Batrachochytrium salamandrivorans
(Bsal)

Batrachochytrium salamandrivorans (Bsal) is a single-celled fungus (closely related to B. dendrobatidis which has had serious effects on amphibian populations around the world) that infects Urodelans (newts and salamanders), causing a fatal skin disease in non-resistant species. It is native to south-east Asia where it infects native salamanders without causing significant disease. It has recently been introduced to Europe, probably with salamanders imported for the pet trade; after initial discovery in the Netherlands it has been found in neighbouring countries as well. It has caused very serious declines in populations of native host species in the areas where it is present. In view of its virulence and the fact that it appears to have a wide host range, it is feared that it could devastate European newt and salamander populations, and that it could have a similar effect in North America if it were to be introduced there.

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.

The risk of introducing Bsal is very high due to the high numbers of Asian salamanders traded to and within North America and Europe (Martel et al., 2014, Yap et al., 2015). Also, captive non-Asian salamanders like fire salamanders can be infected, as shown in Sabino-Pinto et al. (2015), which indicates that not only Asian urodelans should be treated with caution. For professional and private breeders it is of the utmost importance to dispose of waste water, substrate and other materials in an enclosure according to hygiene protocols as proposed by Cunningham et al. (2015), as water, other materials, or the escape or release of infected animals risk spreading the disease to wild populations (Cunningham et al, 2015; BC Inter-Ministry Invasive Species Working Group, undated). Human-mediated spread is also possible if people visit Bsal infected areas or handle amphibians and do not adhere to hygiene protocols such as disinfecting hands, field equipment, boots and so forth. (Price et al. (2016) provide evidence of the role of human activity in spreading another amphibian pathogen, namely ranaviruses). It is also possible that wild waterfowl could spread the disease (T. Stark, consultant, Netherlands, personal communication, 2016).

The virulence and host range of Bsal mean that it could devastate newt and salamander populations. In Europe up to 44 species of could be lost with this figure being significantly higher in the Americas -- this is no longer a problem limited to just the Netherlands, Belgium and Germany but could soon become a global problem. The Americas hold the highest urodelan diversity globally with nearly 50% of all species occurring on these continents; it is feared that if Bsal is introduced to the Americas it will devastate urodelan communities. Yap et al. (2015) published their findings and recommendations on preventing Bsal from entering North America. They created a map using a predictive model, identified suitable habitat for Bsal and overlapped this with areas with high salamander diversity. The most important high-risk zones are the south-eastern USA (Appalachian mountains), the Pacific Northwest, the Sierra Nevada mountain range and the highlands of Central Mexico. In addition, they identified the most likely entry points of Bsal, namely the US ports of Los Angeles, Tampa, New York, Atlanta, and San Francisco, which are all very near to these vulnerable zones. Between 2010 and 2014, 779,002 salamanders (99% from Asia) came through these ports. Three Asian species have been identified as carriers of Bsal: the blue-tailed fire-bellied newt (Cynops cyanurus [Hypselotriton cyanurus]), the Japanese fire-bellied newt (Cynops pyrrhogaster), and the Tam Dao salamander (Paramesotriton deloustali). These two genera account for 91% of salamanders imported to North America. Richgels et al. (2016) also use a predictive model to assess high risk areas, and identify the Pacific coast, southern Appalachians and Mid-Atlantic coast as areas that are most at risk. Gray et al. (2015) and Grant et al. (2016) also discuss the threats to American salamanders and the actions needed to prevent an outbreak of Bsal in the USA. A “Bsal Task Force” has been established and other measures such as a strategic action plan are under development.

In January 2016, the US Fish and Wildlife Service (UFWS) took action by imposing 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).

Much needs to be learned about the host range and host-pathogen interaction in Bsal’s native range.

In north-western Europe, in some locations where Bsal is present population declines appear absent even in a very susceptible species as the fire salamander (Salamandra salamandra) (Spitzen van der Sluijs et al., 2016); it is not yet known whether this is due to recent introduction which has not given declines time to happen or whether there are other reasons such as environmental factors.

How Bsal interacts with its host is not yet known in detail. Why it specifically affects Urodelans, how the pathogen establishes itself in the skin and induces death, possible immune responses (innate and acquired) and host susceptibility are all fields which require more investigation in the future (Rooij et al., 2015).

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