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Anticipating the potential impacts of Batrachochytrium salamandrivorans on Neotropical salamander diversity
Abstract
Emergent infectious disease caused by the fungal pathogens Batrachochytrium dendrobatidis ( Bd ) and Batrachochytrium salamandrivorans ( Bsal ) represents one of the major causes of biodiversity loss in amphibians. While Bd has affected amphibians worldwide, Bsal remains restricted to Asia and Europe, but also could be a major threat for salamanders in the Western hemisphere, including the 320 bolitoglossine species described. Here, we predict the suitable areas for Bsal in the Neotropics and assess its potential impact on bolitoglossine diversity. For this, we determined the geographic patterns of taxonomic, phylogenetic, and functional diversity for bolitoglossines and modeled the potential distribution of Bsal in the Neotropics. We identified which species and regions could be at risk from an eventual introduction of Bsal in the region, quantified the degree of overlap between regions of high diversity and the suitable conditions for the pathogen, and considered species IUCN Red List status, and geographic range size. We found that regions of high taxonomic, phylogenetic, and functional diversity are concentrated in the Trans‐Mexican Volcanic Belt, Sierra Madre Oriental, the southern portion of Sierra Madre del Sur and the mountains of Oaxaca in México, as well as the Chiapan‐Guatemalan highlands, and the Cordilleras of Costa Rica and Panama. Alarmingly, the regions of high diversity for bolitoglossines and over 75% of the ranges of the more threatened species could be affected by Bsal . Given the unknown vulnerability of these species, we strongly recommend measures to avoid the introduction of Bsal in the continent.
Abstract in Spanish is available with online material.
... Ecological Niche Models (ENM, also referred to as Species Distribution Models) are valuable tools for understanding species' habitat and therefore generating efficient and targeted surveillance efforts. ENM have been employed to evaluate the risk of invasion of Bd in Costa Rica, and Bsal in North America, Europe, and Central and South America [9, 30,36,[42][43][44]. García-Rodríguez and colleagues recently generated Bsal ENM for Central and South America that identified multiple hotspots for Bsal introduction, mostly located in central and southern Mexico and Costa Rican mountain ranges [43,44]. ...
... ENM have been employed to evaluate the risk of invasion of Bd in Costa Rica, and Bsal in North America, Europe, and Central and South America [9, 30,36,[42][43][44]. García-Rodríguez and colleagues recently generated Bsal ENM for Central and South America that identified multiple hotspots for Bsal introduction, mostly located in central and southern Mexico and Costa Rican mountain ranges [43,44]. Despite the fact that the work by García-Rodríguez et al. [44] identifies sites where the diversity of salamanders and an optimal environment for Bsal converge, we believe that, in order to have a preventive effect on the transmission of the pathogen, we must consider the most probable sources of transmission and their relationship with the divers and susceptible areas. ...
... García-Rodríguez and colleagues recently generated Bsal ENM for Central and South America that identified multiple hotspots for Bsal introduction, mostly located in central and southern Mexico and Costa Rican mountain ranges [43,44]. Despite the fact that the work by García-Rodríguez et al. [44] identifies sites where the diversity of salamanders and an optimal environment for Bsal converge, we believe that, in order to have a preventive effect on the transmission of the pathogen, we must consider the most probable sources of transmission and their relationship with the divers and susceptible areas. Indeed, recent work modeling Bsal spread in Europe has found that trail density is an important predictor of the pathogen's presence [45]. ...
Remotely-sensed risk assessments of emerging, invasive pathogens are key to targeted surveillance and outbreak responses. The recent emergence and spread of the fungal pathogen, Batrachochytrium salamandrivorans (Bsal), in Europe has negatively impacted multiple salamander species. Scholars and practitioners are increasingly concerned about the potential consequences of this lethal pathogen in the Americas, where salamander biodiversity is higher than anywhere else in the world. Although Bsal has not yet been detected in the Americas, certain countries have already proactively implemented monitoring and detection plans in order to identify areas of greatest concern and enable efficient contingency planning in the event of pathogen detection. To predict areas in Costa Rica with a high Bsal transmission risk, we employed ecological niche modeling combined with biodiversity and tourist visitation data to ascertain the specific risk to a country with world renowned biodiversity. Our findings indicate that approximately 23% of Costa Rica’s landmass provides suitable conditions for Bsal, posing a threat to 37 salamander species. The Central and Talamanca mountain ranges, in particular, have habitats predicted to be highly suitable for the pathogen. To facilitate monitoring and mitigation efforts, we identified eight specific protected areas that we believe are at the greatest risk due to a combination of high biodiversity, tourist visitation, and suitable habitat for Bsal. We advise regular monitoring utilizing remotely-sensed data and ecological niche modeling to effectively target in-situ surveillance and as places begin implementing educational efforts.
... Fortunately, the salamander and anuran populations have been recovering since the beginning of this century (Rodriguez et al., 2020;Zumbado-Ulate et al., 2021). However, the threat of the salamander-eating fungus (Batrachochytrium salamandrivorans) is still latent in the highland species of Costa Rica and Panama (Garcia- Rodriguez et al., 2022). The biological monitoring of highland amphibians, including sampling mountain bog habitats, is therefore of high priority. ...
High-altitude mountain bogs, located in the Central and Talamanca Mountain Ranges of Costa Rica (1200–3100 m a.s.l.), remain one of the least explored inland aquatic ecosystems and potentially one of the most geographically restricted. These unique wetlands are confined to topographic depressions with limited drainage, rely solely on rainfall for the maintenance of their water bodies, and can dry up entirely during prolonged dry spells. Since they are limited to specific topographic and soil conditions and maintain a characteristic biota with many endemic species, mountain bogs deserve urgent conservation attention. Unfortunately, human activities have significantly impacted these fragile ecosystems (e.g. soil drainage for agricultural purposes, illicit extraction of plant species, fragmentation, pollution, and fire). Concentrated predominantly in Talamanca, mountain bogs represent discrete biomes embedded within oak forests and páramos, reflecting a complex interplay between the parent material, the topography, and climatic factors. Here, we discuss the ecological traits, biogeographic significance, limnological characteristics, representative organisms, and climate change vulnerability of mountain bogs and propose key research areas to enhance the management and conservation of this ecosystem. We compiled a list of 108 vascular plant species (27% endemics), analyzed the bird species composition, and listed representative amphibians and reptiles, particularly the endemic Bolitoglossa salamanders. We present a preliminary list of expected mammals (57 species, 18 endemics, and 3 bat genera). Aquatic insects and crustaceans are just beginning to be explored, but several new reports and new species were reported. Mountain bogs are particularly diverse and are characterized by high levels of endemism. They are important carbon reservoirs and serve as a comprehensive paleobotanical pollen record showing fluctuations in the location of the tree line and the extension of páramos in the geologic past. Climate change may cause significant species turnover and elevational shifts due to decreasing rainfall and increasing temperatures, further compounded by the risk of biological invasions and habitat loss mediated by human activities such as road construction and powerline installation. Urgent scientific research and comprehensive conservation strategies are imperative to safeguard the endangered mountain bog ecosystem, ensuring its continued existence and resilience amidst escalating environmental pressures and anthropogenic disturbances.
... With this historical context in mind, the more recent emergence of fatal amphibian chytridiomycosis caused by the novel amphibian chytrid fungus Bsal in Europe (Martel et al., 2013;Stegen et al., 2017) with potential palearctic reach (Martel et al., 2014) resulted in an immediate proactive call for strategic efforts in North America (Gray et al., 2015), and a more recent alert echoing concerns for neotropical amphibians (Garcıá-Rodrıǵuez et al., 2022). Heightened concerns for the world centers of salamander biodiversity represented by Appalachia and the Pacific Northwest were supported by initial Bsal risk models and maps (Yap et al., 2015;Richgels et al., 2016) that integrated early knowledge of infection risk by host amphibian taxon (Martel et al., 2014) with North American host ranges, environmental conditions, and proximity to international ports and pet stores (as the pet trade was identified as a likely route of introduction to middle European populations: Martel et al., 2013;Martel et al., 2014; see also Cunningham et al., 2017;Nguyen et al., 2017;Fitzpatrick et al., 2018;Yuan et al., 2018). ...
Western palearctic salamander susceptibility to the skin disease caused by the amphibian chytrid fungus Batrachochytrium salamandrivorans (Bsal) was recognized in 2014, eliciting concerns for a potential novel wave of amphibian declines following the B. dendrobatidis (Bd) chytridiomycosis global pandemic. Although Bsal had not been detected in North America, initial experimental trials supported the heightened susceptibility of caudate amphibians to Bsal chytridiomycosis, recognizing the critical threat this pathogen poses to the North American salamander biodiversity hotspot. Here, we take stock of 10 years of research, collaboration, engagement, and outreach by the North American Bsal Task Force. We summarize main knowledge and conservation actions to both forestall and respond to Bsal invasion into North America. We address the questions: what have we learned; what are current challenges; and are we ready for a more effective reaction to Bsal’s eventual detection? We expect that the many contributions to preemptive planning accrued over the past decade will pay dividends in amphibian conservation effectiveness and can inform future responses to other novel wildlife diseases and extreme threats.
... These stressors can act synergistically, endangering populations globally (Bosch et al., 2021;Pastorino et al., 2023b). Factors contributing to amphibian declines include road traffic mortality (Morelli et al., 2023), habitat degradation (Pabijan et al., 2023), overcollecting (Natusch and Lyons, 2012), climate change (Chunlin et al., 2022), introduced predators (Nunes et al., 2019), and the humanmediated spread of pathogens (García-Rodríguez et al., 2021). Recent reports of amphibian mass mortality events (e.g., Pastorino et al., 2023b) emphasise the need to investigate the combined effects of these stressors. ...
Amphibians are vital components of global biodiversity and fulfil diverse ecological roles, including insect population control and serving as environmental health indicators. However, there is a concerning decline in amphibian populations globally due to factors such as habitat loss, climate change, and emerging diseases. Concurrently, the issue of microplastic pollution has gained prominence because of its potential to harm aquatic ecosystems. Microplastics, derived from various sources, endanger aquatic organisms, especially amphibians during their sensitive larval stages. In this study, we examined the prevalence of microplastic pollution in the larval stages of 10 amphibian species, covering both tailed (Urodela) and tailless (Anura) amphibians. We observed a significant correlation between amphibian species identity, the extent of artificial land cover, and the degree of microplastic contamination in larvae. Notably, our results indicate interspecific differences in micro-plastic bioaccumulation. Furthermore, this research is the first to demonstrate a positive correlation between microplastic pollution in amphibian larvae and anthropogenic pressure. Our findings add to the expanding literature underscoring the intricate interplay between human activities and aquatic ecosystem health.
... In contrast, Bsal mainly affects caudates and several anurans [9,10]. It has led to severe declines in native salamanders only in Europe so far, although the pathogen is present in Asia [4][5][6]11]; however, the impending threat for the highly diverse North American and Neotropical salamanders is significant [12][13][14][15][16][17][18]. Knowledge of Bsal ecology is critical as it provides proactive information for amphibian conservation, including identifying new susceptible species and analyzing their occurrences with the identification of the relevant ecological drivers. ...
The chytrid fungal pathogens Batrachochytrium salamandrivorans (Bsal) and B. dendrobatidis (Bd) are driving amphibian extinctions and population declines worldwide. As their origins are believed to be in East/Southeast Asia, this region is crucial for understanding their ecology. However, Bsal screening is relatively limited in this region, particularly in hotspots where Bd lineage diversity is high. To address this gap, we conducted an extensive Bsal screening involving 1101 individuals from 36 amphibian species, spanning 17 natural locations and four captive facilities in the biodiversity-rich Guangxi Zhuang Autonomous Region (GAR). Our PCR assays yielded unexpected results, revealing the complete absence of Bsal in all tested samples including 51 individuals with Bd presence. To understand the potential distribution of Bsal, we created niche models, utilizing existing occurrence records from both Asia and Europe. These models estimated potential suitable habitats for Bsal largely in the northern and southwestern parts of the GAR. Although Bsal was absent in our samples, the niche models identified 10 study sites as being potentially suitable for this pathogen. Interestingly, out of these 10 sites, Bd was detected at 8. This suggests that Bsal and Bd could possibly co-exist in these habitats, if Bsal were present. Several factors seem to influence the distribution of Bsal in Asia, including variations in temperature, local caudate species diversity, elevation, and human population density. However, it is climate-related factors that hold the greatest significance, accounting for a notable 60% contribution. The models propose that the specific climatic conditions of arid regions, primarily seen in the GAR, play a major role in the distribution of Bsal. Considering the increased pathogenicity of Bsal at stable and cooler temperatures (10–15 °C), species-dependent variations, and the potential for seasonal Bd-Bsal interactions, we emphasize the importance of periodic monitoring for Bsal within its projected range in the GAR. Our study provides deeper insights into Bsal’s ecological niche and the knowledge generated will facilitate conservation efforts in amphibian populations devastated by chytrid pathogens across other regions of the world.
... Hence, the establishment of infection in a region places species in neighboring countries at greater risk. Mexico and Central America hold more than half of the known caudate species, 74% of which are being threatened and models suggest that there are areas suitable for Bsal in these countries (Basanta et al. 2019, García-Rodríguez 2022. ...
Batrachochytrium salamandrivorans (Bsal), a species related to the destructive pathogen Batrachochytrium dendrobatidis (Bd), was found and identified in Europe in 2013. Now, a decade later, a large amount of information is available. This includes data from studies in the field, reports of infection in captive amphibians, laboratory studies testing host susceptibility, and data from prospective studies that test for Bsal ’s presence in a location. We conducted a systematic review of the published literature and compiled a dataset of Bsal tests. We identified 67 species that have been reported positive for Bsal, 20 of which have a threatened conservation status. The distribution of species that have been found with infection encompasses 69 countries, highlighting the potential threat that Bsal poses. We point out where surveillance to detect Bsal have taken place and highlight areas that have not been well monitored. The large number of host species belonging to the families Plethodontidae and Salamandridae suggests a taxonomic pattern of susceptibility. Our results provide insight into the risk posed by Bsal and identifies vulnerable species and areas where surveillance is needed to fill existing knowledge gaps.
... The related pathogen, Batrachochytrium salamandrivorans (Bsal; Martel et al., 2013) has not yet arrived in the Americas, but BdxBsal infections cause worse infections in salamanders than Bd or Bsal alone . Altogether, understanding the eco-evolutionary dynamics of this disease in collapsed and persisting populations will lend insights into future conservation relevant to population responses in unexposed regions (e.g., salamanders in North and Central America; García-Rodríguez et al., 2022), as well as arrival of new strains in other regions (e.g., new global pandemic lineages or hybridization events). ...
Amphibians face global declines, and it remains unclear the extent to which species have responded, and through what mechanisms, to persist in the face of emerging diseases and climate change. In recent years, the rediscovery of species considered possibly extinct has sparked public and scientific attention. These are hopeful cases in an otherwise bleak story. Yet, we know little about the population status of these rediscovered species, or the biology underlying their persistence. Here, we highlight the iconic Harlequin frogs (Bufonidae: Atelopus) as a system that was devastated by declines but now encompasses between 18 and 32 rediscoveries (25–37 % of possible extinctions) in the last two decades. Geographic distributions of rediscoveries closely match regional described species abundance, and rediscoveries are documented at elevations from 100 m to >3500 m, with no significant differences between mean historical and contemporary elevations. We also provide genomic data on six decimated species, with historical sample comparisons for two of the species and find a pattern of decreasing genetic variation the longer a species had been missing. Further, we document marked decrease in heterozygosity in one species, but not the other, indicating potential idiosyncratic consequences of declines. Finally, we discuss research priorities to guide the potential transition from amphibian declines to recoveries and to maximize conservation efforts.
... Differences in bacterial community composition in individuals of Pseudoeurycea with and without Bd could point either to a protective role of the microbiome in some individuals or community disturbance caused by Bd infection. The link between community composition and Bd infection in this group merits further study given the level of threat that many Neotropical salamanders face from Bd and potentially from B. salamandrivorans should it arrive in the Neotropics [17,90]. ...
Host microbial communities are increasingly seen as an important component of host health. In amphibians, the first land vertebrates that are threatened by a fungal skin disease globally, our understanding of the factors influencing the microbiome of amphibian skin remains incomplete because recent studies have focused almost exclusively on bacteria, and little information exists on fungal communities associated with wild amphibian species. In this study, we describe the effects of host phylogeny, climate, geographic distance, and infection with a fungal pathogen on the composition and structure of bacterial and fungal communities in seven tropical salamander species that occur in the Trans-Mexican Volcanic Belt of Central Mexico. We find that host phylogenetic relatedness is correlated with bacterial community composition while a composite climatic variable of temperature seasonality and precipitation is significantly associated with fungal community composition. We also estimated co-occurrence networks for bacterial and fungal taxa and found differences in the degree of connectivity and the distribution of negative associations between the two networks. Our results suggest that different factors may be responsible for structuring the bacterial and fungal communities of amphibian skin and that the inclusion of fungi in future studies could shed light on important functional interactions within the microbiome.
Amphibian chytridiomycosis due to Batrachochytrium dendrobatidis (Bd) and ranaviral disease caused by ranaviruses are two emerging infectious diseases associated with amphibian declines. Both pathogens are widespread in South America, but Ranavirus has been much less studied. Geographically, Bd has highly favorable habitats in the Andes and Atlantic forests. Among the taxa exhibiting high Bd occurrence are Ranidae, Telmatobiidae, Calyptocephalellidae, and Pipidae, reflecting their close association with aquatic environments and therefore higher contact with the infective stage of Bd. Surprisingly, families exhibiting unusually low Bd prevalence comprise species in which lethal chytridiomycosis has caused high impacts, such as Harlequin toads (Atelopus spp.), Andean water frogs (Telmatobius spp.), and Darwin’s frogs (Rhinoderma spp.). Ranavirus-associated die-offs occur frequently in farmed North American bullfrogs (Lithobates catesbeianus; e.g., Brazil and Uruguay), and outbreaks causing high mortality have been described in the Patagonia frog (Atelognathus patagonicus) in Argentina and L. catesbeianus in Brazil. Widespread invasive amphibian species showing high Bd and Ranavirus prevalence are good target species that can be subjected to management for disease mitigation. A better understanding of the epidemiology of Bd and Ranavirus will help guide the prioritization of conservation actions to prevent further biodiversity loss in the world’s most amphibian diverse region.
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.
The chytrid fungal pathogens Batrachochytrium salamandrivorans ( Bsal ) and B. dendrobatidis ( Bd ) are driving amphibian extinctions and population declines worldwide. They are thought to have originated in East/Southeast Asia, and hence Asia remains crucial for understanding the ecology of these pathogens. However, Bsal screening is relatively limited in this region, particularly in hotspots where Bd lineage diversity is high. To address this gap, we conducted an extensive survey across the Guangxi region of Southern China, now considered a Bd hotspot. We examined 1230 individuals from 38 amphibian species and 36 environmental water bodies sampled during mostly the middle spring and summer months of 2019-21. However, PCR testing revealed absence of Bsal in our samples. A subsequent niche modeling analysis for Bsal suggested that the bioclimatic conditions of much of the region may not be conducive to Bsal . Although our findings show absence of Bsal in the surveyed habitats, periodic monitoring in amphibians is still needed, particularly across seasons. This is because Bsal pathogenicity could increase at relatively lower temperatures, and Bsal may be partitioning its niche with Bd across seasons. Our results suggest that the climatic conditions of the karstic Guangxi plains and perhaps competition from other Bd lineages may suppress Bsal establishment in the region. Our study provide interesting insights into Bsal niche dynamics and the knowledge generated will facilitate the conservation efforts in amphibian populations devastated by chytrid pathogens across other regions of the world.
The chytrid fungal pathogens Batrachochytrium salamandrivorans ( Bsal ) and B. dendrobatidis ( Bd ) are driving amphibian extinctions and population declines worldwide. They are thought to have originated in East/Southeast Asia, and hence Asia remains crucial for understanding the ecology of these pathogens. However, Bsal screening is relatively limited in this region, particularly in hotspots where Bd lineage diversity is high. To address this gap, we conducted an extensive survey across the Guangxi region of Southern China, now considered a Bd hotspot. We examined 1230 individuals from 38 amphibian species and 36 environmental water bodies sampled during mostly the middle spring and summer months of 2019-21. However, PCR testing revealed absence of Bsal in our samples. A subsequent niche modeling analysis for Bsal suggested that the bioclimatic conditions of much of the region may not be conducive to Bsal . Although our findings show absence of Bsal in the surveyed habitats, periodic monitoring in amphibians is still needed, particularly across seasons. This is because Bsal pathogenicity could increase at relatively lower temperatures, and Bsal may be partitioning its niche with Bd across seasons. Our results suggest that the climatic conditions of the karstic Guangxi plains and perhaps competition from other Bd lineages may suppress Bsal establishment in the region. Our study provide interesting insights into Bsal niche dynamics and the knowledge generated will facilitate the conservation efforts in amphibian populations devastated by chytrid pathogens across other regions of the world.
The recent emergence of the pathogen Batrachochytrium salamandrivorans (Bsal) is associated with rapid population declines of salamanders in Europe and its arrival to new areas could cause dramatic negative effects on other amphibian populations and species. Amphibian species, present in areas with high amphibian diversity such as Mexico, could be highly threatened due to the arrival of Bsal, particularly salamander species which are more vulnerable to chytridiomycosis caused by this pathogen. Thus, immediate surveillance is needed as a strategy to efficiently contend with this emerging infectious disease. In this study, we analyzed 490 wild and captive amphibians from 48 species across 76 sites in the North, Central, and South of Mexico to evaluate the presence of Bsal. Amphibians were sampled in sites with variable degrees of amphibian richness and suitability for Bsal according to previous studies. From the 76 sampling sites, 10 of them were located in areas with high amphibian richness and potential moderate to high Bsal habitat suitability. We did not detect Bsal in any of the samples, and no signs of the disease were observed in any individual at the time of sampling. Our results suggest that Bsal has not yet arrived at the sampled sites or could be at low prevalence within populations with low occurrence probability. This is the first study that evaluates the presence of Bsal in different regions and amphibian species in Mexico, which is the second most diverse country in salamander species in the world. We highlight the risk and the importance of continuing surveillance of Bsal in Mexico and discuss control strategies to avoid the introduction and spread of Bsal in the country.
Emerging infectious diseases are among the leading drivers of the sixth mass extinction. The recent invasion of a highly pathogenic chytrid fungus, Batrachochytrium salamandrivorans (Bsal), across Europe has led to salamander mass mortality. To date, it remains unclear whether Bsal will cause salamander mass mortalities in North America. Here, we tested the Bsal susceptibility of eight wild-caught salamander species (Plethodon cinereus, P. glutinosus, P. montanus, P. cylindraceus, Desmognathus fuscus, D. wrighti, Eurycea wilderae, and Notophthalmus viridescens) by inoculating individuals sequentially with a low (10,000 zoospores) and high (500,000 zoospores) Bsal dose. Overall, we found rapid and complete mortality of N. viridescens accompanied with high-Bsal infections (> 200,000 Bsal zoospores) and severe Bsal lesions distributed across the body and deep within the skin. In contrast, we found low mortality of plethodontid salamanders, where only 5 of 60 (8%) Bsal-exposed individuals died over the course of the experiment. In general, plethodontid salamanders experienced moderate Bsal infections (~ 4000 Bsal zoospores) with small numbers of Bsal-type lesions limited to the head and lateral body. Following the first Bsal inoculation, we found that Bd co-infections negatively affected Bsal infections, suggesting cross reactivity of the immune system or competitive exclusion, but this pattern did not persist following the second inoculation. We also found that Bsal infection intensity decreased over time following the second higher Bsal inoculation, suggesting evidence of immune priming. Throughout the experiment, all species and treatments experienced stable or increasing body condition over time. Lastly, ancestral state reconstruction of Bsal susceptibility indicated that although the most recent common ancestor (MRCA) of the family Plethodontidae is resistant to Bsal, the MRCA of the genus Plethodon is tolerant of Bsal. This highlights the variation in Bsal-infection outcomes across Plethodontidae. Collectively, our results suggest that Plethodontidae salamanders differ in their Bsal susceptibility, with some species less impacted than others, which will likely have consequences for their conservation and management.
Globally, numerous amphibian species have declined due to the introduction of the chytrid fungus Batrachochytrium dendrobatidis ( Bd ). However, the understanding of the spatiotemporal dynamics remains incomplete. Therefore, estimating the current geographic distribution of Bd is urgently needed, especially in countries like Costa Rica, where susceptible species are still recovering from Bd ‐driven declines. We conducted model tuning and spatial analysis to compare the habitat suitability for epizootic and enzootic Bd in Costa Rica and to identify data‐deficient regions, opportunistic sampling, and Bd hotspots. Our dataset combined two methods of detection (histology and PCR methods) for a total of 451 Bd ‐positive records from 34 localities. We found that the distribution of enzootic Bd in Costa Rica increased 60% since previous estimates in the early 2000s and extended to highlands and dry lowlands that were considered unsuitable for Bd . We also found that Bd is common across protected lands (80%) and within the herpetological provinces containing the highest amphibian richness and endemism in Costa Rica. Opportunistic sampling of Bd has focused on sites where epizootics occurred with the strongest intensity, leading to deficient or absent sampling across the Talamanca Range, the Nicoya Peninsula, and the northern lowlands. Our results showed that PCR increased the power of Bd detection in lowlands and favored the identification of Bd hotspots across the Caribbean side of Costa Rica. Our results add to the understanding of disease spread during enzootics and can be used to identify new hotspots for disease to mitigate future outbreaks of this pathogen.
Abstract in Spanish is available with online material
Wildlife diseases are contributing to the current Earth's sixth mass extinction; one disease, chytridiomycosis, has caused mass amphibian die-offs. While global spread of a hypervirulent lineage of the fungus Batrachochytrium dendrobatidis (BdGPL) causes unprecedented loss of vertebrate diversity by decimating amphibian populations, its impact on amphibian communities is highly variable across regions. Here, we combine field data with in vitro and in vivo trials that demonstrate the presence of a markedly diverse variety of low virulence isolates of BdGPL in northern European amphibian communities. Pre-exposure to some of these low virulence isolates protects against disease following subsequent exposure to highly virulent BdGPL in midwife toads (Alytes obstetricans) and alters infection dynamics of its sister species B. salamandrivorans in newts (Triturus marmoratus), but not in salamanders (Sala-mandra salamandra). The key role of pathogen virulence in the complex host-pathogen-environment interaction supports efforts to limit pathogen pollution in a globalized world.
The reliability of transferring species distribution models (SDMs) to new ranges and future climates has been widely debated. Biological invasions offer the unique opportunity to evaluate model transferability, as distribution data between species’ native and introduced ranges are geographically independent of each other. Here, we performed the first global quantitative synthesis of the spatial transferability of SDMs for 235 invasive species and assessed the association of model transferability with the focal invader, model choice and parameterisation. We found that SDMs had limited spatial transferability overall. However, model transferability was higher for terrestrial endotherms, species introduced from or to the Southern Hemisphere, and species introduced more recently. Model transferability was also positively associated with the number of presences for model calibration and evaluation, respectively, but negatively with the number of predictors. These findings highlight the importance of considering the characteristics of the focal invader, environment and modelling in the application and assessment of SDMs. This study is the first global quantitative synthesis of the spatial transferability of SDMs for invasive species. Spatial transferability was found to be limited overall, but was closely associated with the characteristics of the focal invader, environment and modelling approach.
The salamander plague, caused by the amphibian chytrid fungus Batrachochytrium salamandrivorans (Bsal), is one of the most devastating amphibian diseases, currently threatening the entire Western Palearctic caudate diversity with extinction. Apparently of Asian origin and recently introduced into Europe, Bsal is known from currently ca. 80 sites in the wild in four European countries. Germany is the Bsal 'hotspot' , with more than half (N = 50) of all known European records to date. We here present data based on > 8,500 caudate specimens sampled for Bsal mainly via skin swabbing and quantitative real time PCR (> 3,300 since 2019). Within regions of Bsal occurrence ~ 6-7% of the studied caudates were Bsal-positive. The oldest known European record of the pathogen is from this country (2004), but a massive Bsal dispersal has only been recognized within the last five years with 17 new Bsal sites since 2019 alone. Currently, Bsal is spreading within the northern and the southern Eifel and-since 2017-the Ruhr District. Most recently, the pathogen was for the first time detected in southern Germany (Bavaria) and a further range expansion is expected. A new species distribution model (SDM) of Bsal based on > 100 native and invasive records predicts suitable areas in most parts of Germany. Bsal affects all five caudate species known from these regions and has catastrophic effects on the European fire salamander (Salamandra salamandra). All affected populations in Germany (as well as Belgium and The Netherlands) have dramatically declined. While some may have become extinct due to the salamander plague, in most Bsal-positive sites European fire salamanders can still be recorded at low numbers (at least via systematic larval surveys), and at least one population seems to have recovered as currently Bsal detection remains negative. Little is known about the effect of Bsal on newts, and both prevalence and individual infection load can vary greatly over time, even within one population. However, the situation of the northern crested newt (Triturus cristatus) is alarming, as this species also undergoes declines due to Bsal invasions at some sites. Although some anurans are suggested as potential Bsal reservoirs and transmitters, we detected Bsal in only one individual of the common frog (Rana temporaria) out of 365 anurans of various species tested. Co-infection of Bsal with the related chytrid taxon Batrachochytrium dendrobatidis is known from three taxa (S. salamandra, T. cristatus, Ichthyosaura alpestris) and at four sites. The alarming data from Bsal in Germany call for immediate conservation action at all levels, including ex situ conservation. We therefore strongly support the establishment and implementation of a national Bsal Action Plan.
The salamander chytrid fungus (Batrachochytrium salamandrivorans [Bsal]) is causing massive mortality of salamanders in Europe. The potential for spread via international trade into North America and the high diversity of salamanders has catalyzed concern about Bsal in the U.S. Surveillance programs for invading pathogens must initially meet challenges that include low rates of occurrence on the landscape, low prevalence at a site, and imperfect detection of the diagnostic tests. We implemented a large-scale survey to determine if Bsal was present in North America designed to target taxa and localities where Bsal was determined highest risk to be present based on species susceptibility and geography. Our analysis included a Bayesian model to estimate the probability of occurrence of Bsal given our prior knowledge of the occurrence and prevalence of the pathogen. We failed to detect Bsal in any of 11,189 samples from 594 sites in 223 counties within 35 U.S. states and one site in Mexico. Our modeling indicates that Bsal is highly unlikely to occur within wild amphibians in the U.S. and suggests that the best proactive response is to continue mitigation efforts against the introduction and establishment of the disease and to develop plans to reduce impacts should Bsal establish.
The genus Chiropterotriton is endemic to Mexico with a geographical distribution along the Sierra Madre Oriental, the Trans Mexican Volcanic Belt and the Sierra de Juárez. The recent use of molecular tools has shown that Mexico’s amphibian diversity is highly underestimated, including a large number of cryptic, unnamed species. Chiropterotriton has 18 described species including terrestrial, arboreal and cave-dwelling species. In previous molecular studies, the presence of multiple undescribed species was evident. We present a phylogenetic hypothesis based on mitochondrial data, which includes all described species and six undescribed taxa. Based on the morphological analyses and, when available, combined with molecular data, we describe five new species of the genus; Chiropterotriton casasi sp. nov., C. ceronorum sp. nov., C. melipona sp. nov., C. perotensis sp. nov. and C. totonacus sp. nov. In addition, we redescribe two others: Chiropterotriton chiropterus and C. orculus, and provide a comparable account of one additional sympatric congener. This increases the number of species in the genus to 23, which represent a considerable component of Mexican plethodontid richness.
Batrachochytrium salamandrivorans (Bsal) is an emerging invasive pathogen that is highly pathogenic to salamander species. Modeling infection dynamics in this system can facilitate proactive efforts to mitigate this pathogen's impact on North American species. Given its widespread distribution and high abundance, the eastern newt (Notophthalmus viridescens) has the potential to significantly influence Bsal epidemiology. We designed experiments to 1) estimate contact rates given different host densities and habitat structure and 2) estimate the probability of transmission from infected to susceptible individuals. Using parameter estimates from data generated during these experiments, we modeled infection and disease outcomes for a population of newts using a system of differential equations. We found that host contact rates were density-dependent, and that adding habitat structure reduced contacts. The probability of Bsal transmission given contact between newts was very high (>90%) even at early stages of infection. Our simulations show rapid transmission of Bsal among individuals following pathogen introduction, with infection prevalence exceeding 90% within one month and >80% mortality of newts in three months. Estimates of basic reproductive rate (R0) of Bsal for eastern newts were 1.9 and 3.2 for complex and simple habitats, respectively. Although reducing host density and increasing habitat complexity might decrease transmission, these management strategies may be ineffective at stopping Bsal invasion in eastern newt populations due to this species’ hyper-susceptibility.
Scheele et al. (Reports, 29 March 2019, p. 1459) bring needed attention to the effects of amphibian infectious disease. However, the data and methods implicating the disease chytridiomycosis in 501 amphibian species declines are deficient. Which species are affected, and how many, remains a critical unanswered question. Amphibians are imperiled; protective actions require public support and robust science.
The chytrid fungus Batrachochytrium dendrobatidis has caused the most prominent loss of vertebrate diversity ever recorded, which peaked in the 1980s. Recent incursion by its sister species B. salamandrivorans in Europe raised the alarm for a new wave of declines and extinctions in western Palearctic urodeles. The European Commission has responded by restricting amphibian trade. However, private amphibian collections, the main end consumers, were exempted from the European legislation. Here, we report how invasion by a released, exotic newt coincided with B. salamandrivorans invasion at over 1000 km from the nearest natural outbreak site, causing mass mortality in indigenous marbled newts (Triturus marmoratus), and posing an acute threat to the survival of nearby populations of the most critically endangered European newt species (Montseny brook newt, Calotriton arnoldi). Disease management was initiated shortly after detection in a close collaboration between policy and science and included drastic on site measures and intensive disease surveillance. Despite these efforts, the disease is considered temporarily contained but not eradicated and continued efforts will be necessary to minimize the probability of further pathogen dispersal. This precedent demonstrates the importance of tackling wildlife diseases at an early stage using an integrated approach, involving all stakeholders and closing loopholes in existing regulations.
The emerging fungal pathogen, Batrachochytrium salamandrivorans (Bsal), is a significant conservation threat to salamander biodiversity in Europe, although its potential to affect North American species is poorly understood. We tested the susceptibility of two genera (Eurycea and Pseudotriton) and three populations of lungless salamanders (Plethodontidae) to Bsal. All species became infected with Bsal and two (Pseudotriton ruber and Eurycea wilderae) developed chytridiomycosis. We also documented that susceptibility of E. wilderae differed among populations. Regardless of susceptibility, all species reduced feeding when exposed to Bsal at the highest zoospore dose, and P. ruber and one population of E. wilderae used cover objects less. Our results indicate that Bsal invasion in eastern North America could have significant negative impacts on endemic lungless salamander populations. Future conservation efforts should include surveillance for Bsal in the wild and in captivity, and championing legislation that requires and subsidizes pathogen‐free trade of amphibians.
Chytridiomycosis caused by fungus Batrachochytrium dendrobatidis (Bd) is one of the decline global causes of amphibians. Currently, it is distributed throughout a broad range of climates and ecosystems around the world. An epidemic wave of chytridiomycosis began in North America, resulting in population decline and local extinction of many species, reconfiguring species composition of amphibian communities in the Americas. In Mexico, Bd has caused an amphibian population decrease, and its potential distribution area has not been determined. We reviewed the number of species infected, obtaining Bd frequency of infection by land use and vegetation type, and by elevation range. We examined the known distribution of Bd , estimated the potential distribution, and obtained the bioclimate variables relevant for Bd . Our results indicate that in Mexico, Bd has been detected in 78 species of amphibians in 10 families, from 29 different land use and vegetation types, with cloud forest having the highest number of cases (139) and infected species (15). Bd occurs over an elevation range of 1–3,300 m asl and is most frequent at 1,200–1,500 m asl (36%). In addition to the regions previously described as suitable for Bd , our model included desert, coastal, and tropical forest regions, revealing an increase in the area where amphibians could be at risk of infection. Distribution of Bd is mainly associated with temperature of the wettest quarter and potential evapotranspiration of the warmer quarter. We offer an estimate of the ideal conditions for Bd in Mexico, also information for future studies on Bd and the conservation of amphibians.
Abstract in Spanish is available with online material.
Batrachochytrium dendrobatidis (Bd) has been associated with the severe declines and extinctions of amphibians in Costa Rica that primarily occurred during the 1980s and 1990s. However, the current impact of Bd infection on amphibian species in Costa Rica is unknown. We aimed to update the list of amphibian species in Costa Rica and evaluate the prevalence and infection intensity of Bd infection across the country to aid in the development of effective conservation strategies for amphibians. We reviewed taxonomic lists and included new species descriptions and records for a total of 215 amphibian species in Costa Rica. We also sampled for Bd at nine localities from 2015–2018 and combined these data with additional Bd occurrence data from multiple studies conducted in amphibian communities across Costa Rica from 2005–2018. With this combined dataset, we found that Bd was common (overall infection rate of 23%) across regions and elevations, but infection intensity was below theoretical thresholds associated with mortality. Bd was also more prevalent in Caribbean lowlands and in terrestrial amphibians with an aquatic larval stage; meanwhile, infection load was the highest in direct-developing species (forest and stream-dwellers). Our findings can be used to prioritize regions and taxonomic groups for conservation strategies.
The infectious chytrid fungus Batrachochytrium salamandrivorans ( Bsal ) has been responsible for severe population declines of salamander populations in Europe. Serious population declines and loss of urodelan diversity may occur if appropriate action is not taken to mitigate against the further spread and impact of Bsal . We provide an overview of several potential mitigation methods, and describe their possible advantages and limitations. We conclude that long-term, context-dependent, multi-faceted approaches are needed to successfully mitigate adverse effects of Bsal , and that these approaches should be initiated pre-arrival of the pathogen. The establishment of ex situ assurance colonies, or management units, for species threatened with extinction, should be considered as soon as possible. While ex situ conservation and preventive measures aimed at improving biosecurity by limiting amphibian trade may be implemented quickly, major challenges that lie ahead are in designing in situ disease containment and mitigation post-arrival and in increasing public awareness.
Invasive fungal pathogens Batrachochytrium dendrobatidis (Bd) and B. salamandrivorans (Bsal) are causing mortality events and population declines in amphibians around the world. B. salamandrivorans has not been found in the Americas but is predicted to emerge there given the presence of competent hosts, high volume import pathways, and lack of effective biosecurity measures. Eastern newts (Notophthalmus viridescens) are the most abundant and widespread salamanders in United States with known susceptibility to both fungi. However, little is known about how their current Bd infections will interact with novel Bsal infections. Here, we ran a series of experiments in which we exposed newts to each fungal pathogen, combinations of both fungi, and three Bd isolates to: (1) determine if natural exposure to Bd provides protection against Bsal, (2) quantify the effect of co-infections on newt survival, and (3) examine if resistance responses are general to multiple lineages. We found that hosts exposed under simultaneous co-infections experienced 78% mortality over a period of 18 weeks, which was driven by the persistence of Bsal because newts cleared Bd infection within a month. In a subsequent experiment, resistant newts also resolved infections of three Bd genotypes, suggesting that the defense mechanism is effective across all lineages. However, re-exposing these individuals with a tenfold higher dose (10 ⁶ Bd zoospores) increased their susceptibility to Bsal, and 93% of them sustained Bsal infections. Our findings will improve the estimates of decline risk for a species that could serve as a potential superspreader of Bsal in North America.
The demise of amphibians?
Rapid spread of disease is a hazard in our interconnected world. The chytrid fungus Batrachochytrium dendrobatidis was identified in amphibian populations about 20 years ago and has caused death and species extinction at a global scale. Scheele et al. found that the fungus has caused declines in amphibian populations everywhere except at its origin in Asia (see the Perspective by Greenberg and Palen). A majority of species and populations are still experiencing decline, but there is evidence of limited recovery in some species. The analysis also suggests some conditions that predict resilience.
Science , this issue p. 1459 ; see also p. 1386
The recent decline in populations of European salamanders caused by the chytrid fungus Batrachochytrium salamandrivorans (Bsal) has generated worldwide concern, as it is a major threat to amphibians. Evaluation of the areas most suitable for the establishment of Bsal combined with analysis of the distribution of salamander species could be used to generate and implement biosecurity measures and protect biodiversity at sites with high salamander diversity. In this study, we identified the areas most suitable for the establishment of Bsal in Mexico. Mexico has the second-highest salamander species diversity in the world; thus, we identified areas moderately to highly suitable for the establishment of Bsal with high salamander diversity as potential hotspots for surveillance. Central and Southern Mexico were identified as high-risk zones, with 13 hotspots where 30% of Mexican salamander species occur, including range-restricted species and endangered species. We propose that these hotspots should be thoroughly monitored for the presence of Bsal to prevent the spread of the pathogen if it is introduced to the country.
Predictive models are central to many scientific disciplines and vital for informing management in a rapidly changing world. However, limited understanding of the accuracy and precision of models transferred to novel conditions (their ‘transferability’) undermines confidence in their predictions. Here, 50 experts identified priority knowledge gaps which, if filled, will most improve model transfers. These are summarized into six technical and six fundamental challenges, which underlie the combined need to intensify research on the determinants of ecological predictability, including species traits and data quality, and develop best practices for transferring models. Of high importance is the identification of a widely applicable set of transferability metrics, with appropriate tools to quantify the sources and impacts of prediction uncertainty under novel conditions.
Escalating occurrences of emerging infectious diseases underscore the importance of understanding microbiome-pathogen interactions. The amphibian cutaneous microbiome is widely studied for its potential to mitigate disease-mediated amphibian declines. Other microbial interactions in this system, however, have been largely neglected in the context of disease outbreaks. European fire salamanders have suffered dramatic population crashes as a result of the newly emerged Batrachochytrium salamandrivorans (Bsal). In this paper, we investigate microbial interactions on multiple fronts within this system. We show that wild, healthy fire salamanders maintain complex skin microbiotas containing Bsal-inhibitory members, but these community are present at a remarkably low abundance. Through experimentation, we show that increasing bacterial densities of Bsal-inhibiting bacteria via daily addition slowed disease progression in fire salamanders. Additionally, we find that experimental-Bsal infection elicited subtle changes in the skin microbiome, with selected opportunistic bacteria increasing in relative abundance resulting in septicemic events that coincide with extensive destruction of the epidermis. These results suggest that fire salamander skin, in natural settings, maintains bacterial communities at numbers too low to confer sufficient protection against Bsal, and, in fact, the native skin microbiota can constitute a source of opportunistic bacterial pathogens that contribute to pathogenesis. By shedding light on the complex interaction between the microbiome and a lethal pathogen, these data put the interplay between skin microbiomes and a wildlife disease into a new perspective.
Aim
Identifying hosts and regions susceptible to invasion by an emerged pathogen is vital to inform early risk assessments. We here show how differences between a pathogen's native and invasive observed niche and their underlying environments affect this process, using the recent emergence of Batrachochytrium salamandrivorans (Bsal) as a critical, empirical example.
Location
Palaearctic.
Methods
To quantify observed niches, we first gathered occurrences from the native Asian and invasive European distribution of Bsal. Through ordination in PCA‐bound environmental space, we then applied overlap tests to compare native and invasive Bsal niches with those of 56 putative Western Palaearctic host species. At last, we ensembled bivariate niche models (ESMs) for each Bsal niche to assess how differences in observed niches influenced suitability predictions.
Results
The observed invasive Bsal niche is a conservative, partially filled subset of its wider native niche. Pathogen–host overlap measured using the narrow invasive niche was nevertheless found to be significantly higher than that of the native niche, which is partly situated in subtropical conditions absent from the Western Palaearctic. ESMs created using the native niche predict high suitability for Bsal throughout Europe. Conversely, a more restricted range was predicted using the invasive niche, which coincides with the presence of oceanic climates in north‐western Europe and several Mediterranean mountain ranges.
Main conclusions
Unequal relative availability of environments in native and invasive ranges may lead to underestimation of observed niche overlap between native pathogen populations and putative hosts in the invasive range. The existence of partially filled niches may add uncertainty to overlap measurements, and predictions of potential further spread. Results based on the invasive niche therefore provide a conservative estimate; yet demonstrate, in our case, that Bsal is already present in conditions shared by numerous host species. Further niche filling may accordingly increase risk of salamander diversity across the Western Palaearctic.
Panzootic chytrid fungus out of Asia
Species in the fungal genus Batrachochytrium are responsible for severe declines in the populations of amphibians globally. The sources of these pathogens have been uncertain. O'Hanlon et al. used genomics on a panel of more than 200 isolates to trace the source of the frog pathogen B. dendrobatidis to a hyperdiverse hotspot in the Korean peninsula (see the Perspective by Lips). Over the past century, the trade in amphibian species has accelerated, and now all lineages of B. dendrobatidis occur in traded amphibians; the fungus has become ubiquitous and is diversifying rapidly.
Science , this issue p. 621 ; see also p. 604
The emergence of the chytrid fungus Batrachochytrium salamandrivorans (Bsal) represents a dramatic new threat to European amphibians. This skin pathogen causes skin lesions and ulcerations in European salamanders, eventually causing their death. Bsal first emerged in the Netherlands and Belgium where it caused mass mortality in populations of fire salamanders (Salamandra salamandra). As the affected sites were situated at less than 10 km distance from the German border, the occurrence of the pathogen was also to be expected in the adjacent Eifel region in Germany. Monitoring work to elucidate the possible occurrence of Bsal in Germany was started in 2014 by the universities of Trier and Braunschweig, along with the Biological Stations in Düren and Aachen. Salamanders and newts were systematically swabbed and screened for Bsal in the Northern (in the state of North Rhine-Westphalia, NRW) and Southern Eifel (Rhineland-Palatinate, RP). The sampling was complemented by 186 fire salamander swabs from other parts of NRW, Lower Saxony and Thuringia. While Bsal could not yet be detected in 2014, positive individuals were found at no less than four sites in the Northern Eifel in 2015. This number increased in the Northern Eifel to ten in 2017, distributed over almost the entire study region. At three further sites with formerly large fire salamander populations, almost no individuals could be observed in the study period, providing evidence for drastic declines. Besides fire salamanders, Bsal-infected individuals were also found for all newt species in the Northern Eifel and adjacent areas north of it (Ichthyosaura alpestris, Lissotriton helveticus, L. vulgaris, Triturus cristatus), partly in sites outside of the range of fire salamanders. In the Southern Eifel, no Bsal-positives were detected, but at numerous sites where fire salamander populations had been recorded in the 1990s, neither adults nor larvae could be found. Furthermore, in 2017, a second outbreak was confirmed around the city of Essen (in NRW, but > 70 km from the Eifel), including massive fire salamander mortality events, and it is unknown how the pathogen has reached this area. Clearly Bsal is on its way to become one of strongest and most imminent threats to the amphibian diversity of Europe. By expected range expansions from its current nuclei in the Netherlands, Belgium and Germany, but also driven by amphibian imports from its probable native range in Asia, this fungus might well push numerous populations and even species of newts and salamanders Europewide over the brink to extinction. To avoid such range expansions to be further expedited, field biologists are urged to keep to recommended hygiene standards, and to consider the danger of spreading this pathogen when translocating or reintroducing amphibians. We also call for immediate implementation of a better regulation of the amphibian trade, specifically for Germany, in order to ensure adequate quarantine, screening and treatment of imported amphibians
Species distribution models (SDMs) increasingly have been used to anticipate the spread of invasive species. However, these models are powerful conservation tools only if they are biologically relevant, and thus validation of these models is essential. Here, we evaluate four model selection frameworks for their ability to identify a best fit model of spread under low data conditions early in an invasion, specifically testing the efficacy of methods that utilize absence data in addition to presence data in evaluating models. We test this question using a simulation where we generated data with varying confidence in the accuracy of the absence data, as absences in early invasions may become presences in the future, and increasing quantity of observation data to test the models. We create these simulations based on a real-world example of a newly emergent, invasive fungal pathogen, Batrachochytrium salamandrivorans (Bsal). The simulation demonstrated that AIC and Likelihood consistently outperform both Kappa and AUC in selecting the true model as the best model when data are limited and absence data are low quality, with AIC providing the most conservative results due to penalties for overparameterization. With these results, we then used these techniques to compare five candidate models for predicting the spread of Bsal. Consistent with the simulation, the best fit model of the candidate models for Bsal was inconsistent across the four metrics. However, AIC, which performed best in the simulation study, suggested that the spread of Bsal into Western Europe was best predicted by a combination of bioclimatic suitability, salamander richness, and number of salamander imports. Our results highlight the difficulty in evaluating predictive models when data are limited and of low quality, as with a newly invasive species, but show that these challenges can be partially addressed with the appropriate model selection approach. Use of this approach is critical as SDMs of invasive species are often used to inform conservation policy and efforts before the invasion spreads, when limited data are available.
Understanding introduction routes for wildlife pathogens is vital for the development of threat abatement plans. The chytrid fungus Batrachochytrium salamandrivorans (Bsal) has recently emerged in Europe, where it is considered to be a serious threat for urodelan conservation. If the highly diverse Chinese urodelans were to constitute a Bsal reservoir, then the significant international trade in these species may vector Bsal into naïve urodelan communities. Here, we analyzed a total of 1,143 samples, representing 36 Chinese salamander species from 51 localities across southern China for the presence of Bsal. We found Bsal was present across a wide taxonomic, geographical, and environmental range. In particular, Bsal DNA was detected in 33 samples from the genera Cynops, Pachytriton, Paramesotriton, Tylototriton, and Andrias, including the heavily traded species Paramesotriton hongkongensis and Cynops orientalis. The true Bsal prevalence across our data set was estimated between 2% and 4%, with a maximum of 50% in a population of P. hongkongensis. Even at this overall relatively low Bsal prevalence, the exportation of millions of animals renders Bsal introduction in naïve, importing countries a near certainty, which calls for the urgent implementation of proper biosecurity in the international wildlife trade.
Amphibians are experiencing devastating population declines globally. A major driver is chytridiomycosis, an emerging infectious disease caused by the fungal pathogens Batrachochytrium dendrobatidis (Bd) and Batrachochytrium salamandrivorans (Bsal). Bd was described in 1999 and has been linked with declines since the 1970s, while Bsal is a more recently discovered pathogen that was described in 2013. It is hypothesized that Bsal originated in Asia and spread via international trade to Europe, where it has been linked to salamander die-offs. Trade in live amphibians thus represents a significant threat to global biodiversity in amphibians. We review the current state of knowledge regarding Bsal and describe the risk of Bsal spread. We discuss regional responses to Bsal and barriers that impede a rapid, coordinated global effort. The discovery of a second deadly emerging chytrid fungal pathogen in amphibians poses an opportunity for scientists, conservationists, and governments to improve global biosecurity and further protect humans and wildlife from a growing number of emerging infectious diseases.
Pathogen pollution has caused dramatic losses of amphibian diversity on a global scale. The recently emerged chytrid fungus Batrachochytrium salamandrivorans (Bsal) has been hypothesized to have its origin in Asian urodelan populations, from which it may have been introduced to Europe through the trade in live urodelans. We here show that Bsal is present on wild small-webbed fire-bellied toads (Bombina microdeladigitora) from Vietnam and on representatives of the same species that have recently been imported in Germany. This finding suggests that the installment of measures to mitigate the Bsal threat through the amphibian trade should not be limited to urodeles, but should equally take anurans into account. © 2017
The IUCN Red List of Ecosystems is a global framework for monitoring the status of ecosystems. It is part of the growing toolbox for assessing risks to biodiversity and aims to support conservation, resource use, and management decisions by identifying ecosystems most at risk of biodiversity loss. By targeting a level of biological organisation above species, the IUCN Red List of Ecosystems complements The IUCN Red List of Threatened Species™. The IUCN Red List of Ecosystems Categories and Criteria are designed to be: widely applicable across ecosystem types and geographical areas; transparent and scientifically rigorous; and easily understood by policy makers and the public.
The IUCN Red List of Ecosystems Categories and Criteria
The basis of the IUCN Red List of Ecosystems is the IUCN Red List of Ecosystems Categories and Criteria, a set of eight categories and five criteria that provide a consistent method for assessing the risk of ecosystem collapse. The eight categories of ecosystem risk are: Collapsed (CO), Critically Endangered (CR), Endangered (EN), Vulnerable (VU), Near Threatened (NT), Least Concern (LC), Data Deficient (DD), and Not Evaluated (NE).
The IUCN Red List of Ecosystems protocol comprises five rule-based criteria (A-E) for assigning ecosystems to a risk category. Two of these criteria assess spatial symptoms of ecosystem collapse: declining distribution (A) and restricted distribution (B). Two criteria assess functional symptoms of ecosystem collapse: environmental degradation (C) and disruption of biotic processes and interactions (D). Multiple threats and symptoms can be integrated in a model of ecosystem dynamics to produce quantitative estimates of the risk of collapse (E). The Guidelines include comprehensive sections to support application of each of the five criteria, including information on relevant theory, thresholds and examples.
Application and documentation standards
The Guidelines assist correct implementation of the IUCN Red List of Ecosystems Categories and Criteria by providing information on the development of the protocol and a detailed overview of the scientific foundations supporting the categories and criteria. They define assessment units (ecosystem types); define ecosystem collapse; discuss the influence of scale; and explain the structure of the risk assessment protocol. The Guidelines also provide detailed definitions of the terms used in the IUCN Red List of Ecosystems Categories and Criteria.
The Guidelines aim to support the practical implementation of the IUCN Red List of Ecosystems Categories and Criteria from subnational to global areas of assessment. The Guidelines therefore outline the necessary steps to: define the assessment area; define the unit under assessment; apply the criteria; and prepare the assessment documentation for peer review and publication. All the steps are illustrated with examples spanning a wide range of ecosystem types, geographical localities and levels of data availability.
The future of the IUCN Red List of Ecosystems
The IUCN Red List of Ecosystems programme will assess the global status of the world’s terrestrial, marine, freshwater and subterranean ecosystems. In addition, the programme aims to support the development of national and regional Red Lists to inform conservation planning and sustainable development. For more information on the IUCN Red List of Ecosystems please consult the IUCN Red List of Ecosystems website (www.iucnrle.org).
The recent arrival of Batrachochytrium salamandrivorans in Europe was followed by rapid expansion of its geographical distribution and host range, confirming the unprecedented threat that this chytrid fungus poses to western Palaearctic amphibians. Mitigating this hazard requires a thorough understanding of the pathogen's disease ecology that is driving the extinction process. Here, we monitored infection, disease and host population dynamics in a Belgian fire salamander (Salamandra salamandra) population for two years immediately after the first signs of infection. We show that arrival of this chytrid is associated with rapid population collapse without any sign of recovery, largely due to lack of increased resistance in the surviving salamanders and a demographic shift that prevents compensation for mortality. The pathogen adopts a dual transmission strategy, with environmentally resistant non-motile spores in addition to the motile spores identified in its sister species B. dendrobatidis. The fungus retains its virulence not only in water and soil, but also in anurans and less susceptible urodelan species that function as infection reservoirs. The combined characteristics of the disease ecology suggest that further expansion of this fungus will behave as a 'perfect storm' that is able to rapidly extirpate highly susceptible salamander populations across Europe.
The amphibian chytrid fungi, Batrachochytrium dendrobatidis (Bd) and B. salamandrivorans (Bsal), pose a major threat to amphibian biodiversity. Recent evidence suggests Southeast Asia as a potential cradle for both fungi, which likely resulted in widespread host-pathogen co-existence. We sampled 583 salamanders from 8 species across Vietnam in 55 locations for Bsal and Bd, determined scaled mass index as a proxy for fitness and collected environmental data. Bsal was found within 14 of the 55 habitats (2 of which it was detected in 2013), in 5 salamandrid species, with a prevalence of 2.92%. The globalized pandemic lineage of Bd was found within one pond on one species with a prevalence of 0.69%. Combined with a complete lack of correlation between infection and individual body condition and absence of indication of associated disease, this suggests low level pathogen endemism and Bsal and Bd co-existence with Vietnamese salamandrid populations. Bsal was more widespread than Bd, and occurs at temperatures higher than tolerated by the type strain, suggesting a wider thermal niche than currently known. Therefore, this study provides support for the hypothesis that these chytrid fungi may be endemic to Asia and that species within this region may act as a disease reservoir.
A new fungus, Batrachochytrium salamandrivorans (Bsal), was identified in wild populations of salamanders in The Netherlands, Belgium and in kept populations in Germany and UK. EFSA assessed the potential of Bsal to affect the health of wild and kept salamanders in the EU, the effectiveness and feasibility of a movement ban of traded salamanders, the validity, reliability and robustness of available diagnostic methods for Bsal detection, and possible alternative methods and feasible risk mitigation measures to ensure safe international and EU trade of salamanders and their products. Bsal was isolated and characterized in 2013 from a declining fire salamander (Salamandra salamandra) population in The Netherlands. Based on the available evidence, it is likely that Bsal is a sufficient cause for the death of Salamandra salamandra both in the laboratory and in the wild. Despite small sample sizes, the available experimental evidence indicates that Bsal is associated with disease and death in individuals of 12 European and 3 Asian Caudata, and with high mortality rate outbreaks in
kept salamanders. Bsal experimental infection was detected in individuals of at least one species pertaining to the families Salamandridae, Plethodontidae, Hynobiidae and Sirenidae. Movement bans constitute key risk mitigation measures to prevent pathogen spread into naïve areas and populations. The effectiveness of a movement ban is mainly dependent on the import volumes, possibility of Bsal to remain viable outside susceptible/tolerant species, and the capacity to limit illegal movements. Duplex real-time qPCR can be used to detect Bsal DNA, but has not been fully validated. Quarantining salamanders, enacting legislation that requires testing of animals to demonstrate freedom from Bsal, before movement can take place, restricting salamander movements, tracking all traded species, hygienic procedures/biosecurity measures before and during movements, and increasing public awareness are relevant measures for ensuring safe intra-EU and international trade of salamanders.
The chytrid fungus Batrachochytrium salamandrivorans (Bsal) is a dangerous pathogen to
salamanders and newts. Apparently native to Asia, it has recently been detected in Western
Europe where it is expected to spread and to have dramatic effects on naïve hosts.
Since 2010, Bsal has led to some catastrophic population declines of urodeles in the Netherlands
and Belgium. More recently, it has been discovered in additional, more distant sites
including sites in Germany. With the purpose to contribute to a better understanding of
Bsal, we modelled its potential distribution in its invasive European range to gain insights
about the factors driving this distribution. We computed Bsal Maxent models for two predictor
sets, which represent different temporal resolutions, using three different background
extents to account for different invasion stage scenarios. Beside `classical' bioclimate, we
employed weather data, which allowed us to emphasize predictors in accordance with the
known pathogen's biology. The most important predictors as well as spatial predictions varied
between invasion scenarios and predictor sets. The most reasonable model was based
on weather data and the scenario of a recent pathogen introduction. It identified temperature
predictors, which represent optimal growing conditions and heat limiting conditions, as
the most explaining drivers of the current distribution. This model also predicted large areas
in the study region as suitable for Bsal. The other models predicted considerably less, but
shared some areas which we interpreted as most likely high risk zones. Our results indicate
that growth relevant temperatures measured under laboratory conditions might also be relevant
on a macroecological scale, if predictors with a high temporal resolution and relevance
are used. Additionally, the conditions in our study area support the possibility of a
further Bsal spread, especially when considering that our models might tend to underestimate
the potential distribution of Bsal.
Chytridiomycosis is an emerging infectious disease of amphibians that affects over 700 species on all continents where amphibians occur. The amphibian–chytridiomycosis system is complex, and the response of any amphibian species to chytrid depends on many aspects of the ecology and evolutionary history of the amphibian, the genotype and phenotype of the fungus, and how the biological and physical environment can mediate that interaction. Impacts of chytridiomycosis on amphibians are varied; some species have been driven extinct, populations of others have declined severely, whereas still others have not obviously declined. Understanding patterns and mechanisms of amphibian responses to chytrids is critical for conservation and management. Robust estimates of population numbers are needed to identify species at risk, prioritize taxa for conservation actions, design management strategies for managing populations and species, and to develop effective measures to reduce impacts of chytrids on amphibians.
This article is part of the themed issue ‘Tackling emerging fungal threats to animal health, food security and ecosystem resilience’.
Batrachochytrium salamandrivorans (Bsal) is a virulent fungal pathogen that infects salamanders. It is implicated in the recent collapse of several populations of fire salamanders in Europe. This pathogen seems much like that of its sister species, Batrachochytrium dendrobatidis (Bd), the agent responsible for anuran extinctions and extirpations worldwide, and is considered to be an emerging global threat to salamander communities. Bsal thrives at temperatures found in many mountainous regions rich in salamander species; because of this, we have screened specimens of salamanders representing 17 species inhabiting mountain ranges in three continents: The Smoky Mountains, the Swiss Alps, and the Peruvian Andes. We screened 509 salamanders, with 192 representing New World salamanders that were never tested for Bsal previously. Bsal was not detected, and Bd was mostly present at low prevalence except for one site in the Andes.
Emerging fungal diseases can drive amphibian species to local extinction. During 2010-2016, we examined 1,921 urodeles in 3 European countries. Presence of the chytrid fungus Batrachochytrium salamandrivorans at new locations and in urodeles of different species expands the known geographic and host range of the fungus and underpins its imminent threat to biodiversity.
A newly identified fungal pathogen, Batrachochytrium salamandrivorans(Bsal), is responsible for mass mortality events and severe population declines in European salamanders. The eastern USA has the highest diversity of salamanders in the world and the introduction of this pathogen is likely to be devastating. Although data are inevitably limited for new pathogens, disease-risk assessments use best available data to inform management decisions. Using characteristics of Bsalecology, spatial data on imports and pet trade establishments, and salamander species diversity, we identify high-risk areas with both a high likelihood of introduction and severe consequences for local salamanders. We predict that the Pacific coast, southern Appalachian Mountains and mid-Atlantic regions will have the highest relative risk from Bsal. Management of invasive pathogens becomes difficult once they are established in wildlife populations; therefore, import restrictions to limit pathogen introduction and early detection through surveillance of high-risk areas are priorities for preventing the next crisis for North American salamanders.
Understanding the responses of naïve communities to the invasion of multihost pathogens requires accurate estimates of susceptibility across taxa. In the Americas, the likely emergence of a second amphibian pathogenic fungus (Batrachochytrium salamandrivorans, Bsal) calls for new ways of prioritizing disease mitigation among species due to the high diversity of naïve hosts with prior B. dendrobatidis (Bd) infections. Here, we applied the concept of pathogenic potential to quantify the virulence of chytrid fungi on naïve amphibians and evaluate species for conservation efforts in the event of an outbreak. The benefit of this measure is that it combines and summarizes the variation in disease effects into a single numerical index, allowing for comparisons across species, populations or groups of individuals that may inherently exhibit differences in susceptibility. As a proof of concept, we obtained standardized responses of disease severity by performing experimental infections with Bsal on five plethodontid salamanders from southeastern United States. Four out of five species carried natural infections of Bd at the start of the experiments. We showed that Bsal exhibited its highest value of pathogenic potential in a species that is already declining (Desmognathus auriculatus). We find that this index provides additional information beyond the standard measures of disease prevalence, intensity, and mortality, because it leveraged these disease parameters within each categorical group. Scientists and practitioners could use this measure to justify research, funding, trade, or conservation measures.
HIGHLIGHTS
• We evaluate the risk of infection by chytrid fungi in five species of salamanders.
• We apply the concept of pathogenic potential to compare across species.
• Chytrid invasion could threaten Desmognathus auriculatus and Eurycea cirrigera populations.
The fungal pathogen Batrachochytrium dendrobatidis ( Bd ) is implicated in global mass die-offs and declines in amphibians. In Mesoamerica, the Bd epidemic wave hypothesis is supported by detection of Bd in historic museum specimens collected over the last century, yet the timing and impact of the early stages of the wave remain poorly understood. Chiropterotriton magnipes , the only obligate troglodytic Neotropical salamander, was abundant in its small range in the decade following its description in 1965, but subsequently disappeared from known localities and was not seen for 34 years. Its decline is roughly coincident with that of other populations of Neotropical salamanders associated with the invasion and spread of Bd . To determine the presence and infection intensity of Bd on C. magnipes and sympatric amphibian species (which are also Bd hosts), we used a noninvasive sampling technique and qPCR assay to detect Bd on museum specimens of C. magnipes collected from 1952 to 2012, and from extant populations of C. magnipes and sympatric species of amphibians. We also tested for the presence of the recently discovered Batrachochytrium salamandivorans ( Bsal ), another fungal chytridiomycete pathogen of salamanders, using a similar technique specific for Bsal . We did not detect Bd in populations of C. magnipes before 1969, while Bd was detected at low to moderate prevalence just prior to and during declines. This pattern is consistent with Bd -caused epizootics followed by host declines and extirpations described in other hosts. We did not detect Bsal in any extant population of C. magnipes . We obtained one of the earliest positive records of the fungus to date in Latin America, providing additional historical evidence consistent with the Bd epidemic wave hypothesis. Genotyping results show that at least one population is currently infected with the Global Panzootic Lineage of Bd , but our genotyping of the historical positive samples was unsuccessful. The lack of large samples from some years and the difficulty in genotyping historical Bd samples illustrate some of the difficulties inherent in assigning causality to historical amphibian declines. These data also provide an important historical baseline for actions to preserve the few known remaining populations of C. magnipes .
Aim
The links between taxonomic, functional, and phylogenetic diversity and how these vary geographically are key to understanding how historical and contemporary processes have shaped communities at regional and local scales. Here, we evaluate the links between taxonomic, functional and phylogenetic diversity for the amphibians in the Continental Americas and how these vary geographically under an explicit hypothesis testing framework.
Location
Continental Americas.
Taxon
Amphibia.
Methods
We identify spatial disparities between biodiversity dimensions (taxonomic, functional and phylogenetic) using geographically weighted regressions. Based on these mismatches we examined whether different eco‐evolutionary processes would fit (competitive exclusion, habitat filtering, available ecological space, strong biotic interactions, speciation rates, and dispersion).
Results
We found extensive variation in spatial mismatches between the three dimensions of biodiversity examined here. In general, at higher latitudes, we detected relatively little phylogenetic diversity, suggesting rapid functional diversification from temperate clades. In contrast, at low latitudes, environmental filtering mechanisms appear to be restricting functional diversity.
Main conclusions
The geographical mismatches between dimensions of diversity suggest different eco‐evolutionary causes. Patterns of diversification across amphibian lineages demonstrate how different environments can have contrasting effects on the different dimensions of diversity, potentially leading to decoupling. Neither dimension of alpha diversity of amphibians is a general predictor for another, and thus, general explanations for amphibian diversity and evolution should be avoided. Nonetheless, these dimensions can provide critical insights about conservation measures that explicitly emphasize evolutionary history, functionality or classic species richness.
Genome size (C-value) can affect organismal traits across levels of biological organization from tissue complexity to metabolism. Neotropical salamanders show wide variation in genome and body sizes, including several clades with miniature species. Because miniaturization imposes strong constraints on morphology and development and because genome size is strongly correlated with cell size, we hypothesize that body size has played an important role in the evolution of genome size in bolitoglossine salamanders. If this hypothesis is correct, then genome size and body size should be correlated in this group. Using Feulgen image analysis densitometry, we estimated genome sizes for 60 species of Neotropical salamanders. We also estimated the “biological size” of species by comparing genome size and physical body sizes in a phylogenetic context. We found a significant correlation between C-value and physical body size using optimal regression with an Ornstein-Uhlenbeck model and report the smallest salamander genome found to date. Our index of biological size showed that some salamanders with large physical body size have smaller biological body size than some miniature species and that several clades demonstrate patterns of increased or decreased biological size compared with their physical size. Our results suggest a causal relationship between physical body size and genome size and show the importance of considering the impact of both on the biological size of organisms. Indeed, biological size may be a more appropriate measure than physical size when considering phenotypic consequences of genome size evolution in many groups.
As globalization lowers geographic barriers to movement, coinfection with novel and enzootic pathogens is increasingly likely. Novel and enzootic pathogens can interact synergistically or antagonistically, leading to increased or decreased disease severity. Here we examine host immune responses to coinfection with two closely related fungal pathogens: Batrachochytrium dendrobatidis (Bd) and Batrachochytrium salamandrivorans (Bsal). Both pathogens have had detrimental effects on amphibian populations, with Bd now largely enzootic, while Bsal is currently spreading and causing epizootics. Recent experimental work revealed that newts coinfected with Bd and Bsal had significantly higher mortality than those infected with either pathogen alone. Here we characterize host immunogenomic responses to chytrid coinfection relative to single infection. Across several classes of immune genes including pattern recognition receptors, cytokines, and MHC, coinfected host gene expression was weakly upregulated or comparable to that seen in single Bd infection, but significantly decreased when compared to Bsal infection. Combined with strong complement pathway downregulation and keratin upregulation, these results indicate that coinfection with Bd and Bsal compromises immune responses active against Bsal alone. As Bsal continues to invade naïve habitats where Bd is enzootic, coinfection will be increasingly common. If other Bd‐susceptible species in the region have similar responses, interactions between the two pathogens could cause severe population and community‐level declines.
Predator-prey interactions can impose strong selective pressures that scale up to affect the structure and function of communities and ecosystems. Salamanders are prey to a variety of predators that differ in their foraging tactics (e.g., specialists vs. generalists), morphologies, behaviors, and ecologies. Salamanders are an ideal group to explore and quantify patterns that may affect the evolution and persistence of defensive strategies. We examined patterns of predator diversity and body-size relationships of salamander species and their predators by compiling a database of observations documenting predator-prey interactions using natural history notes published in Herpetological Review (1975–2018), Herpetology Notes (2008–2018) and other outside sources. Our database contains 156 salamander predator-prey interactions comprised of 69 salamander species that were preyed upon by 89 predator species. Snakes were the most frequently reported predators (35% of predations reported), followed by salamanders (24%), and birds (16%). We found that snake predators consistently consumed salamander prey that was smaller than themselves, whereas invertebrate predators consumed salamanders across a broader body size range. Snakes are gape-limited predators and unable to eat prey that attain a certain size class, whereas invertebrate predators can use other tactics (e.g., use of venom, chewing mouthparts) to consume prey larger than themselves. These patterns can serve to help generate hypotheses on the evolution of defensive strategies in salamanders.
Aim
We examined the geographical distribution of functional diversity for American amphibians and tested the relationship between functional diversity and environment. We also explored how the functional evenness of life‐history traits varies across biogeographical regions.
Location
Continental Americas.
Methods
We performed a trait classification based on an Eltonian approach and calculated functional diversity using Hill numbers, Shannon and Gini–Simpson indices. We tested the relationship between functional diversity and different axes of environmental variation by using a series of spatial autoregressive (SAR) models.
Results
Based on 212 different functional attributes for 2,776 species, we found that functional diversity has a latitudinal gradient consistent with that of species richness, regardless of the diversity index used. Evenness of functional diversity of amphibian assemblages varies depending on the region, but in general they are close to the maximum possible value. Areas with more functional richness relative to species richness are associated with high annual precipitation and low precipitation seasonality regardless of temperature; in contrast, areas with fewer functions than expected are associated with high aridity.
Main conclusions
The highest functional diversity is located in mountainous regions. Overall, functional diversity is positively correlated with humid environments with low precipitation seasonality and low aridity regardless of temperature. This is especially relevant for amphibians facing contemporary climate change because it suggests that future variation in rainfall patterns, but not in annual mean temperature, might interact with functional diversity to pose an imminent threat to amphibian functional diversity.
“Phylogenetic diversity” and its abbreviation “PD” have now become popular terms describing a fundamental aspect of biodiversity based on phylogeny. After more than 25 years of work on PD (following the 1992 paper in Biological Conservation), methods and applications have explored a wide range of taxonomic groups and geographic scales. PD provides a way to address biodiversity at the level of features or characteristics of species, based on its well-corroborated model linking phylogeny and feature variation. The quantification of feature diversity justifies PD as a measure of option value – the value of living variation in keeping options open for society. This justification for PD in biodiversity conservation gives attention to often-neglected arguments for the value to society of biotic diversity. These largely global option values are complemented by the “insurance” value of PD at the local ecosystem scale. Microbial applications of PD, particularly in human health studies, have successfully implemented a range of PD calculations, including PD dissimilarities among samples. Reduced microbial PD in the human body may indicate reduced resilience, and it is now associated with many human diseases. “Macrobial” ecology has been less successful in integrating PD into a consistent coherent approach. Here, the traditional recognition of many “diversity” indices has been extended to phylogeny. PD as a “biodiversity” measure is confounded with the multitude of phylogeny-based diversity indices describing various ecological factors. Greater integration among the different areas of PD application could better establish PD as a core biodiversity measure, with a shared toolbox providing a range of PD-related calculations.
After more than fifteen years of existence, the R package ape has continuously grown its contents, and has been used by a growing community of users. The release of version 5.0 has marked a leap towards a modern software for evolutionary analyses. Efforts have been put to improve efficiency, flexibility, support for 'big data' (R's long vectors), ease of use, and quality check before a new release. These changes will hopefully make ape a useful software for the study of biodiversity and evolution in a context of increasing data quantity.
Availability:
ape is distributed through the Comprehensive R Archive Network: http://cran.r-project.org/package=apeFurther information may be found athttp://ape-package.ird.fr/.
Significance
Determining the drivers of extinction risk has been a key pursuit of conservation biology. Considering that body mass could be a strong predictor of extinction risk, we constructed a global database of body masses for 27,647 vertebrate species. Results show that the smallest- and largest-bodied vertebrates have elevated extinction risk. The largest vertebrates are mostly threatened by direct killing by humans, whereas the smallest species are more likely to have restricted geographic ranges—an important predictor of extinction risk—and be threatened by habitat degradation. Declines of large and small vertebrate species will truncate the size distributions characterizing these taxa, jeopardizing ecosystem services to humans, and generating cascading ecological and evolutionary effects on other species and processes.
Interest in, and opportunities to include functional and phylogenetic attributes of species in community ecology and biogeography are rapidly growing and seen as vital for the assessment of status and trends in biodiversity. However, the fundamental underlying evidence remains the (co-)occurrence of the biological units, such as species, in time and space and our ability to appropriately detect and quantify them. Here, we examine the implications of imperfect detection of species for functional and phylogenetic diversity (FD and PD) estimates. We explore how FD and PD might have different detectabilities than taxonomic diversity (TD) and how all three might vary differently along spatial and environmental gradients. We also extend occupancy modeling and dendrogram-based methods to address the imperfect detection of different biodiversity facets.
The Precautionary Principle is both celebrated and criticized. It has become an important principle for decision making, but it is also subject to criticism. One problem that is often pointed out with the principle is that is not clear what it actually says and how to use it. I have taken on this problem by performing an analysis of some of the most influential formulations of the principle in an attempt to identify the core ideas behind it, with the purpose of producing a formulation of the principle that is clear and practically applicable. It was found that what is called the Precautionary Principle is not a principle that tells us what do to achieve extra precaution or how to handle situations when extra precaution is called for. Instead, it was found to be a list of circumstances that each justify extra precaution. An analysis of some of the most common and influential formulations of the Precautionary Principle identified four such circumstances: (1) When we deal with important values that tend to be systematically downplayed by traditional decision methods - such as human health and the environment. (2) When we suspect that the decision might lead to irreversible and severe consequences and the values at stake are also irreplaceable, (3) When timing is at least as important as being right. (4) When it is more important to avoid false negatives than false positives. This interpretation of the Precautionary Principle does not say anything about what kind of actions to take when extra precaution is called for, but it does provide a clear and practically useful list of circumstances that call for extra precaution and that is not subject to the most common objections to the Precautionary Principle.