Invasive Species Compendium

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Datasheet report for Batrachochytrium salamandrivorans (Bsal)

Invasive Species Compendium Datasheet report for Batrachochytrium salamandrivorans (Bsal) Pictures Picture

Title Batrachochytrium salamandrivorans (Bsal); Bsal symptoms

Caption Copyright Batrachochytrium salamandrivorans (Bsal); severe Bsal symptoms, lethal chytridiomycosis, causing ©Tariq the death of this fire salamander (Salamandra salamandra). Belgium, May, 2015. Stark 2015

Identity Preferred Scientific Name Batrachochytrium salamandrivorans Martel et al., 2013

Preferred Common Name Bsal

International Common Names English: Bs; Eater of Salamanders

Local Common Names Germany: SalamanderChytrid Pilz

Summary of Invasiveness Batrachochytrium salamandrivorans (Bsal) is a singlecelled 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 nonresistant species. It is native to southeast 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 Tree Domain: Eukaryota Kingdom: Fungi Phylum: Chytridiomycota Class: Chytridiomycetes Order: Rhizophydiales Genus: Batrachochytrium Species: Batrachochytrium salamandrivorans

Notes on Taxonomy and Nomenclature 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).

Disease/s Table Batrachochytrium salamandrivorans infection

Distribution Native Distribution The native distribution of Batrachochytrium salamandrivorans (hereafter Bsal) is thought to lie in southeast 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 southeast 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.

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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 northwestern Europe was examined by testing 1921 urodelans in 20102016. This study demonstrated a substantial range extension in wild urodelans in the Netherlands, Belgium and Germany (Spitzenvan 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 (20092011) and Illinois (20082011), which all tested negative, as did samples of 65 anuran and one urodelan species from Panama collected in 20072008. Captivity Bsal has been detected in a salamander collection in Germany after causing a mass mortality of captive Salamandra species (SabinoPinto 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 Table 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. Country

Distribution

Last Reported

Origin

First Reported

Invasive

References

Notes

ASIA Japan

Present

Native

Not invasive Not invasive Not invasive

Martel et al., 2014

Endemic in at least five host species

Thailand

Present

Native

Martel et al., 2014

Endemic in at least one host species

Vietnam

Present

Native

Martel et al., 2014

Endemic in at least three host species

Present Present

Introduced Introduced

Invasive Invasive

Introduced Introduced

Invasive

Martel et al., 2014 Spitzenvan der Sluijs et al., 2016 Martel et al., 2013 Cunningham et al., 2015

EUROPE Belgium Germany

Netherlands Present UK Absent, intercepted only

History of Introduction and Spread 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 northwestern 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. Humanmediated 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 (Spitzenvan 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% (Spitzenvan 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 (Spitzenvan der Sluijs et al., 2016) the distribution of Bsal in northwestern Europe has been examined by testing 1921 urodelans in 20102016. 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.

Introductions Introduced to Belgium

Introduced from

South East Asia Germany South East Asia Netherlands South East Asia

Year

Reason

Pet trade (pathway cause) Pet trade (pathway cause) 2010 Pet trade (pathway cause)


Introduced by

Established in wild through Natural Continuous reproduction restocking Yes Yes Yes

References

Martel et al., 2014 Martel et al., 2014 Martel et al., 2014

Notes

Probably via trade in Asian salamanders Probably via trade in Asian salamanders Probably via trade in Asian salamanders

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Risk of Introduction 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 nonAsian salamanders like fire salamanders can be infected, as shown in SabinoPinto 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 InterMinistry Invasive Species Working Group, undated). Humanmediated 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 highrisk zones are the southeastern 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 bluetailed firebellied newt (Cynops cyanurus [Hypselotriton cyanurus]), the Japanese firebellied 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 MidAtlantic 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 Characteristics 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 tryptonegelatine hydrolysatelactose (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 15.750.3 μm with an average of 27.9 μm. Motile zoospores are fairly spherical and have a diameter of 4.05.5 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 6.917.2 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 southeast 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).

Host Animals Animal name Caudata Cynops ensicauda Cynops pyrrhogaster (Japanese firebellied salamander) Hynobius nebulosus Hypselotriton cyanurus Ichthyosaura alpestris Lissotriton vulgaris Onychodactylus japonicus Paramesotriton deloustali Salamandra algira Salamandra corsica Salamandra infraimmaculata Salamandra salamandra Salamandrella keyserlingii Speleomantes Tylototriton uyenoi Tylototriton vietnamensis Tylototriton ziegleri

Context Life stage System In captivity, Wild host Subclinical, Wild host Subclinical, Wild host Subclinical, Wild host In captivity, Subclinical Wild host Wild host Subclinical, Wild host Subclinical, Wild host In captivity In captivity In captivity Wild host Subclinical, Wild host In captivity Subclinical, Wild host In captivity, Subclinical Subclinical, Wild host

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Climate C Temperate/Mesothermal climate Cf Warm temperate climate, wet all year Cs Warm temperate climate with dry summer Cw Warm temperate climate with dry winter Df Continental climate, wet all year Ds Continental climate with dry summer Dw Continental climate with dry winter

Status Description Tolerated Average temp. of coldest month > 0°C and 10°C Tolerated Warm average temp. > 10°C, Cold average temp. > 0°C, wet all year Tolerated Warm average temp. > 10°C, Cold average temp. > 0°C, dry summers

Remark

Tolerated Warm temperate climate with dry winter (Warm average temp. > 10°C, Cold average temp. > 0°C, dry winters) Preferred Continental climate, wet all year (Warm average temp. > 10°C, coldest month 10°C, coldest month 10°C, coldest month 25

Pathway Causes Cause Breeding/ propagation

Captive breeding of salamanders with possible infection

Long Distance Yes

Hitchhiker Interconnected waterways Pet/aquarium trade

Possible humanmediated (direct) dispersal by pathogen adherence to boots or shoes Possible dispersal of pathogen by interconnected waterways

Yes

Yes Yes

Yes

Yes

Martel et al., 2014

Yes

Yes Yes

Martel et al., 2014 Martel et al., 2014

Research Smuggling

Notes

Trade of salamanders within countries and import of (Asian) salamanders to Europe and the Americas Disease could be spread by field researchers who do not adhere to field hygiene protocols Possible illegal trading of salamanders

Local Yes

References SabinoPinto et al., 2015 Martel et al., 2014

Pathway Vectors Vector Debris and waste associated with human activities Pets and aquarium species Plants or parts of plants Vector/host species

Notes Disposal of possibly infected materials associated with captive salamanders Trade of salamanders within countries and import of (Asian) salamanders to Europe and the Americas Disposal of possibly infected materials associated with captive salamanders Infected animals escaping or introduced into natïve host communities

Long Local References Distance Yes BC InterMinistry Invasive Species Working Group undated; Cunningham et al., 2015 Yes Yes Martel et al., 2014 Yes

Cunningham et al., 2015

Yes

BC InterMinistry Invasive Species Working Group undated; Cunningham et al., 2015

Impact Summary Category Impact Native fauna Negative

Economic Impact 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 Impact 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 Spitzenvan der Sluijs et al., 2013) have been reduced by as much as 99.99% (Spitzenvan der Sluijs et al., 2016). Presumably after initial introduction in a naïve population, enigmatic population declines occur (Spitzenvan 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 (Spitzenvan 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).


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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; SabinoPinto et al., 2015; Yap et al., 2015; Spitzenvan 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 midlevel 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 Species Threatened Species Conservation Status Where Threatened Mechanism References Notes Salamandra salamandra National list(s) Netherlands Pathogenic Spitzenvan der Sluijs et al., 2013

Risk and Impact Factors Impact mechanisms Pathogenic

Impact outcomes Host damage Negatively impacts animal/plant collections Negatively impacts trade/international relations Reduced native biodiversity Threat to/ loss of endangered species Threat to/ loss of native species

Invasiveness Fast growing Has a broad native range Proved invasive outside its native range Reproduces asexually Tolerant of shade

Likelihood of entry/control Difficult to identify/detect as a commodity contaminant Difficult to identify/detect in the field Difficult/costly to control Highly likely to be transported internationally accidentally Highly likely to be transported internationally illegally

Gaps in Knowledge/Research Needs Much needs to be learned about the host range and hostpathogen interaction in Bsal’s native range. In northwestern 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).

References Association Française des Etablissements Publics Territoriaux de Bassin, 2016. Un dispositif de surveillance accrue du Batrachochytrium salamandrivorans dans les Hauts de France ([English title not available]). Paris, France: Association Française des Etablissements Publics Territoriaux de Bassin. http://polezhi.org/undispositifde surveillanceaccruedubatrachochitriumsalamandrivoransdansleshautsdefrance Bales EK, Hyman OJ, Loudon AH, Harris RN, Lipps G, Chapman E, Roblee K, Kleopfer JD, Terrell KA, 2015. Pathogenic chytrid fungus Batrachochytrium dendrobatidis, but not B. salamandrivorans, detected on eastern Hellbenders. PLoS ONE, 10(2):e0116405. http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0116405 BC InterMinistry Invasive Species Working Group, undated. Salamander chytrid disease (Batrachochytrium salamandrivorans). Victoria, British Columbia, Canada: BC InterMinistry Invasive Species Working Group, 2 pp. https://www.for.gov.bc.ca/hra/invasivespecies/publications/SpeciesAlerts/Salamander_chytrid_disease.pdf Berger L, Speare R, Daszak P, Green DE, Cunningham AA, Goggin CL, Slocombe R, Ragan MA, Hyatt AD, McDonald KR, Hines HB, Lips KR, Marantelli G, Parkes H, 1998. Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. Proceedings of the National Academy of Sciences of the United States of America, 95(15):90319036. Best ML, Welsh HH Jr, 2014. The trophic role of a forest salamander: impacts on invertebrates, leaf litter retention, and the humification process. Ecosphere, 5(2):art16. http://www.esajournals.org/doi/full/10.1890/ES1300302.1


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Blooi M, Martel A, Haesebrouck F, Vercammen F, Bonte D, Pasmans F, 2015. Treatment of urodelans based on temperature dependent infection dynamics of Batrachochytrium salamandrivorans. Scientific Reports, 5(8037):srep08037. http://www.nature.com/articles/srep08037 Blooi M, Pasmans F, Longcore JE, Spitzenvan der Sluijs A, Vercammen F, Martel A, 2013. Duplex realtime PCR for rapid simultaneous detection of Batrachochytrium dendrobatidis and Batrachochytrium salamandrivorans in amphibian samples. Journal of Clinical Microbiology, 51(12):41734177. http://jcm.asm.org/content/51/12/4173.abstract Blooi M, Pasmans F, Rouffaer L, Haesebrouck F, Vercammen F, Martel A, 2015. Successful treatment of Batrachochytrium salamandrivorans infections in salamanders requires synergy between voriconazole, polymyxin E and temperature. Scientific Reports, 5(11788):srep11788. http://www.nature.com/articles/srep11788 Bosch J, MartínezSolano I, 2006. Chytrid fungus infection related to unusual mortalities of Salamandra salamandra and Bufo bufo in the Peñalara Natural Park, Spain. Oryx, 40(1):8489. http://journals.cambridge.org Creemers RCM, Delft JCW van, 2009. De amfibieën en reptielen van Nederland (The amphibians and reptiles of the Netherlands). [Nederlandse Fauna 9.] Cunningham AA, Beckmann K, Perkins M, Fitzpatrick L, Cromie R, Redbond J, O'Brien MF, Pria Ghosh, Shelton J, Fisher MC, 2015. Emerging disease in UK amphibians. Veterinary Record 176(18):468. http://veterinaryrecord.bvapublications.com/archive/ Davic RD, Welsh HH Jr, 2004. On the ecological roles of salamanders. Annual Review of Ecology, Evolution, and Systematics, 35:405434. Gimeno A, Meikl M, Pitt A, Winkler M, Berninger UG, Borsdorf A, Köck G, Scott B, Braun V, 2015. Testing of Fire Salamanders around Salzburg for Batrachochytrium salamandrivorans within a school project. eco.mont (Journal on Protected Mountain Areas Research), 7(1):7276. http://hw.oeaw.ac.at/0xc1aa500e_0x0031dc95.pdf Goverse E, Zeeuw M de, 2015. [English title not available]. (Trends in aantallen NEM Meetnet Amfibieën 2014.) Schubben & Slijm, 26:1214. http://www.ravon.nl/Portals/0/PDF3/schubbenslijm26.pdf Grant EHC, Muths E, Katz RA, Canessa S, Adam MJ, Ballard JR, Berger L, Briggs CJ, Coleman J, Gray MJ, Harris MC, Harris RN, Hossack BR, Huyvaert KP, Kolby JE, Lips KR, Lovich RE, McCallum HI, Mendelson JR III, Nanjappa P, Olson DH, Powers JG, Richgels KLD, Russell RE, Schmidt BR, Spitzenvan der Sluijs A, Watry MK, Woodhams DC, White CL, 2016. Salamander chytrid fungus (Batrachochytrium salamandrivorans) in the United States Developing research, monitoring, and management strategies. Reston, Virginia, USA: U.S. Geological Survey, v + 16 pp. [OpenFile Report 20151233.] https://pubs.er.usgs.gov/publication/ofr20151233 Gray MJ, Lewis JP, Nanjappa P, Klocke B, Pasmans F, Martel A, Stephen C, Olea GP, Smith SA, SacerdoteVelat A, Christman MR, 2015. Batrachochytrium salamandrivorans: The North American Response and a Call for Action. PLoS Pathogens, 11(12):e1005251. http://journals.plos.org/plospathogens/article? id=10.1371/journal.ppat.1005251 Kolby JE, 2015. Saving Salamanders with Citizen Science. FrogLog, 23 (4) (116):19. http://www.amphibians.org/froglog/fl116/ Longcore JE, Pessier AP, Nichols DK, 1999. Batrachochytrium dendrobatidis gen. et sp. nov., a chytrid pathogenic to amphibians. Mycologia, 91(2):219227. Martel A, Blooi M, Adriaensen C, Rooij P van, Beukema W, Fisher MC, Farrer RA, Schmidt BR, Tobler U, Goka K, Lips KR, Muletz C, Zamudio KR, Bosch J, Lötters S, Wombwell E, Garner TWJ, Cunningham AA, Spitzenvan der Sluijs A, Salvidio S, Ducatelle R, Nishikawa K, Nguyen TT, Kolby JE, Bocxlaer I van, Bossuyt F (et al.), 2014. Recent introduction of a chytrid fungus endangers Western Palearctic salamanders. Science (Washington), 346(6209):630631. http://www.sciencemag.org Martel A, Spitzenvan der Sluijs A, Blooi M, Bert W, Ducatelle R, Fisher MC, Woeltjes A, Bosman W, Chiers K, Bossuyt F, Pasmans F, 2013. Batrachochytrium salamandrivorans sp. nov. causes lethal chytridiomycosis in amphibians. Proceedings of the National Academy of Sciences of the United States of America, 110(38):1532515329. http://www.pnas.org/content/110/38/15325.full Price SJ, Garner TWJ, Cunningham AA, Langton TES, Nichols RA, 2016. Reconstructing the emergence of a lethal infectious disease of wildlife supports a key role for spread through translocations by humans. Proceedings of the Royal Society B: Biological Sciences, 283(1839):article 20160952. http://dx.doi.org/10.1098/rspb.2016.0952 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 Rooij P van, Martel A, Haesebrouck F, Pasmans F, 2015. Amphibian chytridiomycosis: a review with focus on fungushost interactions. Veterinary Research, 46(137):(25 November 2015). http://www.veterinaryresearch.org/content/46/1/137 SabinoPinto J, Bletz M, Hendrix R, Perl RB, Martel A, Pasmans F, Lötters S, Mutschmann F, Schmeller DS, Schmidt BR, Veith M, Wagner N, Vences M, Steinfartz S, 2015. 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Emerging Infectious Diseases, 22(7):in press. http://dx.doi.org/10.3201/eid2207.160109 Spitzenvan der Sluijs A, Spikmans F, Bosman W, Zeeuw M de, Meij T van der, Goverse E, Kik M, Pasmans F, Martel A, 2013. Rapid enigmatic decline drives the fire salamander (Salamandra salamandra) to the edge of extinction in the Netherlands. Amphibia Reptilia, 34(2):233239. http://booksandjournals.brillonline.com/content/journals/10.1163/1568538100002891 Standing Committee to the Convention on the Conservation of European Wildlife and Natural Habitats, 2015. Convention on the conservation of European wildlife and natural habitats 35th meeting of the Standing Committee Strasbourg, 1 December 4 December 2015 Recommendation no. 176 (2015) on the prevention and control of the Batrachochytrium salamandrivorans chytrid fungus. Strasbourg, France: Council of Europe, 3 pp. [TPVS(2015)09E.] https://wcd.coe.int/ViewDoc.jsp? p=&id=2332303 Vredenburg VT, Knapp RA, Tunstall TS, Briggs CJ, 2010. 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https://www.researchgate.net/publication/304673856_Amphibian_A_Case_Definition_and_Diagnostic_Criteria_for_Batrachochytrium_salamandrivorans_Chytridiomycosis Yap TA, Koo MS, Ambrose RF, Wake DB, Vredenburg VT, 2015. Averting a North American biodiversity crisis. Science, 349(6347):481482. http://dx.doi.org/doi:10.1126/science.aab1052 Zhu W, Xu F, Bai C, Liu X, Wang S, Gao X, Yan S, Li X, Liu Z, Li Y, 2014. A survey for Batrachochytrium salamandrivorans in Chinese amphibians. Current Zoology, 60(6):729735. http://www.actazool.org/temp/%7B1D1500F86BAC47E7ADB6B4EDC79E407B%7D.pdf

Links to Websites Website AmphibiaWeb Bsal Task Force Saving Salamanders with Citizen Science SOS salamander

URL http://amphibiaweb.org/ http://www.salamanderfungus.org/ https://www.inaturalist.org/projects/saving salamanderswithcitizenscience http://sossalamander.nl/home

RAVON (BSAL)

http://www.ravon.nl/bsal

Comment

Latest news compiled by RAVON, Netherlands, on the salamander fungus Batrachochytrium salamandrivorans (Bsal), infected species, publications, protocols, tips etc.

Organisations 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.tubs.de/ Germany: Trier University Faculty of Regional and Environmental Sciences, Department of Biogeography, 54286 Trier, https://www.unitrier.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/

Contributors 04/04/2016 Original text by: Tariq Stark, consultant, Netherlands

World Map

Present, no further details Widespread Localised Confined and subject to quarantine Occasional or few reports

Evidence of pathogen Last reported Presence unconfirmed See regional map for distribution within the country

Africa


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Asia

Europe

Pacific


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North America

Central America

South America


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Date of report: 15 November, 2016


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