Wouter Beukema

Recent introduction of a chytrid fungus endangers Western Palearctic salamanders

A new, yet old, threat to amphibians 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 A new fungal disease from Asia threatens salamanders in Europe, the Middle East, and North Africa. Emerging infectious diseases are reducing biodiversity on a global scale. Recently, the emergence of the chytrid fungus Batrachochytrium salamandrivorans resulted in rapid declines in populations of European fire salamanders. Here, we screened more than 5000 amphibians from across four continents and combined experimental assessment of pathogenicity with phylogenetic methods to estimate the threat that this infection poses to amphibian diversity. Results show that B. salamandrivorans is restricted to, but highly pathogenic for, salamanders and newts (Urodela). The pathogen likely originated and remained in coexistence with a clade of salamander hosts for millions of years in Asia. As a result of globalization and lack of biosecurity, it has recently been introduced into naïve European amphibian populations, where it is currently causing biodiversity loss.

Expanding Distribution of Lethal Amphibian Fungus Batrachochytrium salamandrivorans in Europe.

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.

Resistance to Chytridiomycosis in European Plethodontid Salamanders of the Genus Speleomantes

North America and the neotropics harbor nearly all species of plethodontid salamanders. In contrast, this family of caudate amphibians is represented in Europe and Asia by two genera, Speleomantes and Karsenia, which are confined to small geographic ranges. Compared to neotropical and North American plethodontids, mortality attributed to chytridiomycosis caused by Batrachochytrium dendrobatidis (Bd) has not been reported for European plethodontids, despite the established presence of Bd in their geographic distribution. We determined the extent to which Bd is present in populations of all eight species of European Speleomantes and show that Bd was undetectable in 921 skin swabs. We then compared the susceptibility of one of these species, Speleomantes strinatii, to experimental infection with a highly virulent isolate of Bd (BdGPL), and compared this to the susceptible species Alytes muletensis. Whereas the inoculated A. muletensis developed increasing Bd-loads over a 4-week period, none of five exposed S. strinatii were colonized by Bd beyond 2 weeks post inoculation. Finally, we determined the extent to which skin secretions of Speleomantes species are capable of killing Bd. Skin secretions of seven Speleomantes species showed pronounced killing activity against Bd over 24 hours. In conclusion, the absence of Bd in Speleomantes combined with resistance to experimental chytridiomycosis and highly efficient skin defenses indicate that the genus Speleomantes is a taxon unlikely to decline due to Bd.

Area prioritization and performance evaluation of the conservation area network for the Moroccan herpetofauna: a preliminary assessment

The integration of spatial area prioritization algorithms and species distribution modelling has shown great promise in conservation planning in recent years. However, despite the fact that reptiles and amphibians have the highest threat status of all terrestrial vertebrates, these species are often under-represented in conservation planning. The Kingdom of Morocco possesses the richest and most varied herpetofauna in the Maghreb and the western Mediterranean, and is characterized by high species richness, endemism and number of European relict species. Despite the fact that Moroccan reptiles and amphibians have been the subject of numerous studies by a large number of international herpetologists since the beginning of the 20th century, few or none of these concerned their conservation. This study had three main objectives: (1) to identify those areas that harbour the highest species richness; (2) to evaluate the existing and proposed future ‘important biological and ecological sites’ (SIBES) conservation area network (CAN) with respect to their ability to protect the herpetofauna adequately; and (3) to identify priority areas into which the existing protected areas can be augmented. We used maximum-entropy species distribution modelling to run distribution models for 11 amphibian and 86 reptile species (27.6% endemics and 12.4% threatened) for which we had 2,170 single geographic records. A total of 97 models were used to create a richness map of the Moroccan herpetofauna and thereby detect both areas of high species richness and the distribution patterns of individual species. This map was subsequently used as a basis for performance evaluation of the CAN and area prioritization using the ConsNet conservation planning software initialized by “Rarity” first, while using representation targets of 5% and 10%. Additionally, the proposed future Moroccan CAN (SIBES) was evaluated in terms of its overlay and proximity with ConsNet solutions using visual interpretation and distance measurements in a GIS. Our results show that Moroccan herpetofauna is poorly protected under the existing and future CAN. Prioritization of areas shows that a major increase in conservation area is required to guarantee the persistence of individual herpetofauna species even with a global minimum representation target of only 10%. An increase of the existing CAN is especially needed along parts of the Atlantic coast, in the north-western Mediterranean region, on the north-eastern Moroccan coast, as well as in several areas in the Sahara, notably vast proportions of the Vallée du Haut and Bas Drâa.

Corresponding Mitochondrial DNA and Niche Divergence for Crested Newt Candidate Species

Genetic divergence of mitochondrial DNA does not necessarily correspond to reproductive isolation. However, if mitochondrial DNA lineages occupy separate segments of environmental space, this supports the notion of their evolutionary independence. We explore niche differentiation among three candidate species of crested newt (characterized by distinct mitochondrial DNA lineages) and interpret the results in the light of differences observed for recognized crested newt species. We quantify niche differences among all crested newt (candidate) species and test hypotheses regarding niche evolution, employing two ordination techniques (PCA-env and ENFA). Niche equivalency is rejected: all (candidate) species are found to occupy significantly different segments of environmental space. Furthermore, niche overlap values for the three candidate species are not significantly higher than those for the recognized species. As the three candidate crested newt species are, not only in terms of mitochondrial DNA genetic divergence, but also ecologically speaking, as diverged as the recognized crested newt species, our findings are in line with the hypothesis that they represent cryptic species. We address potential pitfalls of our methodology.

A SURVEY FOR BATRACHOCHYTRIUM DENDROBATIDIS IN ENDANGERED AND HIGHLY SUSCEPTIBLE VIETNAMESE SALAMANDERS (TYLOTOTRITON SPP.)

Until now, Asian amphibians appear to have largely escaped declines driven by chytridiomycosis. Vietnamese salamanders that belong to the genus Tylototriton are rare and have a patchy distribution in mountainous areas, falling within the proposed environmental envelope of chytrid infections, surrounded by Batrachochytrium dendrobatidis infected regions. If these salamanders are susceptible to chytridiomycosis, then their populations could be highly vulnerable after the introduction of B. dendrobatidis. Examination for the presence of the chytrid fungus in skin swabs from 19 Tylototriton asperrimus and 104 Tylototriton vietnamensis by using quantitative polymerase chain reaction was performed. Susceptibility of T. asperrimus to experimental infection by using the global panzootic lineage (BdGPL) strain of B. dendrobatidis was examined. The fungus was absent in all samples from all wild salamanders examined. Inoculation with the BdGPL strain resulted in mortality of all five inoculated salamanders within 3 weeks after inoculation with infected animals that manifested severe orthokeratotic hyperkeratosis, epidermal hyperplasia, and spongiosis. Although infection by B. dendrobatidis currently appears absent in Vietnamese Tylototriton populations, the rarity of these animals, their pronounced susceptibility to chytridiomycosis, an apparently suitable environmental context and increasing likelihood of the pathogen being introduced, together suggest the need of urgent measures to avoid future scenarios of extinction as witnessed in Central America and Australia.

Nomenclature, lectotype designation and type locality restriction for Amietophrynus mauritanicus (Schlegel, 1841) (Anura, Bufonidae)

As part of his function as assistant to the director of the Rijksmuseum van Natuurlijke Historie in Leiden, the Netherlands (RMNH, currently Naturalis Biodiversity Center), the German biologist Hermann Schlegel received several herpetological specimens from Algeria for identification purposes during the mid-19 th century. These specimens were sent to him by Moritz Wagner, who undertook an expedition to Algeria between 1836 and 1838 (Wagner et al. 2012). As part of the publication describing the specimens collected on this expedition, Schlegel (1841) provided a description and diagnosis of Amietophrynus mauritanicus (Schlegel 1841) mainly based on a single specimen which is still extant in the RMNH. This specimen was treated as holotype by M. S. Hoogmoed in Frost (1985). During a recent appraisal of historical documentation dealing with north-west African amphibians (Beukema et al. 2013) we came across the account of Schlegel (1841) describing A. mauritanicus , and noticed the following issues; (i) Schlegel did not intend to describe A. mauritanicus as a new species; (ii) a single specimen is described in detail, but it is obvious from the description that it was based on multiple observed individuals; (iii) there is confusion on the type locality, which has been described to comprise multiple regions (e.g. Frost 2012) despite the assumed presence of only a single type specimen; (iv) Schlegel is shown as sole author while the account is in the plural (i.e. ‘wir’ – see also Wagner et al . 2012). Herein, we address these issues, provide a lectotype designation and restrict the type locality of A. mauritanicus following the International Code of Zoological Nomenclature (ICZN 1999).