Batrachochytrium salamandrivorans (Bsal)
- Summary of Invasiveness
- Taxonomic Tree
- Notes on Taxonomy and Nomenclature
- Distribution Table
- History of Introduction and Spread
- Risk of Introduction
- Pathogen Characteristics
- Latitude/Altitude Ranges
- Air Temperature
- Impact Summary
- Economic Impact
- Environmental Impact
- Threatened Species
- Risk and Impact Factors
- Gaps in Knowledge/Research Needs
- Links to Websites
- Distribution Maps
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PicturesTop of page
IdentityTop of page
Preferred Scientific Name
- Batrachochytrium salamandrivorans Martel et al., 2013
Preferred Common Name
International Common Names
- English: Bs; Eater of Salamanders
Local Common Names
- Germany: Salamander-Chytrid Pilz
Summary of InvasivenessTop of page
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.
Taxonomic TreeTop of page
- Domain: Eukaryota
- Kingdom: Fungi
- Phylum: Chytridiomycota
- Class: Chytridiomycetes
- Order: Rhizophydiales
- Genus: Batrachochytrium
- Species: Batrachochytrium salamandrivorans
Notes on Taxonomy and NomenclatureTop of page
Batrachochytrium salamandrivorans (Bsal) is closely related to its congener B. dendrobatidis (Bd). Divergence occurred approximately 67.3 million years ago. The species name refers to the destructive and deadly growth on urodelan skin. The holotype (AMFP13/1) was isolated from a fire salamander (Salamandra salamandra terrestris) and deposited at Ghent University, Belgium, where it is kept in liquid nitrogen (Martel et al., 2013).
DistributionTop of page
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.
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).
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.
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.
Distribution TableTop of page
The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.
|Continent/Country/Region||Distribution||Last Reported||Origin||First Reported||Invasive||Reference||Notes|
|Japan||Present||Native||Not invasive||Martel et al., 2014||Endemic in at least five host species|
|Thailand||Present||Native||Not invasive||Martel et al., 2014||Endemic in at least one host species|
|Vietnam||Present||Native||Not invasive||Martel et al., 2014||Endemic in at least three host species|
|Belgium||Present||Introduced||Invasive||Martel et al., 2014|
|Germany||Present||Introduced||Invasive||Spitzen-van der Sluijs et al., 2016|
|Netherlands||Present||Introduced||Invasive||Martel et al., 2013|
|UK||Absent, intercepted only||Introduced||Cunningham et al., 2015|
History of Introduction and SpreadTop of page
Bsal is believed to originate from South East Asia where it has coevolved with the native urodelans. Globalization and the international pet trade in Asian salamanders have probably led to its introduction to north-western Europe (Martel et al., 2014); it could have reached wild hosts by means of waste water from an enclosure with captive Asian salamanders or via escaped/released individuals. 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.
The disease was first noticed in the southern Netherlands, where three small but otherwise healthy populations of fire salamanders (Salamandra salamandra terrestris), the only ones in the country, used to be present. Steep declines were noticed from 2008/2010, continuing to the present day (Spitzen-van der Sluijs et al., 2013; Spitzen-van der Sluijs et al., 2016). A well monitored population in a forest remnant called “Bunderbos” in the Netherlands has declined by 99.99% (Spitzen-van der Sluijs et al., 2016). Deaths and population declines in fire salamanders were noticed in 2013 and 2014 in several locations in Belgium, near the Dutch outbreak sites (Martel et al., 2014). Infected and dead alpine newts (Ichthyosaura alpestris) were also found in Belgium at this time (Martel et al., 2014).
In a recent study (Spitzen-van der Sluijs et al., 2016) the distribution of Bsal in north-western Europe has been examined by testing 1921 urodelans in 2010-2016. This demonstrated a substantial range extension in wild Urodelans in the Netherlands, Belgium and Germany -- the current range of Bsal in these three countries may be up to approximately 10,000 km2. In addition this study has shown that the host range encompasses not only fire salamanders and alpine newts but also smooth newts (Lissotriton vulgaris). A survey conducted to detect the presence of Bsal in fire salamander populations in Austria in the vicinity of Salzburg failed to detect the pathogen (Gimeno et al., 2015).
Bsal has been 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.
The Americas, which are a hotspot for urodelan biodiversity and until very recently imported the same Asian salamanders, are also at risk (Yap et al., 2015; Richgels et al., 2016), although the pathogen has not so far been found there.
IntroductionsTop of page
|Introduced to||Introduced from||Year||Reason||Introduced by||Established in wild through||References||Notes|
|Natural reproduction||Continuous restocking|
|Belgium||South East Asia||Pet trade (pathway cause)||Yes||Martel et al. (2014)||Probably via trade in Asian salamanders|
|Germany||South East Asia||Pet trade (pathway cause)||Yes||Martel et al. (2014)||Probably via trade in Asian salamanders|
|Netherlands||South East Asia||2010||Pet trade (pathway cause)||Yes||Martel et al. (2014)||Probably via trade in Asian salamanders|
Risk of IntroductionTop of page
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).
Pathogen CharacteristicsTop of page
B. salamandrivorans (Bsal) belongs like its congener B. dendrobatidis (Bd) to the primitive single celled eukaryote phylum Chytridiomycota (Berger et al., 1998; Martel et al., 2013). This novel chytrid fungus has, like Bd, two main life stages: a zoospore which is motile and propelled by a single posteriorly directed flagellum, and the thallus which is the reproductive body and asexually produces zoospores (Longcore et al., 1999; Martel et al., 2013). The latter is also referred to as the zoosporangium. Bsal grows well in tryptone-gelatine hydrolysate-lactose (TGhL) or in broth containing peptonized milk, tryptone and glucose (PmTG). In vitro thalli are mostly monocentric but can be colonial as well. Rhizoids are fine and isodiametric and extend from several or a single area. Zoosporangium diameter ranges from 15.7-50.3 μm with an average of 27.9 μm. Motile zoospores are fairly spherical and have a diameter of 4.0-5.5 μm with an average of 4.6 μm. In the epidermis of amphibians, Bsal forms predominantly colonial thalli which contain several walled sporangia. Diameter of thalli located in keratinocytes ranges from 6.9-17.2 μm (average 12.2 ± 1.9 μm). Zoospore ultrastructure is very similar to that of Bd (Martel et al., 2013).
Sexual reproduction has not been observed in Bsal as yet. The life cycle of Bsal in amphibian skin is presumed to be similar to that of Bd, but has not yet been illustrated in detail (Rooij et al., 2015). Currently Bsal is only known to affect urodelans despite laboratory trials attempting to infect midwife toads (Alytes obestetricans) and caecilians (Martel et al., 2013; Martel et al., 2014). Surveys of wild anurans in Bsal’s native range in south-east Asia failed to detect the presence of the pathogen, suggesting that it is restricted to urodelans (Zhu et al., 2014). Bsal has markedly different thermal preferences from Bd. Optimal growth temperatures for Bsal lie between 10 and 15 °C and it can still continue to grow at a temperature of 5 °C (Martel et al., 2013). Temperatures of 25 °C and higher are lethal (Blooi et al., 2015a). (The host species in Thailand and Vietnam mostly live at fairly high altitudes). Bsal grows not only on keratin in amphibian skin but also on keratinous toe squamae of wild geese (Rooij et al., 2015). How Bsal survives outside of the skin of the host is not yet known (Rooij et al., 2015).
ClimateTop of page
|C - Temperate/Mesothermal climate||Tolerated||Average temp. of coldest month > 0°C and < 18°C, mean warmest month > 10°C|
|Cf - Warm temperate climate, wet all year||Tolerated||Warm average temp. > 10°C, Cold average temp. > 0°C, wet all year|
|Cs - Warm temperate climate with dry summer||Tolerated||Warm average temp. > 10°C, Cold average temp. > 0°C, dry summers|
|Cw - Warm temperate climate with dry winter||Tolerated||Warm temperate climate with dry winter (Warm average temp. > 10°C, Cold average temp. > 0°C, dry winters)|
|Df - Continental climate, wet all year||Preferred||Continental climate, wet all year (Warm average temp. > 10°C, coldest month < 0°C, wet all year)|
|Ds - Continental climate with dry summer||Tolerated||Continental climate with dry summer (Warm average temp. > 10°C, coldest month < 0°C, dry summers)|
|Dw - Continental climate with dry winter||Tolerated||Continental climate with dry winter (Warm average temp. > 10°C, coldest month < 0°C, dry winters)|
Latitude/Altitude RangesTop of page
|Latitude North (°N)||Latitude South (°S)||Altitude Lower (m)||Altitude Upper (m)|
Air TemperatureTop of page
|Parameter||Lower limit||Upper limit|
|Mean annual temperature (ºC)||5||25|
|Mean maximum temperature of hottest month (ºC)||>25|
Impact SummaryTop of page
Economic ImpactTop of page
The moratorium which came into effect in January 2016 prohibits the trade within the United States of 201 species of salamanders and their import into the country. Relatively few businesses rely on this trade and the economic value is less than 2 million US dollars/year nationwide. Salamanders also have many medical applications ranging from skin secretions to applications gained from research on their regenerative abilities; these might also be affected by restrictions on trade.
Environmental ImpactTop of page
Impact on Biodiversity
Severe declines in the population of fire salamanders (Salamandra salamandra terrestris), smooth newts (Lissotriton vulgaris) and Alpine newts (Ichthyosaura alpestris) have already been observed in places where Bsal has been introduced in Europe; fire salamander populations in parts of the extreme south of the Netherlands (the only part of the country where the species is found -- Spitzen-van der Sluijs et al., 2013) have been reduced by as much as 99.99% (Spitzen-van der Sluijs et al., 2016). Presumably after initial introduction in a naïve population, enigmatic population declines occur (Spitzen-van der Sluijs et al., 2013, Goverse and Zeeuw, 2015). Co-housing experiments with infected Asian urodelans and European urodelans showed that Bsal is easily transferred (Martel et al., 2014). However, in some locations where Bsal is present, population declines appear absent even in a very susceptible species such as the fire salamander (Spitzen-van der Sluijs et al., 2016). Whether this is because introduction is recent and declines have not yet ensued, or for other reasons such as environmental factors, is not yet known. Not all declines have been directly tied to Bsal presence, however, as is the case in one location in the Netherlands where a community of four newt species has sharply declined since 2000 by between 87% and 96.6% (depending on the species), but a causal link with Bsal introduction cannot be proved because no samples were collected before 2015 (Spitzen van der Sluijs et al., 2016).
Given the virulence and apparently wide host range of Bsal, and the effects that B. dendrobatidis has had (it has been described, in an article cited by Vredenburg et al. (2010), as the greatest loss of vertebrate diversity attributable to disease in recorded history), it has the potential to devastate urodelan biodiversity in Europe, North Africa, western Asia and the Americas (Martel et al., 2014; Sabino-Pinto et al., 2015; Yap et al., 2015; Spitzen-van der Sluijs et al., 2016). In Europe up to 44 species could be lost, with the figure being significantly higher in the Americas which contain the world’s richest and most diverse salamander fauna (Yap et al., 2015).
Impact on Habitats
Extinctions or large reductions in salamander populations could have significant ecological effects. Salamanders throughout their global range are often abundant vertebrates in a wide variety of habitats and connect aquatic and terrestrial food webs and contribute to ecosystem stability. They regulate food webs directly as mid-level predators and indirectly by controlling grazers and detritivores; in some cases they effectively contribute to the carbon cycle (Davic & Welsh, 2004; Best & Welsh, 2014). In North American forests Plethodontid salamanders often outnumber any vertebrate species in biomass -- for example Ensatina enscholtzii predates on many invertebrates and effectively promotes leaf litter retention and fixation or slow release of carbon (Best & Welsh, 2014). Many species burrow and contribute to soil quality and dynamics as well as providing tertiary consumers with energy and nutrients (Davic & Welsh, 2004). Salamanders, as all amphibians, are also indicators for ecosystem health (Creemers & Delft, 2009). If Bsal were to be introduced in such communities and devastate them such ecosystem services might well be lost.
Threatened SpeciesTop of page
Risk and Impact FactorsTop of page Invasiveness
- Proved invasive outside its native range
- Has a broad native range
- Tolerant of shade
- Fast growing
- Reproduces asexually
- Host damage
- Reduced native biodiversity
- Threat to/ loss of endangered species
- Threat to/ loss of native species
- Negatively impacts animal/plant collections
- Negatively impacts trade/international relations
- Highly likely to be transported internationally accidentally
- Highly likely to be transported internationally illegally
- Difficult to identify/detect as a commodity contaminant
- Difficult to identify/detect in the field
- Difficult/costly to control
Gaps in Knowledge/Research NeedsTop of page
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).
ReferencesTop of page
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Richgels KL; Russell RE; Adams MJ; White CL; Grant EHC, 2016. Spatial variation in risk and consequence of Batrachochytrium salamandrivorans introduction in the USA. Royal Society Open Science, 3(2):150616. http://rsos.royalsocietypublishing.org/content/3/2/150616.abstract
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OrganizationsTop of page
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/
ContributorsTop of page
04/04/2016 Original text by:
Tariq Stark, consultant, Netherlands
Distribution MapsTop of page
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