European Salamanders Research Articles

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

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

Divergent population responses following salamander mass mortalities and declines driven by the emerging pathogen Batrachochytrium salamandrivorans.

Understanding wildlife responses to novel threats is vital in counteracting biodiversity loss. The emerging pathogen Batrachochytrium salamandrivorans (Bsal) causes dramatic declines in European salamander populations, and is considered an imminent threat to global amphibian biodiversity. However, real-life disease outcomes remain largely uncharacterized. We performed a multidisciplinary assessment of the longer-term impacts of Bsal on highly susceptible fire salamander (Salamandra salamandra) populations, by comparing four of the earliest known outbreak sites to uninfected sites. Based on large-scale monitoring efforts, we found population persistence in strongly reduced abundances to over a decade after Bsal invasion, but also the extinction of an initially small-sized population. In turn, we found that host responses varied, and Bsal detection remained low, within surviving populations. Demographic analyses indicated an ongoing scarcity of large reproductive adults with potential for recruitment failure, while spatial comparisons indicated a population remnant persisting within aberrant habitat. Additionally, we detected no early signs of severe genetic deterioration, yet nor of increased host resistance. Beyond offering additional context to Bsal-driven salamander declines, results highlight how the impacts of emerging hypervirulent pathogens can be unpredictable and vary across different levels of biological complexity, and how limited pathogen detectability after population declines may complicate surveillance efforts.

Assessing the extinction risks of amphibians impacted by infectious diseases

Emerging infectious diseases (EIDs) are a major threat to amphibians worldwide. Determining the extinction risk of species susceptible to EIDs is challenging because of data limitations, especially in the initial stages of emergence and spread of disease. The fast rate of spread of many EIDs makes it necessary to assess the extinction risk of impacted host species before detailed mechanistic (epidemiological) or correlative (ecological niche) models can be developed. We present a simple method for identifying species that are at the highest risk of extinction due to an EID. Our method incorporates projections of the spatial spread of disease into IUCN Red List assessments under criteria A3 (based on future population reductions), D2 (plausible future threats), and E (probability of extinction). We apply this method to assess the extinction risk of salamander species in Europe susceptible to population declines caused by Batrachochytrium salamandrivorans (Bsal), the agent of the salamander plague. Our results indicate a high risk of extinction for European salamanders as a result of the spreading Bsal infection. Depending on the rate of spread from the current Bsal localities, and the emergence of new localities through human travel and transport, the number of species threatened by Bsal can range from a few to almost 30 of the 40 species that occur in Europe. Our method allows preliminary assessments of extinction risk based on limited information. For species at risk of extinction due to fast-spreading EIDs, it provides a pragmatic and precautionary solution until more realistic models can be developed.

Incorporating caudate species susceptibilities and climate change into models of Batrachochytrium salamandrivorans risk in the United States of America

Worldwide, amphibians are threatened by several factors including climate change and pathogens. One emerging fungal pathogen, Batrachochytrium salamandrivorans (Bsal) has caused die-offs of European salamander populations, representing a conservation concern for hotspots of salamander diversity in the United States of America (U.S.A). While Bsal has not been detected in the U.S.A., previous work has suggested high invasion potential. As species susceptibility to Bsal is temperature dependent, we expect climate change to impact Bsal risk, which has not been explored. Here, we used predicted changes in environmental conditions, species-specific susceptibility estimates, and novel approaches assessing introduction risks to estimate current and future Bsal invasion risk. To generate predictions, we used geospatial data representing introduction risks, species susceptibility, and climatic suitability. Across climatic scenarios, our models predicted greatest overall risk of Bsal emergence in the southeastern and northwestern U.S.A. Bsal climatic suitability was greatest in the northwest, whereas the greatest number of susceptible species was predicted in the southeast. Under future scenarios, we predicted that climatically suitable areas for Bsal will be reduced by 3–14 % under the most extreme climate model.

Habitat connectivity supports the local abundance of fire salamanders (Salamandra salamandra) but also the spread of Batrachochytrium salamandrivorans

ContextHabitat connectivity can stabilise animal populations by facilitating immigration and genetic exchange, but it increases the risk of infectious diseases being spread by hosts. Chytridiomycosis caused by Batrachochytrium salamandrivorans (Bsal) threatens European salamander diversity. The extent to which the connectivity of populations of fire salamanders (Salamandra salamandra) contributes to the spread of Bsal remains unclear.ObjectivesWe analysed the impact of habitat connectivity of fire salamanders on the spread of Bsal. Moreover, we show how local salamander abundance is associated with habitat connectivity over a five-year period.MethodsWe developed fire salamander habitat suitability models (HSMs) for the Eifel area (Germany), currently considered the core of the range of Bsal in Europe. Habitat models were used to calculate pairwise resistance between salamander occurrences to test whether Bsal presence and salamander abundance were associated with habitat connectivity.ResultsFire salamanders are widely distributed in the Eifel. Solid bedrock and topographic positioning were important predictors of stream suitability as breeding habitats, while deciduous forests and grassland cover determined overall fire salamander habitat suitability along with breeding habitat suitability. Bsal-positive salamander occurrences were better-connected than Bsal-negative or untested occurrences. Nevertheless, fire salamander larvae were more abundant in well-connected sites.ConclusionThe connection of salamander populations by suitable habitat seems to support local salamander abundance while facilitating the spread of Bsal. In situ conservation measures counteracting host species connectivity to interrupt Bsal transmission pathways must be implemented with caution, as they may weaken the demographic advantages of connectivity.

Widespread occurrence of Batrachochytrium dendrobatidis in Ontario, Canada, and predicted habitat suitability for the emerging Batrachochytrium salamandrivorans.

Chytridiomycosis, caused by the fungi Batrachochytrium dendrobatidis and Batrachochytrium salamandrivorans, is associated with massive amphibian mortality events worldwide and with some species’ extinctions. Previous ecological niche models suggest that B. dendrobatidis is not well‐suited to northern, temperate climates, but these predictions have often relied on datasets in which northern latitudes are underrepresented. Recent northern detections of B. dendrobatidis suggest that these models may have underestimated the suitability of higher latitudes for this fungus. We used qPCR to test for B. dendrobatidis in 1,041 non‐invasive epithelial swab samples from 18 species of amphibians collected across 735,345 km2 in Ontario and Akimiski Island (Nunavut), Canada. We detected the pathogen in 113 samples (10.9%) from 11 species. Only one specimen exhibited potential clinical signs of disease. We used these data to produce six Species Distribution Models of B. dendrobatidis, which classified half of the study area as potential habitat for the fungus. We also tested each sample for B. salamandrivorans, an emerging pathogen that is causing alarming declines in European salamanders, but is not yet detected in North America. We did not detect B. salamandrivorans in any of the samples, providing a baseline for future surveillance. We assessed the potential risk of future introduction by comparing salamander richness to temperature‐dependent mortality, predicted by a previous exposure study. Areas with the highest species diversity and predicted mortality risk extended 60,530 km2 across southern Ontario, highlighting the potential threat B. salamandrivorans poses to northern Nearctic amphibians. Preventing initial introduction will require coordinated, transboundary regulation of trade in amphibians (including frogs that can carry and disperse B. salamandrivorans), and surveillance of the pathways of introduction (e.g., water and wildlife). Our results can inform surveillance for both pathogens and efforts to mitigate the spread of chytridiomycosis through wild populations.

A New Disease Caused by an Unidentified Etiological Agent Affects European Salamanders.

Simple SummaryIn the last few years, multiple new infectious diseases have affected amphibians, causing unprecedented declines and extinctions at the global scale. Many of these diseases are caused by pathogens that have been described during recent decades. In this study we report a novel disease, affecting European amphibians. In a protected area of Northern Italy, since the autumn of 2013, we started to find some adult salamanders with cysts at the throat level (subgular region). Following this observation, we ran a regular monitoring of the salamander population and performed multiple morphological and molecular investigations to identify the cause of this undescribed disease. The cysts surround peculiar cells, probably protists, of about 30 µm covered by numerous motile cilia/undulipodia. Despite multiple attempts with a broad spectrum of techniques, the detailed identification remains challenging as we have been unable to match its features with previously described organisms. We provide the results achieved till now to promote a rapid dissemination on this new enigmatic wildlife pathogen and to create a basis for further and deeper studies.New pathologies are causing dramatic declines and extinctions of multiple amphibian species. In 2013, in one fire salamander population of Northern Italy, we found individuals with undescribed cysts at the throat level, a malady whose existence has not previously been reported in amphibians. With the aim of describing this novel disease, we performed repeated field surveys to assess the frequency of affected salamanders from 2014 to 2020, and integrated morphological, histological, and molecular analyses to identify the pathogen. The novel disease affected up to 22% of salamanders of the study population and started spreading to nearby populations. Cysts are formed by mucus surrounding protist-like cells about 30 µm long, characterized by numerous cilia/undulipodia. Morphological and genetic analyses did not yield a clear match with described organisms. The existence of this pathogen calls for the implementation of biosecurity protocols and more studies on the dynamics of transmission and the impact on wild populations.

Patterns, Mechanisms and Genetics of Speciation in Reptiles and Amphibians.

In this contribution, the aspects of reptile and amphibian speciation that emerged from research performed over the past decade are reviewed. First, this study assesses how patterns and processes of speciation depend on knowing the taxonomy of the group in question, and discuss how integrative taxonomy has contributed to speciation research in these groups. This study then reviews the research on different aspects of speciation in reptiles and amphibians, including biogeography and climatic niches, ecological speciation, the relationship between speciation rates and phenotypic traits, and genetics and genomics. Further, several case studies of speciation in reptiles and amphibians that exemplify many of these themes are discussed. These include studies of integrative taxonomy and biogeography in South American lizards, ecological speciation in European salamanders, speciation and phenotypic evolution in frogs and lizards. The final case study combines genomics and biogeography in tortoises. The field of amphibian and reptile speciation research has steadily moved forward from the assessment of geographic and ecological aspects, to incorporating other dimensions of speciation, such as genetic mechanisms and evolutionary forces. A higher degree of integration among all these dimensions emerges as a goal for future research.

Captivity and Infection by the Fungal Pathogen Batrachochytrium salamandrivorans Perturb the Amphibian Skin Microbiome.

The emerging fungal pathogen, Batrachochytrium salamandrivorans (Bsal) is responsible for the catastrophic decline of European salamanders and poses a threat to amphibians globally. The amphibian skin microbiome can influence disease outcome for several host-pathogen systems, yet little is known of its role in Bsal infection. In addition, many experimental in-vivo amphibian disease studies to date have relied on specimens that have been kept in captivity for long periods without considering the influence of environment on the microbiome and how this may impact the host response to pathogen exposure. We characterized the impact of captivity and exposure to Bsal on the skin bacterial and fungal communities of two co-occurring European newt species, the smooth newt, Lissotriton vulgaris and the great-crested newt, Triturus cristatus. We show that captivity led to significant losses in bacterial and fungal diversity of amphibian skin, which may be indicative of a decline in microbe-mediated protection. We further demonstrate that in both L. vulgaris and T. cristatus, Bsal infection was associated with changes in the composition of skin bacterial communities with possible negative consequences to host health. Our findings advance current understanding of the role of host-associated microbiota in Bsal infection and highlight important considerations for ex-situ amphibian conservation programmes.

Potential risk of Batrachochytrium salamandrivorans in Mexico.

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.

Efficacy of chemical disinfectants for the containment of the salamander chytrid fungus Batrachochytrium salamandrivorans.

The recently emerged chytrid fungus Batrachochytrium salamandrivorans (Bsal) causes European salamander declines. Proper hygiene protocols including disinfection procedures are crucial to prevent disease transmission. Here, the efficacy of chemical disinfectants in killing Bsal was evaluated. At all tested conditions, Biocidal®, Chloramine-T®, Dettol medical®, Disolol®, ethanol, F10®, Hibiscrub®, potassium permanganate, Safe4®, sodium hypochlorite, and Virkon S®, were effective at killing Bsal. Concentrations of 5% sodium chloride or lower, 0.01% peracetic acid and 0.001–1% copper sulphate were inactive against Bsal. None of the conditions tested for hydrogen peroxide affected Bsal viability, while it did kill Batrachochytrium dendrobatidis (Bd). For Bsal, enzymatic breakdown of hydrogen peroxide by catalases and specific morphological features (clustering of sporangia, development of new sporangia within the original sporangium), were identified as fungal factors altering susceptibility to several of the disinfectants tested. Based on the in vitro results we recommend 1% Virkon S®, 4% sodium hypochlorite and 70% ethanol for disinfecting equipment in the field, lab or captive setting, with a minimal contact time of 5 minutes for 1% Virkon S® and 1 minute for the latter disinfectants. These conditions not only efficiently target Bsal, but also Bd and Ranavirus.

Spatial variation in risk and consequence of Batrachochytrium salamandrivorans introduction in the USA.

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.

Amphibian chytridiomycosis: a review with focus on fungus-host interactions.

Amphibian declines and extinctions are emblematic for the current sixth mass extinction event. Infectious drivers of these declines include the recently emerged fungal pathogens Batrachochytrium dendrobatidis and Batrachochytrium salamandrivorans (Chytridiomycota). The skin disease caused by these fungi is named chytridiomycosis and affects the vital function of amphibian skin. Not all amphibians respond equally to infection and host responses might range from resistant, over tolerant to susceptible. The clinical outcome of infection is highly dependent on the amphibian host, the fungal virulence and environmental determinants. B. dendrobatidis infects the skin of a large range of anurans, urodeles and caecilians, whereas to date the host range of B. salamandrivorans seems limited to urodeles. So far, the epidemic of B. dendrobatidis is mainly limited to Australian, neotropical, South European and West American amphibians, while for B. salamandrivorans it is limited to European salamanders. Other striking differences between both fungi include gross pathology and thermal preferences. With this review we aim to provide the reader with a state-of-the art of host-pathogen interactions for both fungi, in which new data pertaining to the interaction of B. dendrobatidis and B. salamandrivorans with the host’s skin are integrated. Furthermore, we pinpoint areas in which more detailed studies are necessary or which have not received the attention they merit.Electronic supplementary materialThe online version of this article (doi:10.1186/s13567-015-0266-0) contains supplementary material, which is available to authorized users.

State of the World's Amphibians

The Anthropocene is characterized by a widespread biodiversity crisis that is rivaling prehistoric mass extinctions. Amphibians are the most threatened class of vertebrates. In addition to traditional threats such as land-use conversion and pollution, climate change and introduced diseases are expected to further reduce amphibian biodiversity. The fungal disease chytridiomycosis has caused the rapid extirpation of tens to possibly hundreds of amphibian species. Recent advances have revealed a deep evolutionary history and considerable variation in the virulence of strains of the fungal pathogen, patterns that need to be reconciled with the rapid spread of disease and demise of host populations. A conservation priority is surveillance of a newly discovered species of chytrid fungus that is killing European salamanders. The accelerated discovery of new amphibian species challenges existing conservation resources, but it is an opportunity to fill geographical gaps and to enhance programs aimed at preserving amphibian biodiversity.

Chytridiomycosis in Amphibians

Chytridiomycosis is an emerging fungal disease caused by members of the genus Batrachochytrium. Batrachochytrium dendrobatidis has been implicated in declines in wild amphibian populations worldwide. The pathogen is able to infect various groups of amphibians, including anurans, urodeles, and caecilians. B. dendrobatidis is one of the most common pathogens related to diseases in captive amphibian collections. A second species—Batrachochytrium salamandrivorans—was recently described as a threat for European salamanders, and appears to have originated in Asia where it is prevalent in Asian urodeles. This article presents an overview on the biology of these panzootic fungi, including pathology, diagnosis, and possible protocols for treatment and ecological aspects as well.

A new, yet old, threat to amphibians

Wildlife Disease Globally, populations of amphibians have been severely affected by a disease caused by the fungus Batrachochytrium dendrobatidis . Recently, some European salamander populations were decimated by the emergence of a new, related chytrid fungus, B. salamandrivorans . Martel et al. screened amphibians across continents. This newly emerging threat seems to have originated in Asia and traveled to Europe with salamanders transported as part of the pet trade. Asian salamanders have evolved resistance to the pathogen, but salamanders from other parts of the world are highly susceptible. Science , this issue p. [630][1] [1]: /lookup/volpage/346/630?iss=6209

Fungus from Asia threatens European salamanders

Fungus from Asia threatens European salamanders

Mechanisms of pigmentation loss in subterranean fishes

Troglobitic (exclusively subterranean) organisms usually present, among their apomorphies related to the subterranean life (troglomorphisms), the regression of eyes and melanic pigmentation. The degree of regression varies among species, from a slight reduction to the complete loss of eyes and dark pigmentation, without a taxonomic correlation. While mechanisms of eye reduction have been intensively investigated in some troglobites such as the Mexican blind tetra characins, genus Astyanax, and the European salamander, Proteus anguinus, few studies have focused on pigmentation. The Brazilian subterranean ichthyofauna distinguishes not only by the species richness (23 troglobitic fishes so far known) but also by the variation in the degree of reduction of eyes and pigmentation. This study focused on Brazilian fishes completely devoid of melanic pigmentation: the characiform Stygichthys typhlops (Characidae) and the siluriforms Ancistrus formoso (Loricariidae), Rhamdiopsis sp.1 (Heptapteridae; from caves in the Chapada Diamantina, Bahia) and Rhamdiopsis sp. 2 (cave in Campo Formoso, Bahia). In order to investigate if such depigmentation is the result of blockage in some step in the melanogenesis, in vitro tests of administration of L-DOPA were done, using caudal-fin fragments extracted from living fish. Except for Rhamdiopsis sp. 2, all the studied species were DOPA(+), i.e., melanin was synthesized after L-DOPA administration. This indicates these fish do have melanophores but they are unable to convert L-tyrosine to L-DOPA. On the other hand, Rhamdiopsis sp. 2, like the albino specimens of Trichomycterus itacarambiensis previously studied (which correspond to one third of the population), are DOPA(-), either because the block of melanin synthesis occurs downstream in melanogenesis, which is probably the case with T. itacarambiensis (monogenic system in view of the phenotypic discontinuity), or because the so-called albinos do no possess melanophores. The physiological loss in the ability to synthesize melanin, apparently caused by different genetic processes in DOPA(+) and in DOPA(-) fishes, may co-exist in subterranean populations with a decrease in the density of melanophores, as observed in the pigmented two thirds of T. itacarambiensis population, a morphological reduction apparently controlled by polygenic systems producing a continuous phenotypic variation.

Le salamandrine dagli occhiali,Salamandrina terdigitata (Lacépède, 1788) eS. perspicillata (Savi, 1821):1) differenziamento genetico ed ipotesi sulla loro storia evolutiva

Recent genetic investigations revealed the existence of two distinct species within the formerSalamandrina terdigitata, once considered the only representative of its Italian endemic genus. The pattern of genetic differentiation betweenSalamandrina terdigitata andS. perspicillata, as previously assessed with both allozyme and mitochondrial markers, was further analyzed and compared with that observed among congeneric species of European salamanders. Partial sequences of Cytochrome-b and 12S rRNA mtDNA genes were therefore obtained from four European species of the genusSalamandra. Genetic differentiation was particularly high within Salamandrina at mitochondrial level, with values of K2P divergence (17% and 6% for Cyt-b and 12S respectively) exceeding those of many other species of related salamander. The presence of aSalamandrina Miocenic fossil record from Sardinia suggests that the common ancestor ofS. terdigitata andS. perspicillata could have been a Corsica-Sardinian element. The present distribution and the depth of genetic divergence between the two species could be the result of a vicariance event, through the separation of the Calabro-Peloritan massif from Sardinia (7.8–8.6 Myr ago), followed by a subsequent dispersal event from the Corsica-Sardinia plate toward the continent during late Messinian (about 5–6 Myr ago), or through one of the Plio-Pleistocenic landbridges between the Corsica-Sardinia plate and the Tuscan Archipelago.

Faecal pellets used as an economic territorial marker in two terrestrial alpine salamanders

Scent marking is often related to activities associated with the occupation of a home range or territory. It is widely agreed that when an animal sends signals, this influences the decisions made by the animal that receives them. Scent marks are mainly used as a warning, in order to decrease the cost of territorial behaviour. They are deposited directly on a substrate by rubbing them on but also through urination and defecation. European terrestrial salamanders show high site fidelity and move very little around their shelter. Risks and costs are compared before an animal decides whether or not to leave its shelter, and a rapidly detectable and unambiguous cue in the direction of the home shelter reduces risk. Furthermore, territoriality has also been observed in amphibians, both in Anurans (frogs and toads) and Urodela (newts and salamanders). We tested the use of faecal pellets in alpine salamanders in the laboratory (Salamandra lanzai and Salamandra atra) with regard to homing and territorial behaviour. Our experimental design allowed us to distinguish attraction to from avoidance of shelters containing varying olfactory information. Our results clearly argue for the role faecal pellets play in shelter recognition. Furthermore, contrary to the results observed in other terrestrial salamanders such as Plethodontids, the faecal pellets of S. lanzai and S. atra enable intruders to identify the residents, thus fulfilling the requirements of a genuine territorial warning, as observed in mammals. Excrement marking is used as an economic tactic to identify and warn about the occupation of a territory in these two species of alpine salamanders.