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.

Draft genome sequences of 21 Pedobacter strains isolated from amphibian specimens.

The genomes of 21 Pedobacter strains isolated from the European salamander Salamandra salamandra and different Madagascan frog species were sequenced using Illumina sequencing. Here, we report their draft genome sequences (~4.7-7.2 Mbp in size) to allow comparative genomics and taxonomic assignment of these strains.

One Health Approach to Globalizing, Accelerating, and Focusing Amphibian and Reptile Disease Research-Reflections and Opinions from the First Global Amphibian and Reptile Disease Conference.

The world's reptiles and amphibians are experiencing dramatic and ongoing losses in biodiversity, changes that can have substantial effects on ecosystems and human health. In 2022, the first Global Amphibian and Reptile Disease Conference was held, using One Health as a guiding principle. The conference showcased knowledge on numerous reptile and amphibian pathogens from several standpoints, including epidemiology, host immune defenses, wild population effects, and mitigation. The conference also provided field experts the opportunity to discuss and identify the most urgent herpetofaunal disease research directions necessary to address current and future threats to reptile and amphibian biodiversity.

Effects of exogenous elevation of corticosterone on immunity and the skin microbiome of eastern newts (Notophthalmus viridescens).

The amphibian chytrid fungus, Batrachochytrium salamandrivorans (Bsal) threatens salamander biodiversity. The factors underlying Bsal susceptibility may include glucocorticoid hormones (GCs). The effects of GCs on immunity and disease susceptibility are well studied in mammals, but less is known in other groups, including salamanders. We used Notophthalmus viridescens (eastern newts) to test the hypothesis that GCs modulate salamander immunity. We first determined the dose required to elevate corticosterone (CORT; primary GC in amphibians) to physiologically relevant levels. We then measured immunity (neutrophil lymphocyte ratios, plasma bacterial killing ability (BKA), skin microbiome, splenocytes, melanomacrophage centres (MMCs)) and overall health in newts following treatment with CORT or an oil vehicle control. Treatments were repeated for a short (two treatments over 5 days) or long (18 treatments over 26 days) time period. Contrary to our predictions, most immune and health parameters were similar for CORT and oil-treated newts. Surprisingly, differences in BKA, skin microbiome and MMCs were observed between newts subjected to short- and long-term treatments, regardless of treatment type (CORT, oil vehicle). Taken together, CORT does not appear to be a major factor contributing to immunity in eastern newts, although more studies examining additional immune factors are necessary. This article is part of the theme issue 'Amphibian immunity: stress, disease and ecoimmunology'.

Broad host susceptibility of North American amphibian species to Batrachochytrium salamandrivorans suggests high invasion potential and biodiversity risk.

Batrachochytrium salamandrivorans (Bsal) is a fungal pathogen of amphibians that is emerging in Europe and could be introduced to North America through international trade or other pathways. To evaluate the risk of Bsal invasion to amphibian biodiversity, we performed dose-response experiments on 35 North American species from 10 families, including larvae from five species. We discovered that Bsal caused infection in 74% and mortality in 35% of species tested. Both salamanders and frogs became infected and developed Bsal chytridiomycosis. Based on our host susceptibility results, environmental suitability conditions for Bsal, and geographic ranges of salamanders in the United States, predicted biodiversity loss is expected to be greatest in the Appalachian Region and along the West Coast. Indices of infection and disease susceptibility suggest that North American amphibian species span a spectrum of vulnerability to Bsal chytridiomycosis and most amphibian communities will include an assemblage of resistant, carrier, and amplification species. Predicted salamander losses could exceed 80 species in the United States and 140 species in North America.

Parental care contributes to vertical transmission of microbes in a skin-feeding and direct-developing caecilian.

BACKGROUND: Our current understanding of vertebrate skin and gut microbiomes, and their vertical transmission, remains incomplete as major lineages and varied forms of parental care remain unexplored. The diverse and elaborate forms of parental care exhibited by amphibians constitute an ideal system to study microbe transmission, yet investigations of vertical transmission among frogs and salamanders have been inconclusive. In this study, we assess bacteria transmission in Herpele squalostoma, an oviparous direct-developing caecilian in which females obligately attend juveniles that feed on their mother's skin (dermatophagy). RESULTS: We used 16S rRNA amplicon-sequencing of the skin and gut of wild caught H. squalostoma individuals (males, females, including those attending juveniles) as well as environmental samples. Sourcetracker analyses revealed that juveniles obtain an important portion of their skin and gut bacteria communities from their mother. The contribution of a mother's skin to the skin and gut of her respective juveniles was much larger than that of any other bacteria source. In contrast to males and females not attending juveniles, only the skins of juveniles and their mothers were colonized by bacteria taxa Verrucomicrobiaceae, Nocardioidaceae, and Erysipelotrichaceae. In addition to providing indirect evidence for microbiome transmission linked to parental care among amphibians, our study also points to noticeable differences between the skin and gut communities of H. squalostoma and that of many frogs and salamanders, which warrants further investigation. CONCLUSION: Our study is the first to find strong support for vertical bacteria transmission attributed to parental care in a direct-developing amphibian species. This suggests that obligate parental care may promote microbiome transmission in caecilians.

Inhibitory Bacterial Diversity and Mucosome Function Differentiate Susceptibility of Appalachian Salamanders to Chytrid Fungal Infection.

Mucosal defenses are crucial in animals for protection against pathogens and predators. Host defense peptides (antimicrobial peptides, AMPs) as well as skin-associated microbes are key components of mucosal immunity, particularly in amphibians. We integrate microbiology, molecular biology, network-thinking, and proteomics to understand how host and microbially derived products on amphibian skin (referred to as the mucosome) serve as pathogen defenses. We studied defense mechanisms against chytrid pathogens, Batrachochytrium dendrobatidis (Bd) and B. salamandrivorans (Bsal), in four salamander species with different Batrachochytrium susceptibilities. Bd infection was quantified using qPCR, mucosome function (i.e., ability to kill Bd or Bsal zoospores in vitro), skin bacterial communities using 16S rRNA gene amplicon sequencing, and the role of Bd-inhibitory bacteria in microbial networks across all species. We explored the presence of candidate-AMPs in eastern newts and red-backed salamanders. Eastern newts had the highest Bd prevalence and mucosome function, while red-back salamanders had the lowest Bd prevalence and mucosome function, and two-lined salamanders and seal salamanders were intermediates. Salamanders with highest Bd infection intensity showed greater mucosome function. Bd infection prevalence significantly decreased as putative Bd-inhibitory bacterial richness and relative abundance increased on hosts. In co-occurrence networks, some putative Bd-inhibitory bacteria were found as hub-taxa, with red-backs having the highest proportion of protective hubs and positive associations related to putative Bd-inhibitory hub bacteria. We found more AMP candidates on salamanders with lower Bd susceptibility. These findings suggest that salamanders possess distinct innate mechanisms that affect chytrid fungi. IMPORTANCE How host mucosal defenses interact, and influence disease outcome is critical in understanding host defenses against pathogens. A more detailed understanding is needed of the interactions between the host and the functioning of its mucosal defenses in pathogen defense. This study investigates the variability of chytrid susceptibility in salamanders and the innate defenses each species possesses to mediate pathogens, thus advancing the knowledge toward a deeper understanding of the microbial ecology of skin-associated bacteria and contributing to the development of bioaugmentation strategies to mediate pathogen infection and disease. This study improves the understanding of complex immune defense mechanisms in salamanders and highlights the potential role of the mucosome to reduce the probability of Bd disease development and that putative protective bacteria may reduce likelihood of Bd infecting skin.

Endemic Lineages of Batrachochytrium dendrobatidis Are Associated With Reduced Chytridiomycosis-Induced Mortality in Amphibians: Evidence From a Meta-Analysis of Experimental Infection Studies.

Emerging infectious wildlife diseases have caused devastating declines, particularly when pathogens have been introduced in naïve host populations. The outcome of disease emergence in any host population will be dictated by a series of factors including pathogen virulence, host susceptibility, and prior opportunity for coevolution between hosts and pathogens. Historical coevolution can lead to increased resistance in hosts and/or reduced virulence in endemic pathogens that allows stable persistence of host and pathogen populations. Adaptive coevolution may also occur on relatively short time scales following introduction of a novel pathogen. Here, we performed a meta-analysis of multi-strain Batrachochytrium dendrobatidis (Bd) infection experiments to test whether: (1) amphibian hosts exhibit lower mortality rates when infected with strains belonging to endemic Bd lineages relative to the Global Panzootic Lineage (Bd-GPL), hypothetically owing to long co-evolutionary histories between endemic Bd lineages and their amphibian hosts; and (2) amphibians exhibit lower mortality rates when infected with local Bd-GPL strains compared with non-local Bd-GPL strains, hypothetically owing to recent selection for tolerance or resistance to local Bd-GPL strains. We found that in a majority of cases, amphibians in endemic Bd treatments experienced reduced mortality relative to those in Bd-GPL treatments. Hosts presumed to have historically coexisted with endemic Bd did not show reduced mortality to Bd-GPL compared with hosts that have not historically coexisted with endemic Bd. Finally, we detected no overall difference in amphibian mortality between local and non-local Bd-GPL treatments. Taken together, our results suggest that long-term historical coexistence is associated with less disease-induced mortality potentially due to hypovirulence in endemic Bd lineages, and that more recent coexistence between amphibians and Bd-GPL has not yet resulted in reduced host susceptibility or pathogen virulence. This corroborates previous findings that Bd-GPL introduced via the global amphibian trade has a high capacity for causing disease-induced mortality.

An experimental test of disease resistance function in the skin-associated bacterial communities of three tropical amphibian species.

Variation in the structure of host-associated microbial communities has been correlated with the occurrence and severity of disease in diverse host taxa, suggesting a key role of the microbiome in pathogen defense. However, whether these correlations are typically a cause or consequence of pathogen exposure remains an open question, and requires experimental approaches to disentangle. In amphibians, infection by the fungal pathogen Batrachochytrium dendrobatidis (Bd) alters the skin microbial community in some host species, whereas in other species, the skin microbial community appears to mediate infection dynamics. In this study, we completed experimental Bd exposures in three species of tropical frogs (Agalychnis callidryas, Dendropsophus ebraccatus,andCraugastor fitzingeri) that were sympatric with Bd at the time of the study. For all three species, we identified key taxa within the skin bacterial communities that were linked to Bd infection dynamics. We also measured higher Bd infection intensities in D. ebraccatus and C. fitzingeri that were associated with higher mortality in C. fitzingeri. Our findings indicate that microbially mediated pathogen resistance is a complex trait that can vary within and across host species, and suggest that symbiont communities that have experienced prior selection for defensive microbes may be less likely to be disturbed by pathogen exposure.

Responsible biosecurity and risk mitigation for laboratory research on emerging pathogens of amphibians.

The increasing study of emerging wildlife pathogens and a lack of policy or legislation regulating their translocation and use has heightened concerns about laboratory escape, species spillover, and subsequent epizootics among animal populations. Responsible self-regulation by research laboratories, in conjunction with institutional-level safeguards, has an important role in mitigating pathogen transmission and spillover, as well as potential interspecies pathogenesis. A model system in disease ecology that highlights these concerns and related amelioration efforts is research focused on amphibian emerging infectious diseases. Whereas laboratory escape of amphibian pathogens has not been reported and may be rare compared with introduction events from trade or human globalization, the threat that novel disease outbreaks with mass mortality effects pose to wild populations warrants thorough biosecurity measures to ensure containment and prevent spillover. Here, we present a case study of the laboratory biosecurity concerns for the emerging amphibian fungal pathogen Batrachochytrium salamandrivorans. We conclude that proactive biosecurity strategies are needed to integrate researcher and institutional oversight of aquatic wildlife pathogens generally, and we call for increased national and international policy and legislative enforcement. Furthermore, taking professional responsibility beyond current regulations is needed as development of legal guidance can be slow at national and international levels. We outline the need for annual laboratory risk assessments, comprehensive training for all laboratory personnel, and appropriate safeguards specific to pathogens under study. These strategies are critical for upholding the integrity and credibility of the scientific community and maintaining public support for research on wildlife diseases.

Diet diversity and environment determine the intestinal microbiome and bacterial pathogen load of fire salamanders.

Diverse communities of symbiotic microbes inhabit the digestive systems of vertebrates and play a crucial role in animal health, and host diet plays a major role in shaping the composition and diversity of these communities. Here, we characterized diet and gut microbiome of fire salamander populations from three Belgian forests. We carried out DNA metabarcoding on fecal samples, targeting eukaryotic 18S rRNA of potential dietary prey items, and bacterial 16S rRNA of the concomitant gut microbiome. Our results demonstrated an abundance of soft-bodied prey in the diet of fire salamanders, and a significant difference in the diet composition between males and females. This sex-dependent effect on diet was also reflected in the gut microbiome diversity, which is higher in males than female animals. Proximity to human activities was associated with increased intestinal pathogen loads. Collectively, the data supports a relationship between diet, environment and intestinal microbiome in fire salamanders, with potential health implications.

Extraction-free detection of amphibian pathogens from water baths.

Detecting and quantifying pathogens with quick, cost-efficient and sensitive methods is needed across disease systems for addressing pertinent epidemiological questions. Typical methods rely on extracting DNA from collected samples. Here we develop and test an extraction-free method from water bath samples that is both sensitive and efficient for 2 major amphibian pathogens-Batrachochytrium dendrobatidis and B. salamandrivorans. We tested mock samples with known pathogen quantities as well as comparatively assessed detection from skin swabs and water baths from field sampled amphibians. Quantitative PCR (qPCR) directly on lyophilized water baths was able to reliably detect low loads of 10 and 1 zoospores for both pathogens, and detection rates were greater than those of swabs from field samples. Further concentration of samples did not improve detection, and collection container type did not influence pathogen load estimates. This method of lyophilization (i.e. freeze-drying) followed by direct qPCR offers an effective and efficient tool from detecting amphibian pathogens, which is crucial for surveillance efforts and estimating shedding rates for robust epidemiological understanding of transmission dynamics. Furthermore, water bath samples have multiple functions and can be used to evaluate mucosal function against pathogens and characterize mucosal components. The multifunctionality of water bath samples and reduced monetary costs and time expenditures make this method an optimal tool for amphibian disease research and may also prove to be useful in other wildlife disease systems.

Mentorship, equity, and research productivity: lessons from a pandemic.

The coronavirus pandemic is more fully exposing ubiquitous economic and social inequities that pervade conservation science. In this time of prolonged stress on members of the research community, primary investigators or project leaders (PLs) have a unique opportunity to adapt their programs to jointly create more equitable and productive research environments for their teams. Institutional guidance for PLs pursuing field and laboratory work centers on the physical safety of individuals while in the lab or field, but largely ignores the vast differences in how team members may be experiencing the pandemic. Strains on mental, physical, and emotional health; racial trauma; familial responsibilities; and compulsory productivity resources, such as high-speed internet, quiet work spaces, and support are unequally distributed across team members. The goal of this paper is to summarize the shifting dynamics of leadership and mentorship during the coronavirus pandemic and highlight opportunities for increasing equity in conservation research at the scale of the project team. Here, we (1) describe how the pandemic differentially manifests inequity on project teams, particularly for groups that have been structurally excluded from conservation science, (2) consider equitable career advancement during the coronavirus pandemic, and (3) offer suggestions for PLs to provide mentorship that prioritizes equity and wellbeing during and beyond the pandemic. We aim to support PLs who have power and flexibility in how they manage research, teaching, mentoring, consulting, outreach, and extension activities so that individual team members' needs are met with compassion and attention to equity.

Geography, Host Genetics, and Cross-Domain Microbial Networks Structure the Skin Microbiota of Fragmented Brazilian Atlantic Forest Frog Populations.

The host-associated microbiome plays a significant role in health. However, the roles of factors such as host genetics and microbial interactions in determining microbiome diversity remain unclear. We examined these factors using amplicon-based sequencing of 175 Thoropa taophora frog skin swabs collected from a naturally fragmented landscape in southeastern Brazil. Specifically, we examined (1) the effects of geography and host genetics on microbiome diversity and structure; (2) the structure of microbial eukaryotic and bacterial co-occurrence networks; and (3) co-occurrence between microeukaryotes with bacterial OTUs known to affect growth of the fungal pathogen Batrachochytrium dendrobatidis (Bd). While bacterial alpha diversity varied by both site type and host MHC IIB genotype, microeukaryotic alpha diversity varied only by site type. However, bacteria and microeukaryote composition showed variation according to both site type and host MHC IIB genotype. Our network analysis showed the highest connectivity when both eukaryotes and bacteria were included, implying that ecological interactions may occur among domains. Lastly, anti-Bd bacteria were not broadly negatively co-associated with the fungal microbiome and were positively associated with potential amphibian parasites. Our findings emphasize the importance of considering both domains in microbiome research and suggest that for effective probiotic strategies for amphibian disease management, considering potential interactions among all members of the microbiome is crucial.

Characterization of the microbiome of the invasive Asian toad in Madagascar across the expansion range and comparison with a native co-occurring species.

Biological invasions are on the rise, with each invader carrying a plethora of associated microbes. These microbes play important, yet poorly understood, ecological roles that can include assisting the hosts in colonization and adaptation processes or as possible pathogens. Understanding how these communities differ in an invasion scenario may help to understand the host's resilience and adaptability. The Asian common toad, Duttaphrynus melanostictus is an invasive amphibian, which has recently established in Madagascar and is expected to pose numerous threats to the native ecosystems. We characterized the skin and gut bacterial communities of D. melanostictus in Toamasina (Eastern Madagascar), and compared them to those of a co-occurring native frog species, Ptychadena mascareniensis, at three sites where the toad arrived in different years. Microbial composition did not vary among sites, showing that D. melanostictus keeps a stable community across its expansion but significant differences were observed between these two amphibians. Moreover, D. melanostictus had richer and more diverse communities and also harboured a high percentage of total unique taxa (skin: 80%; gut: 52%). These differences may reflect the combination of multiple host-associated factors including microhabitat selection, skin features and dietary preferences.

No impact of a short-term climatic "El Niño" fluctuation on gut microbial diversity in populations of the Galápagos marine iguana (Amblyrhynchus cristatus).

Gut microorganisms are crucial for many biological functions playing a pivotal role in the host's well-being. We studied gut bacterial community structure of marine iguana populations across the Galápagos archipelago. Marine iguanas depend heavily on their specialized gut microbiome for the digestion of dietary algae, a resource whose growth was strongly reduced by severe "El Niño"-related climatic fluctuations in 2015/2016. As a consequence, marine iguana populations showed signs of starvation as expressed by a poor body condition. Body condition indices (BCI) varied between island populations indicating that food resources (i.e., algae) are affected differently across the archipelago during 'El Niño' events. Though this event impacted food availability for marine iguanas, we found that reductions in body condition due to "El Niño"-related starvation did not result in differences in bacterial gut community structure. Species richness of gut microorganisms was instead correlated with levels of neutral genetic diversity in the distinct host populations. Our data suggest that marine iguana populations with a higher level of gene diversity and allelic richness may harbor a more diverse gut microbiome than those populations with lower genetic diversity. Since low values of these diversity parameters usually correlate with small census and effective population sizes, we use our results to propose a novel hypothesis according to which small and genetically less diverse host populations might be characterized by less diverse microbiomes. Whether such genetically depauperate populations may experience additional threats from reduced dietary flexibility due to a limited intestinal microbiome is currently unclear and calls for further investigation.

Winter is coming-Temperature affects immune defenses and susceptibility to Batrachochytrium salamandrivorans.

Environmental temperature is a key factor driving various biological processes, including immune defenses and host-pathogen interactions. Here, we evaluated the effects of environmental temperature on the pathogenicity of the emerging fungal pathogen, Batrachochytrium salamandrivorans (Bsal), using controlled laboratory experiments, and measured components of host immune defense to identify regulating mechanisms. We found that adult and juvenile Notophthalmus viridescens died faster due to Bsal chytridiomycosis at 14°C than at 6 and 22°C. Pathogen replication rates, total available proteins on the skin, and microbiome composition likely drove these relationships. Temperature-dependent skin microbiome composition in our laboratory experiments matched seasonal trends in wild N. viridescens, adding validity to these results. We also found that hydrophobic peptide production after two months post-exposure to Bsal was reduced in infected animals compared to controls, perhaps due to peptide release earlier in infection or impaired granular gland function in diseased animals. Using our temperature-dependent susceptibility results, we performed a geographic analysis that revealed N. viridescens populations in the northeastern United States and southeastern Canada are at greatest risk for Bsal invasion, which shifted risk north compared to previous assessments. Our results indicate that environmental temperature will play a key role in the epidemiology of Bsal and provide evidence that temperature manipulations may be a viable disease management strategy.

Batrachochytrium salamandrivorans ELICITS ACUTE STRESS RESPONSE IN SPOTTED SALAMANDERS BUT NOT INFECTION OR MORTALITY.

The emerging fungal pathogen Batrachochytrium salamandrivorans (Bsal) is a major threat to amphibian species worldwide with potential to infect many species if it invades salamander biodiversity hotspots in the Americas. Bsal can cause the disease chytridiomycosis, and it is important to assess the risk of Bsal-induced chytridiomycosis to species in North America. We evaluated the susceptibility to Bsal of the common and widespread spotted salamander, Ambystoma maculatum, across life history stages and monitored the effect of Bsal exposure on growth rate and response of the stress hormone, corticosterone. We conclude that spotted salamanders appear resistant to Bsal because they showed no indication of disease or infection, and experienced minor effects on growth upon exposure. While we focused on a single population for this study, results were consistent across conditions of exposure including high or repeated doses of Bsal, life-stage at exposure, environmental conditions including two temperatures and two substrates, and promoting pathogen infectivity by conditioning Bsal cultures with thyroid hormone. Exposure to high levels of Bsal elicited an acute but not chronic increase in corticosterone in spotted salamanders, and reduced growth. We hypothesize that the early acute increase in corticosterone facilitated mounting an immune response to the pathogen, perhaps through immunoredistribution to the skin, but further study is needed to determine immune responses to Bsal. These results will contribute to development of appropriate Bsal management plans to conserve species at risk of emerging disease.