and populations is unknown. We determined the distribution of anti-B. dendrobatidis bacterial species among three salamander species (n = 61) sampled at three localities. We identified 50 unique anti-B. dendrobatidis bacterial species and found that all of the tested salamanders were negative for B. dendrobatidis Five anti-B. dendrobatidis bacterial species were commonly detected, suggesting a stable, functional association with these salamanders. The number of anti-B. dendrobatidis bacteria per individual varied among localities but not among co-occurring salamander species, demonstrating that environment is more influential than host factors in structuring the anti-B. dendrobatidis bacterial community. These anti-B. dendrobatidis bacteria may serve a protective function for their salamander hosts.

Disassembly of a tadpole community by a multi-host fungal pathogen with limited evidence of recovery.

Emerging infectious diseases can cause host community disassembly, but the mechanisms driving the order of species declines and extirpations following a disease outbreak are unclear. We documented the community disassembly of a Neotropical tadpole community during a chytridiomycosis outbreak, triggered by the generalist fungal pathogen, Batrachochytrium dendrobatidis (Bd). Within the first 11 months of Bd arrival, tadpole density and occupancy rapidly declined. Species rarity, in terms of tadpole occupancy and adult relative abundance, did not predict the odds of tadpole occupancy declines. But species losses were taxonomically selective, with glassfrogs (Family: Centrolenidae) disappearing the fastest and tree frogs (Family: Hylidae) and dart-poison frogs (Family: Dendrobatidae) remaining the longest. We detected biotic homogenization of tadpole communities, with post-decline communities resembling one another more strongly than pre-decline communities. The entire tadpole community was extirpated within 22 months following Bd arrival, and we found limited signs of recovery within 10 years post-outbreak. Because of imperfect species detection inherent to sampling species-rich tropical communities and the difficulty of devising a single study design protocol to sample physically complex tropical habitats, we used simulations to provide recommendations for future surveys to adequately sample diverse Neotropical communities. Our unique data set on tadpole community composition before and after Bd arrival is a valuable baseline for assessing amphibian recovery. Our results are of direct relevance to conservation managers and community ecologists interested in understanding the timing, magnitude, and consequences of disease outbreaks as emerging infectious diseases spread globally.

Dead or alive? Viability of chytrid zoospores shed from live amphibian hosts.

Pathogens vary in virulence and rates of transmission because of many differences in the host, the pathogen, and their environment. The amphibian chytrid fungus, Batrachochytrium dendrobatidis (Bd), affects amphibian hosts differently, causing extinction and population declines in some species but having limited effects on others. Phenotypic differences in zoospore production rates among Bd lineages likely contribute to some of the variation observed among host responses, although no studies have quantified the viability of zoospores shed from live animals. We compared host survivorship, infection intensity, shedding rates, and zoospore viability between 2 species of endangered tropical frogs, Hylomantis lemur and Atelopus zeteki, when exposed to a highly virulent lineage of Bd (JEL 423). We applied a dye to zoospores 30 to 60 min following animal soaks, to estimate shedding rate and proportion of live zoospores shed by different species. The average infection intensity for A. zeteki was nearly 17 times higher (31,455 ± 10,103 zoospore genomic equivalents [ZGEs]) than that of H. lemur (1832 ± 1086 ZGEs), and A. zeteki died earlier than H. lemur. The proportion of viable zoospores was ~80% in both species throughout the experiment, although A. zeteki produced many more zoospores, suggesting it may play a disproportionate role in spreading disease in communities where it occurs, because the large number of viable zoospores they produce might increase infection in other species where they are reintroduced.