Batrachochytrium salamandrivorans infection

In Bsal’s native range it is known to (non-lethally) infect a number of urodelan species. In Japan it has been found in at least five wild host species: Cynops ensicauda, Cynops pyrrhogaster, Hynobius nebulosus, Onychodactylus japonicus and Salamandrella keyserlingii (Martel et al., 2014). Samples collected in Thailand revealed at least one wild host species, Tylototriton uyenoi, and those in Vietnam three: Paramesotriton deloustali, Tylototriton ziegleri and Tylototriton vietnamensis (Martel et al., 2014). In the latter species Bsal has not been detected (directly) in wild specimens but in captive ones that originated from Vietnam (imported in 2010). In addition, Martel et al. (2014) tested 27 south-east Asian urodelans from China, Japan, Laos, Thailand and Vietnam; all tested negative for Bsal, as did 21 Vietnamese anuran species tested in the same study. These taxa coevolved with Bsal, which seems to be a urodelan specialist, and are able to tolerate or clear the infection, thus effectively functioning as host-reservoirs (Martel et al., 2014). The Chinese species Hypselotriton cyanurus has been experimentally infected in captivity and is able to act as an asymptomatic carrier, although Bsal has not been found in China (Martel et al., 2014).

In the wild in the introduced range, the north-western European urodelans Salamandra salamandra terrestris, Ichthyosaura alpestris and Lissotriton vulgaris are known hosts (Martel et al., 2014; Spitzen-van der Sluijs et al., 2016). In laboratory trials a wide range of European urodelans (although not Lissotriton helveticus) will develop lethal chytridiomycosis after being inoculated with Bsal or housed together with infected Asian urodelans (Martel et al., 2014). In a captive salamander collection in Germany, Bsal caused a mass mortality of captive Salamandra species: Salamandra algira from North Africa, S. corsica from Corsica, S. infraimmaculata from the Near East and S. salamandra and its twelve sub species which can be found throughout large parts of Europe (from Portugal to the Ukraine) (Sabino-Pinto et al., 2015). This study shows that these four species and at least nine (but likely all) of the subspecies of S. salamandra are highly susceptible to this disease., Bsal induced mortality has also been reported in captive Speleomantes spp. (Cunningham et al., 2015; Sabino-Pinto et al., 2015). In the coming years it is likely that more host species in Bsal’s native and naturalized range will be identified.

Bsal has not so far been detected in any species from the Americas, but it is feared that they will be susceptible and that if the disease is introduced to the Americas it will devastate urodelan communities (Yap et al., 2015).

Unlike its congener Bd, Bsal only seems to infect urodelans. Despite laboratory trials to infect anurans and caecilians, only urodelans, especially non-Asian members of the family Salamandridae, seem to be highly susceptible and develop lethal chytridiomycosis (Martel et al., 2014).

Native Distribution

The native distribution of Batrachochytrium salamandrivorans (hereafter Bsal) is thought to lie in south-east Asia (Martel et al., 2014). In this region the pathogen, which diverged from its sister species Batrachochytrium dendrobatidis 67.3 million years ago, coevolved with the native urodelans, exists at low levels and does not cause apparent population declines. In Japan Bsal has been found in at least five wild host species. Samples collected in Thailand revealed at least one wild host species and those from Vietnam three. In addition Martel et al. (2014) tested 27 other species of south-east Asian urodelans from China, Japan, Laos, Thailand and Vietnam. All tested negative for Bsal. The oldest evidence of Bsal presence in Asian urodelans comes from a museum specimen of Cynops ensicauda, a species restricted to the Amami and Okinawa islands in southern Japan (Martel et al., 2014); the specimen is at least 150 years old. Zhu et al. (2014) sampled China extensively for Bsal presence; a total of 665 anurans and urodelans from wild populations, archived museum specimens and samples taken at food markets and farms in 15 Chinese provinces were tested but failed to detect Bsal.

It is suspected that both the distribution and host range of Bsal in its native range are larger than currently known.

Northern Europe

Bsal was originally detected in the southern Netherlands, and in 2013 and 2014 in several locations in nearby parts of Belgium (Martel et al., 2014). In a recent studythe distribution of Bsal in north-western Europe was examined by testing 1921 urodelans in 2010-2016. This study demonstrated a substantial range extension in wild urodelans in the Netherlands, Belgium and Germany (Spitzen-van der Sluijs et al., 2016) -- the current range of Bsal in these three countries may be up to approximately 10,000 km². A survey conducted to detect the presence of Bsal in fire salamander (Salamandra salamandra terrestris) populations in Austria in the vicinity of Salzburg failed to detect the pathogen (Gimeno et al., 2015).

The Americas

Bsal has not as yet been detected in the Americas, but it is feared that if it is introduced there it will devastate urodelan communities.  Bales et al. (2015) conducted surveys to detect Batrachochytrium dendrobatidis (Bd) and Bsal in Cryptobranchus alleganiensis alleganiensis in Ohio, New York, Pennsylvania and Virginia; Bd was detected but not Bsal. Martel et al. (2014) tested samples of 16 anuran and 21 urodelan species collected in Arizona (2009), New York (2011), Tennessee (2009-2011) and Illinois (2008-2011), which all tested negative, as did samples of 65 anuran and one urodelan species from Panama collected in 2007-2008.

Captivity

Bsal has been detected in a salamander collection in Germany after causing a mass mortality of captive Salamandra species (Sabino-Pinto et al., 2015). Recently it was detected in the UK in quarantined amphibians (Speleomantes spp.) which were newly acquired from a UK amphibian breeder by a zoological collection (Cunningham et al., 2015). The infected animals either died while in quarantine or were euthanized to prevent any further spread of the disease.

As the results of Martel et al. (2014) and other studies have shown, it is likely that Bsal may be present in more captive populations.

Clinical signs include excessive shedding of the skin, ataxia, apathy and ultimately death (Martel et al., 2013). Histology, immunohistochemistry and PCR all provide good detection methods for Bsal. In order to rapidly detect its presence, PCR primers were created by Martel et al. (2013). Noninvasive skin samples can be taken in the field or captivity by means of skin swabbing and stored for later analysis. Blooi et al. (2013) developed a duplex real-time PCR that detects Bd and Bsal simultaneously with specific primers and probes. White et al. (2016) provide a case definition and diagnostic criteria for Bsal.

Once Bsal is established in the wild it is currently not possible to clear it from an infected area, which makes it particularly important to prevent its introduction.

Monitoring to detect it has been implemented in the Netherlands, Belgium, Germany, Austria and France,  and it is expected that more European countries will follow suit (Gimeno et al., 2015; Spitzen-van der Sluijs, 2016; Association Française des Etablissements Publics Territoriaux de Bassin, 2016). In the United States, monitoring and surveillance is also recommended (Grant et al., 2016) and an online portal (see Links to Websites table) to report diseased or dead salamanders is already online to ensure early detection (Kolby, 2015). Hygienic field protocols, as are used for Bd and Ranavirus, can be used to limit the spread of Bsal from one area to another (Cunningham et al., 2015).

One of the most effective prevention measures is probably a ban on import of (Asian) salamanders. In January 2016, the US Fish and Wildlife Service (UFWS) took action by introducing a temporary moratorium on the importation of 201 species of salamanders which they saw as being ‘injurious’ to native salamanders. It is hoped that this ban will help prevent the introduction of Bsal to the US. The Standing Committee of the Bern Convention has recommended that there should be a similar ban in Europe (Standing Committee to the Convention on the Conservation of European Wildlife and Natural Habitats, 2015); in February 2016 a letter was sent to the European Commission by 17 scientists and 27 nature organisations asking for the immediate implementation of this recommendation, and for the listing of Bsal as a pathogen of Union concern under the animal health legislation. Switzerland has already banned the import of salamanders and newts (Schmidt, 2016).

Another potential control measure is the use of certificates, validated by a veterinarian, to prove that an animal has been treated and is free of the disease before it is allowed to be sold, although this does have some disadvantages as well (A. Spitzen-van der Sluijs, RAVON, Nijmegen, Netherlands, personal communication, 2016).

Professional and amateur keepers and breeders of Urodelans are advised not to let animals escape or introduce them in native urodelan communities. Waste water and other materials from an enclosure should be treated with a bleach or Virkon S solution to clear these substances of pathogens before disposal. New animals should be quarantined for at least one month and, if the thermal preferences of the species allow, receive a temperature treatment as described in Blooi et al. (2015a) or a combined treatment with fungicides and high temperature (Blooi et al., 2015b).

Grant et al. (2016) describe a plan for a rapid and effective response if Bsal were to be introduced in the United States which is a urodelan biodiversity hot spot.

Belgium: Wildlife Disease Research Group, Ghent University, Department of Pathology, Bacteriology and Poultry Diseases, Salisburylaan 133, 9820 Merelbeke, http://www.treedivbelgium.ugent.be/pe_pathology.html

Germany: Technische Universität Braunschweig, Zoological Institute, Mendelssohnstr. 4, 38106 Braunschweig, http://www.zoologie.tu-bs.de/

Germany: Trier University Faculty of Regional and Environmental Sciences, Department of Biogeography, 54286 Trier, https://www.uni-trier.de/index.php?id=15675

Netherlands: RAVON, Toernooiveld 1, 6525 ED Nijmegen, http://www.ravon.nl/

USA: Vredenburg Lab, San Francisco State University, 1600 Holloway Ave, Department of Biology, SF State University, San Francisco, CA 94132, http://www.vredenburglab.com/

04/04/2016 Original text by:

Tariq Stark, consultant, Netherlands