Batrachochytrium salamandrivorans infection

Pictures

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

Identity

Preferred Scientific Name

• Batrachochytrium salamandrivorans infection

International Common Names

• English: Bs; Bsal

Pathogen/s

Overview

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.

Host Animals

Hosts/Species Affected

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).

Distribution

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.

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.

Pathology

Infected animals exhibit characteristic erosive skin lesions, associated with numerous colonial thalli spread across the epidermis. Necrosis of keratinocytes adjacent to these thalli is characteristic for Bsal infection (Martel et al., 2013). Why Bsal 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).

Diagnosis

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.

List of Symptoms/Signs

Disease Course

How Bsal interacts with its urodelan host is not yet known in detail. When healthy, susceptible hosts are inoculated with zoospores, intracellular invasion of the skin occurs within 24 hours. After initial exposure, an individual usually dies within 2-3 weeks (Martel et al., 2014). In vitro, Bsal develops germ tubes, and it is suspected that invasion of the deeper layers of the epidermis is also germ-tube-mediated (Rooij et al., 2015). In urodelans chytridiomycosis caused by Bsal is characterized by multifocal superficial erosions and extensive ulcerations in the epidermis which are found all over the body (Rooij et al., 2015). How death is induced by Bsal and how the skin function is impaired is not yet known (Rooij et al., 2015). Larvae of the fire salamander (Salamandra salamandra) are not affected (Rooij et al., 2015).

Epidemiology

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. Most infected animals succumb 2-3 weeks after initial exposure (Martel et al., 2014).

The native range of Bsal lies in south-east Asia where it exists at low levels in several urodelan taxa from the families Hynobiidae and Salamandridae (Martel et al., 2014). Much needs to be learned about the host range and host-pathogen interaction in the native range. 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. Currently the range of Bsal in the Netherlands, Germany and Belgium may be as large as approximately 10,000 km². In north-western Europe, at least three species are affected (Martel et al., 2014; Spitzen-van der Sluijs et al., 2016), most notably the fire salamander (Salamandra salamandra terrestris) in the extreme south of the Netherlands (the only part of the country where the species is found -- Spitzen-van der Sluijs et al., 2013), where populations have been reduced by as much as 99.99% (Spitzen-van der Sluijs et al., 2016). Presumably after initial introduction in a naïve population, population declines follow (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 it is present, population declines appear absent even in a very susceptible species as the fire salamander (Spitzen van der Sluijs et al., 2016). It is not yet known whether this is because declines have not yet occurred after recent introduction or because of other reasons such as environmental factors.

Impact: Economic

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.

Impact: Environmental

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.

Disease Treatment

In captivity Bsal can be treated by means of a temperature treatment and/or the use of fungicides. Treatment based on the synergy of both methods is most effective (Blooi et al., 2015b). In vitro, Bsal growth is inhibited by voriconazole, polymyxin E, itraconazole and terbinafine, but not florfenicol. Synergistic effects between polymyxin E and voriconazole or itraconazole significantly decrease the dosage required to inhibit Bsal growth. Topical treatment for ten days of live infected fire salamanders (Salamandra salamandra) with either voriconazole or itraconazole (12.5 μg/ml and 0.6 μg/ml respectively) or in combination with polymyxin E (2000 IU/ml) decreased fungal loads but did not clear Bsal infections (Blooi et al., 2015b). Blooi et al. (2015a) showed that Bsal colonized fire salamanders at ambient temperatures of 15 and 20 °C but not at 25 °C. Keeping infected animals at 25 °C for 10 days cleared the infection completely. Combining both treatment regimens proved very effective and was validated in 12 fire salamanders which had been infected in a field outbreak (Blooi et al., 2015b).

Prevention and Control

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.

References

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Links to Websites

Organizations

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/

Contributors

04/04/2016 Original text by:

Tariq Stark, consultant, Netherlands

Distribution Maps