Ongoing declines for the world's amphibians in the face of emerging threats.

Systematic assessments of species extinction risk at regular intervals are necessary for informing conservation action1,2. Ongoing developments in taxonomy, threatening processes and research further underscore the need for reassessment3,4. Here we report the findings of the second Global Amphibian Assessment, evaluating 8,011 species for the International Union for Conservation of Nature Red List of Threatened Species. We find that amphibians are the most threatened vertebrate class (40.7% of species are globally threatened). The updated Red List Index shows that the status of amphibians is deteriorating globally, particularly for salamanders and in the Neotropics. Disease and habitat loss drove 91% of status deteriorations between 1980 and 2004. Ongoing and projected climate change effects are now of increasing concern, driving 39% of status deteriorations since 2004, followed by habitat loss (37%). Although signs of species recoveries incentivize immediate conservation action, scaled-up investment is urgently needed to reverse the current trends.

Differences in sensitivity to the fungal pathogen Batrachochytrium dendrobatidis among amphibian populations.

Contributing to the worldwide biodiversity crisis are emerging infectious diseases, which can lead to extirpations and extinctions of hosts. For example, the infectious fungal pathogen Batrachochytrium dendrobatidis (Bd) is associated with worldwide amphibian population declines and extinctions. Sensitivity to Bd varies with species, season, and life stage. However, there is little information on whether sensitivity to Bd differs among populations, which is essential for understanding Bd-infection dynamics and for formulating conservation strategies. We experimentally investigated intraspecific differences in host sensitivity to Bd across 10 populations of wood frogs (Lithobates sylvaticus) raised from eggs to metamorphosis. We exposed the post-metamorphic wood frogs to Bd and monitored survival for 30 days under controlled laboratory conditions. Populations differed in overall survival and mortality rate. Infection load also differed among populations but was not correlated with population differences in risk of mortality. Such population-level variation in sensitivity to Bd may result in reservoir populations that may be a source for the transmission of Bd to other sensitive populations or species. Alternatively, remnant populations that are less sensitive to Bd could serve as sources for recolonization after epidemic events.

Detection of the emerging amphibian pathogens Batrachochytrium dendrobatidis and ranavirus in Russia.

In a population of the European common toad Bufo bufo from a rural pond in the region of Lake Glubokoe Regional Reserve in Moscow province, Russia, unexplained mass mortality events involving larvae and metamorphs have been observed over a monitoring period of >20 yr. We tested toads from this and a nearby site for the emerging amphibian pathogens Batrachochytrium dendrobatidis (Bd) and ranavirus (Rv). Both pathogens were detected, and at the rural pond site, with the above-noted losses and decline in toad breeding success, 40% of B. bufo metamorphs were Bd positive, 46% were Rv positive and 20% were co-infected with both pathogens. Toad metamorphs from a neighbouring water body were also Bd and Rv positive (25 and 55%, respectively). This is the first confirmation of these pathogens in Russia. Questions remain as to the origins of these pathogens in Russia and their roles in documented mass mortality events.

Management trade-off between aboveground carbon storage and understory plant species richness in temperate forests.

Because forest ecosystems have the capacity to store large quantities of carbon (C), there is interest in managing forests to mitigate elevated CO2 concentrations and associated effects on the global climate. However, some mitigation techniques may contrast with management strategies for other goals, such as maintaining and restoring biodiversity. Forest thinning reduces C storage in the overstory and recruitment of detrital C. These C stores can affect environmental conditions and resource availability in the understory, driving patterns in the distribution of early and late-seral species. We examined the effects of replicated (N = 7) thinning experiments on aboveground C and understory vascular plant species richness, and we contrasted relationships between aboveground C and early- vs. late-seral species richness. Finally, we used structural equation modeling (SEM) to examine relationships among early- and late-seral species richness and live and detrital aboveground C stores. Six years following thinning, aboveground C was greater in the high-density treatment and untreated control than in moderate- (MD) and variable-density (VD) treatments as a result of reductions in live overstory C. In contrast, all thinning treatments increased species richness relative to controls. Between the growing seasons of years 6 and 11 following treatments, the live overstory C increment tended to increase with residual density, while richness decreased in MD and VD treatments. The richness of early-seral species was negatively related to aboveground C in MD and VD, while late-seral species richness was positively (albeit weakly) related to aboveground C. Structural equation modeling analysis revealed strong negative effects of live overstory C on early-seral species richness balanced against weaker positive effects on late-seral species richness, as well as positive effects of detrital C stocks. A trade-off between carbon and plant species richness thus emerges as a net result of these relationships among species traits, thinning treatments, and live and detrital C storage. Integrating C storage with traditional conservation objectives may require managing this trade-off within stands and landscapes (e.g., maintain early-seral habitat and species within dense, C-rich forests and, conversely, live and detrital C stores in early-seral habitats) or separating these goals across scales and species groupings.

Landscape connectivity among coastal giant salamander (Dicamptodon tenebrosus) populations shows no association with land use, fire frequency, or river drainage but exhibits genetic signatures of potential conservation concern.

Determining the genetic consequences of both historical and contemporary events can clarify the effects of the environment on population connectivity and inform conservation decisions. Historical events (like glaciations) and contemporary factors (like logging) can disrupt gene flow between populations. This is especially true among species with specialized ecological requirements and low dispersal ability, like amphibians. We test for the genetic consequences of historical and contemporary disturbances in the coastal giant salamander (Dicamptodon tenebrosus) in the Pacific Northwest of the United States. We consider predictions based on the contemporary landscape (habitat connectivity, logging, forest fires, and topography), in addition to relatively ancient post-Pleistocene range expansion (following the last glacial retreat). To assess local versus larger-scale effects, we sampled 318 individuals across 23 sites, which were clustered in five sampling regions. Genetic variation was assessed using five microsatellite markers. We found evidence of (i) historical regional isolation, with decreased genetic diversity among more recently colonized northern sites, as well as (ii) high levels of inbreeding and loss of heterozygosity at local scales, despite relatively low overall population differentiation (FST) or strong evidence for population bottlenecks. Genetic diversity was not associated with contemporary disturbances (logging or fire), and there were no detectable effects on the genetic connectivity of populations based on intervening landscape features (habitat fragmentation and topography). However, lower genetic diversity in more northern regions indicates a lag in recovery of genetic diversity following post-Pleistocene expansion. Additionally, some populations had evidence of having undergone a recent genetic bottleneck or had high inbreeding (FIS) values. Lower genetic diversity in more northern sites means populations may be more vulnerable to future environmental changes, and managing for connectivity alone may not be sufficient given low mobility. Recent apparent reductions in some populations were not clearly linked to anthropogenic disturbances we examined. This suggests the type of disturbances this species is sensitive to may not be well understood.

Corrigendum: Global Patterns of the Fungal Pathogen Batrachochytrium dendrobatidis Support Conservation Urgency.

[This corrects the article DOI: 10.3389/fvets.2021.685877.].

Global Patterns of the Fungal Pathogen Batrachochytrium dendrobatidis Support Conservation Urgency.

The amphibian chytrid fungus Batrachochytrium dendrobatidis (Bd) is a skin pathogen that can cause the emerging infectious disease chytridiomycosis in susceptible species. It has been considered one of the most severe threats to amphibian biodiversity. We aimed to provide an updated compilation of global Bd occurrences by host taxon and geography, and with the larger global Bd dataset we reanalyzed Bd associations with environmental metrics at the world and regional scales. We also compared our Bd data compilation with a recent independent assessment to provide a more comprehensive count of species and countries with Bd occurrences. Bd has been detected in 1,375 of 2,525 (55%) species sampled, more than doubling known species infections since 2013. Bd occurrence is known from 93 of 134 (69%) countries at this writing; this compares to known occurrences in 56 of 82 (68%) countries in 2013. Climate-niche space is highly associated with Bd detection, with different climate metrics emerging as key predictors of Bd occurrence at regional scales; this warrants further assessment relative to climate-change projections. The accretion of Bd occurrence reports points to the common aims of worldwide investigators to understand the conservation concerns for amphibian biodiversity in the face of potential disease threat. Renewed calls for better mitigation of amphibian disease threats resonate across continents with amphibians, especially outside Asia. As Bd appears to be able to infect about half of amphibian taxa and sites, there is considerable room for biosecurity actions to forestall its spread using both bottom-up community-run efforts and top-down national-to-international policies. Conservation safeguards for sensitive species and biodiversity refugia are continuing priorities.

Tracking, Synthesizing, and Sharing Global Batrachochytrium Data at AmphibianDisease.org.

Emerging infectious diseases have been especially devastating to amphibians, the most endangered class of vertebrates. For amphibians, the greatest disease threat is chytridiomycosis, caused by one of two chytridiomycete fungal pathogens Batrachochytrium dendrobatidis (Bd) and Batrachochytrium salamandrivorans (Bsal). Research over the last two decades has shown that susceptibility to this disease varies greatly with respect to a suite of host and pathogen factors such as phylogeny, geography (including abiotic factors), host community composition, and historical exposure to pathogens; yet, despite a growing body of research, a comprehensive understanding of global chytridiomycosis incidence remains elusive. In a large collaborative effort, Bd-Maps was launched in 2007 to increase multidisciplinary investigations and understanding using compiled global Bd occurrence data (Bsal was not discovered until 2013). As its database functions aged and became unsustainable, we sought to address critical needs utilizing new technologies to meet the challenges of aggregating data to facilitate research on both Bd and Bsal. Here, we introduce an advanced central online repository to archive, aggregate, and share Bd and Bsal data collected from around the world. The Amphibian Disease Portal (https://amphibiandisease.org) addresses several critical community needs while also helping to build basic biological knowledge of chytridiomycosis. This portal could be useful for other amphibian diseases and could also be replicated for uses with other wildlife diseases. We show how the Amphibian Disease Portal provides: (1) a new repository for the legacy Bd-Maps data; (2) a repository for sample-level data to archive datasets and host published data with permanent DOIs; (3) a flexible framework to adapt to advances in field, laboratory, and informatics technologies; and (4) a global aggregation of Bd and Bsal infection data to enable and accelerate research and conservation. The new framework for this project is built using biodiversity informatics best practices and metadata standards to ensure scientific reproducibility and linkages across other biological and biodiversity repositories.

Shifts in temperature influence how Batrachochytrium dendrobatidis infects amphibian larvae.

Many climate change models predict increases in frequency and magnitude of temperature fluctuations that might impact how ectotherms are affected by disease. Shifts in temperature might especially affect amphibians, a group with populations that have been challenged by several pathogens. Because amphibian hosts invest more in immunity at warmer than cooler temperatures and parasites might acclimate to temperature shifts faster than hosts (creating lags in optimal host immunity), researchers have hypothesized that a temperature shift from cold-to-warm might result in increased amphibian sensitivity to pathogens, whereas a shift from warm-to-cold might result in decreased sensitivity. Support for components of this climate-variability based hypothesis have been provided by prior studies of the fungus Batrachochytrium dendrobatidis (Bd) that causes the disease chytridiomycosis in amphibians. We experimentally tested whether temperature shifts before exposure to Batrachochytrium dendrobatidis (Bd) alters susceptibility to the disease chytridiomycosis in the larval stage of two amphibian species-western toads (Anaxyrus boreas) and northern red legged frogs (Rana aurora). Both host species harbored elevated Bd infection intensities under constant cold (15° C) temperature in comparison to constant warm (20° C) temperature. Additionally, both species experienced an increase in Bd infection abundance after shifted from 15° C to 20° C, compared to a constant 20° C but they experienced a decrease in Bd after shifted from 20° C to 15° C, compared to a constant 15° C. These results are in contrast to prior studies of adult amphibians highlighting the potential for species and stage differences in the temperature-dependence of chytridiomycosis.

Headwater riparian forest-floor invertebrate communities associated with alternative forest management practices.

Headwater streams and their riparian zones are a common, yet poorly understood, component of Pacific Northwest, USA, landscapes. We describe the ecological importance of headwater stream riparian zones as habitat for forest-floor invertebrate communities and assess how alternative management strategies for riparian zones may impact these communities. We compared community composition of forest-floor invertebrates at increasing distances along trans-riparian (stream edge to upslope) transects in mature forests, clearcuts, and riparian buffers of approximately 30-m width with upslope clearcuts. Invertebrates were collected using pitfall traps in five replicate blocks of three treatments each in the Willamette National Forest, Oregon, USA. We measured microclimate and microhabitat variables at pitfall locations. Despite strong elevation and block effects on community composition, community analyses revealed a distinct "riparian" invertebrate community within 1 m of the stream edge in mature forest treatments, which was strongly related to cool, humid microclimate conditions. Invertebrate community composition in buffer treatments was far more similar to that of mature forests than to clearcuts; a pattern mirrored by microclimate. These results suggest that, within our study sites, forest-floor invertebrate distributions are strongly associated with microclimate and that riparian buffers of approximately 30-m width do provide habitat for many riparian and forest species. Riparian reserves may serve as effective forest refugia and/or dispersal corridors for invertebrates and other taxa, and their incorporation into watershed management plans likely will contribute to meeting persistence and connectivity objectives.

Linking Ecology and Epidemiology to Understand Predictors of Multi-Host Responses to an Emerging Pathogen, the Amphibian Chytrid Fungus.

Variation in host responses to pathogens can have cascading effects on populations and communities when some individuals or groups of individuals display disproportionate vulnerability to infection or differ in their competence to transmit infection. The fungal pathogen, Batrachochytrium dendrobatidis (Bd) has been detected in almost 700 different amphibian species and is implicated in numerous global amphibian population declines. Identifying key hosts in the amphibian-Bd system-those who are at greatest risk or who pose the greatest risk for others-is challenging due in part to many extrinsic environmental factors driving spatiotemporal Bd distribution and context-dependent host responses to Bd in the wild. One way to improve predictive risk models and generate testable mechanistic hypotheses about vulnerability is to complement what we know about the spatial epidemiology of Bd with data collected through comparative experimental studies. We used standardized pathogen challenges to quantify amphibian survival and infection trajectories across 20 post-metamorphic North American species raised from eggs. We then incorporated trait-based models to investigate the predictive power of phylogenetic history, habitat use, and ecological and life history traits in explaining responses to Bd. True frogs (Ranidae) displayed the lowest infection intensities, whereas toads (Bufonidae) generally displayed the greatest levels of mortality after Bd exposure. Affiliation with ephemeral aquatic habitat and breadth of habitat use were strong predictors of vulnerability to and intensity of infection and several other traits including body size, lifespan, age at sexual maturity, and geographic range also appeared in top models explaining host responses to Bd. Several of the species examined are highly understudied with respect to Bd such that this study represents the first experimental susceptibility data. Combining insights gained from experimental studies with observations of landscape-level disease prevalence may help explain current and predict future pathogen dynamics in the Bd system.

Projecting the Global Distribution of the Emerging Amphibian Fungal Pathogen, Batrachochytrium dendrobatidis, Based on IPCC Climate Futures.

Projected changes in climate conditions are emerging as significant risk factors to numerous species, affecting habitat conditions and community interactions. Projections suggest species range shifts in response to climate change modifying environmental suitability and is supported by observational evidence. Both pathogens and their hosts can shift ranges with climate change. We consider how climate change may influence the distribution of the emerging infectious amphibian chytrid fungus, Batrachochytrium dendrobatidis (Bd), a pathogen associated with worldwide amphibian population losses. Using an expanded global Bd database and a novel modeling approach, we examined a broad set of climate metrics to model the Bd-climate niche globally and regionally, then project how climate change may influence Bd distributions. Previous research showed that Bd distribution is dependent on climatic variables, in particular temperature. We trained a machine-learning model (random forest) with the most comprehensive global compilation of Bd sampling records (~5,000 site-level records, mid-2014 summary), including 13 climatic variables. We projected future Bd environmental suitability under IPCC scenarios. The learning model was trained with combined worldwide data (non-region specific) and also separately per region (region-specific). One goal of our study was to estimate of how Bd spatial risks may change under climate change based on the best available data. Our models supported differences in Bd-climate relationships among geographic regions. We projected that Bd ranges will shift into higher latitudes and altitudes due to increased environmental suitability in those regions under predicted climate change. Specifically, our model showed a broad expansion of areas environmentally suitable for establishment of Bd on amphibian hosts in the temperate zones of the Northern Hemisphere. Our projections are useful for the development of monitoring designs in these areas, especially for sensitive species and those vulnerable to multiple threats.

Mating pattern variability among western toad (Bufo boreas) populations.

Breeding ecology and mating patterns of the western toad, Bufo boreas, were examined in three large explosively breeding populations in the Oregon Cascade Mountains. Two mating patterns occurred variably within and among the three populations. First, a large male mating advantage was observed in two of the three populations when data from all the days of data collection were combined. When each day of breeding was analyzed separately, there was a large male mating advantage on 3 of 5 days at one population, and mating was random on all days at the two other populations. The second mating pattern, positive assortative mating by size, was observed at two of the three populations. This pattern was found on separate days of breeding as well as when data from all days were combined at one population, and on only one day of breeding at the second population.In a survey of anuran amphibian mating patterns, intraspecific variation was found in 13 of 15 species, including the present study of the western toad. Intrapopulation variation in mating patterns among breeding years has been observed in 5 of 8 anurans, whereas within-site, within-year mating pattern variation has only been reported for the western toad. These results strongly suggest that anuran mating patterns are frequently neither species-specific nor population-specific attributes. Variable mating patterns were most commonly observed in explosively-breeding anurans. Explosive breeders may be susceptible to variable mating patterns because they may be more sensitive to fluctuations in environmental conditions, demographic parameters, and the intensities of intrasexual competition and mate choice.

Heterogeneous occupancy and density estimates of the pathogenic fungus Batrachochytrium dendrobatidis in waters of North America.

Biodiversity losses are occurring worldwide due to a combination of stressors. For example, by one estimate, 40% of amphibian species are vulnerable to extinction, and disease is one threat to amphibian populations. The emerging infectious disease chytridiomycosis, caused by the aquatic fungus Batrachochytrium dendrobatidis (Bd), is a contributor to amphibian declines worldwide. Bd research has focused on the dynamics of the pathogen in its amphibian hosts, with little emphasis on investigating the dynamics of free-living Bd. Therefore, we investigated patterns of Bd occupancy and density in amphibian habitats using occupancy models, powerful tools for estimating site occupancy and detection probability. Occupancy models have been used to investigate diseases where the focus was on pathogen occurrence in the host. We applied occupancy models to investigate free-living Bd in North American surface waters to determine Bd seasonality, relationships between Bd site occupancy and habitat attributes, and probability of detection from water samples as a function of the number of samples, sample volume, and water quality. We also report on the temporal patterns of Bd density from a 4-year case study of a Bd-positive wetland. We provide evidence that Bd occurs in the environment year-round. Bd exhibited temporal and spatial heterogeneity in density, but did not exhibit seasonality in occupancy. Bd was detected in all months, typically at less than 100 zoospores L(-1). The highest density observed was ∼3 million zoospores L(-1). We detected Bd in 47% of sites sampled, but estimated that Bd occupied 61% of sites, highlighting the importance of accounting for imperfect detection. When Bd was present, there was a 95% chance of detecting it with four samples of 600 ml of water or five samples of 60 mL. Our findings provide important baseline information to advance the study of Bd disease ecology, and advance our understanding of amphibian exposure to free-living Bd in aquatic habitats over time.

Host identity matters in the amphibian-Batrachochytrium dendrobatidis system: fine-scale patterns of variation in responses to a multi-host pathogen.

Species composition within ecological assemblages can drive disease dynamics including pathogen invasion, spread, and persistence. In multi-host pathogen systems, interspecific variation in responses to infection creates important context dependency when predicting the outcome of disease. Here, we examine the responses of three sympatric host species to a single fungal pathogen, Batrachochytrium dendrobatidis, which is associated with worldwide amphibian population declines and extinctions. Using an experimental approach, we show that amphibian species from three different genera display significant differences in patterns of pathgen-induced mortality as well as the magnitude and temporal dynamics of infection load. We exposed amphibians to one of four inoculation dose treatments at both larval and post- metamorphic stages and quantified infection load on day 8 and day 15 post-inoculation. Of the three species examined, only one (the Pacific treefrog; Pseudacris regilla) displayed "dose-dependent" responses; survival was reduced and infection load was elevated as inoculation dose was increased. We observed a reduction in survival but no differences in infection load across pathogen treatments in Cascades frogs (Rana cascadae). Western toads (Anaxyrus boreas) displayed differences in infection load but no differences in survival across pathogen treatments. Within species, responses to the pathogen varied with life history stage, and the most heavily infected species at the larval stage was different from the most heavily infected species at the post-metamorphic stage. Temporal changes in infection load were species and life history stage-specific. We show that variation in susceptibility to this multi-host pathogen is complex when viewed at a fine-scale and may be mediated through intrinsic host traits.

Mapping the global emergence of Batrachochytrium dendrobatidis, the amphibian chytrid fungus.

The rapid worldwide emergence of the amphibian pathogen Batrachochytrium dendrobatidis (Bd) is having a profound negative impact on biodiversity. However, global research efforts are fragmented and an overarching synthesis of global infection data is lacking. Here, we provide results from a community tool for the compilation of worldwide Bd presence and report on the analyses of data collated over a four-year period. Using this online database, we analysed: 1) spatial and taxonomic patterns of infection, including amphibian families that appear over- and under-infected; 2) relationships between Bd occurrence and declining amphibian species, including associations among Bd occurrence, species richness, and enigmatic population declines; and 3) patterns of environmental correlates with Bd, including climate metrics for all species combined and three families (Hylidae, Bufonidae, Ranidae) separately, at both a global scale and regional (U.S.A.) scale. These associations provide new insights for downscaled hypothesis testing. The pathogen has been detected in 52 of 82 countries in which sampling was reported, and it has been detected in 516 of 1240 (42%) amphibian species. We show that detected Bd infections are related to amphibian biodiversity and locations experiencing rapid enigmatic declines, supporting the hypothesis that greater complexity of amphibian communities increases the likelihood of emergence of infection and transmission of Bd. Using a global model including all sampled species, the odds of Bd detection decreased with increasing temperature range at a site. Further consideration of temperature range, rather than maximum or minimum temperatures, may provide new insights into Bd-host ecology. Whereas caution is necessary when interpreting such a broad global dataset, the use of our pathogen database is helping to inform studies of the epidemiology of Bd, as well as enabling regional, national, and international prioritization of conservation efforts. We provide recommendations for adaptive management to enhance the database utility and relevance.