Batrachochytrium salamandrivorans

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Batrachochytrium salamandrivorans
Batrachochytrium salamandrivorans, skin preparation of an infected fire salamander (Salamandra salamandra), scale 50 μm [1]

Batrachochytrium salamandrivorans , skin preparation of an infected fire salamander ( Salamandra salamandra ), scale 50 μm

Systematics
Department : Potty mushrooms (Chytridiomycota)
Class : Chytridiomycetes
Order : Rhizophydiales
Family : Incertae sedis
Genre : Batrachochytrium
Type : Batrachochytrium salamandrivorans
Scientific name
Batrachochytrium salamandrivorans
Martel , Blooi , Bossuyt & Pasmans , 2013

Batrachochytrium salamandrivorans , often Bsal in scientific publications, to distinguish it from the chytrid fungus ( Batrachochytrium dendrobatidis, Bd ), also salamander eater or salamander plague in popular scientific literature and the public media , is a pathogenic fungus of the class Chytridiomycetes . It is the closest relative of the chytrid fungus and next to it the second described fungus of the genus Batrachochytrium .

The area of ​​origin of Batrachochytrium salamandrivorans is Asia, the fungus is widespread in Japan, China and Southeast Asia and has been there for millions of years. The local amphibian fauna was able to adapt to the presence of the pathogen over a long period of time; infected amphibians show no symptoms of disease there. Batrachochytrium salamandrivorans was probably introduced into the Netherlands with the international amphibian trade . The pathogen is new to the European tail amphibians, so there are no defense mechanisms.

In contrast to the chytrid fungus, Batrachochytrium salamandrivorans predominantly affects tail amphibians, an infection leads to extensive skin lesions and rapid death of the animals. In the Netherlands and Belgium are populations of the spotted salamander collapsed since of 2010. Nationwide, the decline is more than 95 percent, and the fire salamander is now considered critically endangered in the Netherlands . There have also been mass deaths of fire salamanders in Germany, most recently in the Essen area at the beginning of 2018 . There is concern that the further spread of Batrachochytrium salamandrivorans will threaten the population and extinction of many species of salamandrivorans worldwide.

description

Morphology of both species of Batrachochytrium in vitro, scale 100 μm

Batrachochytrium Salamandrivorans forms in vitro usually single-center thalli , occasionally colonies. Germ tubes form on the thalli, at the tip of which there is a sporangium with a diameter of about 16 to 50 micrometers (average about 28 micrometers). The rhizoids are thin and thread-like and can arise from one or more areas of a sporangium.

As with the chytrid fungus, mobile zoospores are released from the sporangia , which are approximately spherical with a diameter of about 4 to 5.5 micrometers. Their surface is very irregular with numerous projections. In addition, Batrachochytrium salamandrivorans forms permanent spores that are resistant to environmental influences and survive unfavorable environmental conditions for a long time.

In vivo the colony-forming form of the thalli predominates. They are located in the keratinocytes of infected tail amphibians and are between about seven and 17 micrometers in diameter.

Batrachochytrium salamandrivorans differs from the chytrid fungus in particular in vitro through the formation of germ tubes and in vivo through the large number of colony-forming thalli.

The image on the right shows Batrachochytrium dendrobatidis in vitro, with numerous mature sporangia (black arrow) containing zoospores and empty sporangia (white arrow). Batrachochytrium salamandrivorans (below) is characterized in culture by predominantly monocentric thalli (black arrow), it has few colony-forming thalli (white arrow) and encapsulated zoospores with germ tubes (stars).

distribution

Type locality and type host

The Terra typica of Batrachochytrium salamandrivorans is Bunderbos in the Netherlands , a forest on the eastern Maasterrassen between Elsloo (municipality of Stein ) and Bunde , in the province of Limburg ( 50 ° 54 ′ 51 ″  N , 5 ° 44 ′ 59 ″  E ). The type host is the fire salamander ( Salamandra salamandra ).

Spread in the Netherlands and Belgium

Since 2008 dead fire salamanders lying around open have been found in the locations of fire salamanders in the Netherlands, and the number of animals observed has fallen sharply. In 2011 there was a collapse of the populations, the population decreased by 96 percent. The fire salamander is threatened with extinction in the Netherlands today.

In Belgium, the first outbreak occurred in 2013 at Eupen , followed by another in 2014 at Robertville . The affected populations decreased by 95 percent. In 2016, four fire salamanders found dead near the French border near Dinant tested positive for Batrachochytrium salamandrivorans . It could not be clarified how the pathogen overcome the great distance from the locations of the previous outbreaks.

Examination of approximately 2,000 samples taken between 2010 and 2016 from salamanders of various species found dead or captured, revealed a spread of the pathogen. To 14 of 55 sampled locations in Belgium, the Netherlands and Germany, here primarily in the Eifel , could Batrachochytrium Salamandrivorans be detected. The distribution area thus covers more than 10,000 square kilometers. Positive results came not only from fire salamanders, but also from pond newts and mountain newts . In the case of string pigs , northern crested newts and Alpine crested newts , no infected animals could initially be detected.

Spread in Germany

In 2004, two dead fire salamanders were found on a forest path near the Vichtbach near Roetgen and preserved in formalin . Only in 2017 were both specimens examined and infections with Batrachochytrium salamandrivorans detected. An assessment of this find against the background of the current spread of the fungus has not yet been made.

Since the type locality is less than ten kilometers from the German-Dutch border, the spread of Batrachochytrium salamandrivorans to Germany was expected at an early stage . In 2014, 186 samples from North Rhine-Westphalia , but also from Lower Saxony and Thuringia , tested negative for the fungus. In 2015 it was first detected in individuals from four locations in the northern Eifel . In 2017 there was already evidence of ten locations, at three other locations large populations of salamanders except for a few specimens had died out. The pathogen was detected not only in fire salamanders, but also in the other tailed amphibians occurring in the northern Eifel, mountain newt, thread newch, pond newt and northern crested newt. So far, no direct evidence of Batrachochytrium salamandrivorans has been found in the southern Eifel . However, numerous salamander populations known there since the 1990s could no longer be found.

In 2017, a second outbreak of Batrachochytrium salamandrivorans was detected near Essen . How the pathogen covered the distance from the location of the first outbreak - about 70 kilometers - is also unclear in this case. At the beginning of 2018 there was a mass extinction of fire salamanders.

Batrachochytrium salamandrivorans in amphibian housing

The first detection of Batrachochytrium salamandrivorans in Germany was made in a private amphibian husbandry. The keeper had specialized in salamander husbandry for the past 30 years and at that time owned around 200 individuals of fire salamander ( Salamandra salamandra ), North African fire salamander ( Salamandra algira ), Corsican fire salamander ( Salamandra corsica ) and Minor Asian fire salamander ( Salamandra infraimmaculata ) with their subspecies . After a few inexplicable deaths in autumn 2014, there was a mass extinction in spring 2015, to which around half of the animals of all four species fell victim. The affected individuals showed the typical symptoms of chytridiomycosis and tested positive for Batrachochytrium salamandrivorans .

In 2015, individuals of three species of tailed amphibians imported from an amphibian breeder in the United Kingdom were given to a zoological collection and either died or euthanized there in quarantine. The affected animals tested positive for Batrachochytrium salamandrivorans as did individuals of a fourth species from this breeder. The species were not published. A study carried out with the participation of numerous amphibian keepers in the United States, in which wipe samples were taken from privately held amphibians and tested, yielded no positive results. It is therefore assumed that Batrachochytrium salamandrivorans has at best a low distribution in private animal holdings in the USA.

Origin and distribution through the amphibian trade

The molecular genetic investigation of thousands of samples from nature and from zoological collections produced a number of findings that could be identified unequivocally as Batrachochytrium salamandrivorans . All positive findings came from Southeast Asia, namely Thailand , Vietnam and Japan ; the infected animals showed no symptoms of the disease. Batrachochytrium salamandrivorans has probably been widespread in Southeast Asia for around 30 million years, and the amphibian fauna of this region has since had the opportunity to adapt to the pathogen. The hypothesis that the pathogen is an old element of the Asian fungal flora is supported by its evidence in a more than 150-year-old museum specimen of the swordtail newt native to Japan .

The investigation of wild salamanders in Vietnam led to the finding that Batrachochytrium salamandrivorans is more widespread and more common in Vietnam than the chytrid fungus that is also widespread there. The Vietnamese tribes can tolerate higher temperatures than the mushrooms found in Europe.

In 2017, wild Hubei red-bellied toads ( Bombina microdeladigitora ), a species closely related to the Chinese giant toad and also very widespread in the terrarium trade, were examined for the presence of fungi of the genus Batrachochytrium . Infected toads were found, but their pathogen load was low. Infection was found in three of 36 Hubei red-bellied toads that had been imported shortly before as Vietnamese fire-bellied toads from a German pet shop. This was the first time that Batrachochytrium salamandrivorans was detected in live imports in the German pet trade. Both the evidence in Vietnam and the import of contaminated amphibians suggest that Batrachochytrium salamandrivorans came from Vietnam.

Field studies on 36 salamander species from 51 localities in southern China revealed that Batrachochytrium salamandrivorans is not only widespread geographically, but also in terms of the number of infected species and affected ecosystems. Since the Chinese export of amphibians exceeds that of Vietnam many times over, the results of the investigations once again brought the question of improved safety in the international amphibian trade to the fore.

Way of life

Life cycle of species of Batrachochytrium in vitro

The picture shows the life cycles of both species of Batrachochytrium in vitro . Batrachochytrium dendrobatidis only goes through developmental stages A – E, while Batrachochytrium salamandrivorans also has spore stages B1-B2: (A) flagellated mobile zoospore; (B) encapsulated zoospore; (B1) Zoospore in development; (B2) transferring the cell contents into a new thallus; (C) zoospore with rhizoid; (D) immature sporangium; (E) a mature monocentric sporangium releases zoospores through a single tube (right), a colony-forming thallus with multiple sporangia, each with its own tube (left).

Batrachochytrium salamandrivorans shows optimal growth between 10 and 15 ° C in the laboratory. Growth still takes place at temperatures of only 5 ° C, growth stops at temperatures of more than 24 ° C, and after five days at 25 ° C it dies. This means that the fungus has a much lower preferred temperature than its closest relative, the chytrid fungus.

The ability to create agile zoospores that can survive in nature for months, unlike the chytrid, has been a matter of great concern among conservationists. The latest research has shown that Batrachochytrium salamandrivorans has only a poor ability to spread without suitable vectors . The discovery of a healthy population of fire salamanders in the Netherlands, only 800 meters from the site of the first outbreak, raised hopes that quarantine measures could prevent the pathogen from spreading. In addition to infected animals, human activities are also considered as possible transmission routes, such as the spread of spores with insufficiently disinfected equipment or shoes.

In laboratory tests to determine which amphibian species are endangered by Batrachochytrium salamandrivorans , 41 out of 44 examined species in the Salamandridae and Plethodontidae families were infected and quickly died. Further investigations led to the finding that the fungus can colonize the skin of tail amphibians more easily than that of frog amphibians. According to current knowledge, hosts that develop symptoms of the disease are exclusively tail amphibians of temperate zones. Frogs can become infected and spread fungal spores, but they do not become ill themselves.

Systematics

Batrachochytrium salamandrivorans forms a clade with the closely related chytrid fungus ( Batrachochytrium dendrobatidis ) . The division into distinct species probably took place as early as the late Cretaceous or early Paleogene about 67 million years ago.

Initial description

It was first described by An Martel , Mark Blooi and Frank Pasmans from the University of Ghent and Franky Bossuyt from the Vrije Universiteit Brussel . Her publication, written together with seven other authors from various European universities and institutions, was published in September 2013 in the US journal Proceedings of the National Academy of Sciences .

Type material

The holotype of Batrachocytrius salamandrivorans is stored in liquid nitrogen as preparation AMFP13 / 1 by the University of Ghent .

etymology

The generic name Batrachochytrium is formed from the ancient Greek words βᾰ́τρᾰχος (German: frog ) and χυτρίδιον (German: small pot). In the first part he refers to the hosts affected by the first described chytrid fungus and in the second part to its external shape.

The species name refers to the well-known hosts, Caudates or Salamander (ancient Greek: σαλαμάνδρα ). The Latin suffix -vorans means eating, eating, consuming .

Batrachochytrium salamandrivorans as the causative agent of chytridiomycosis

discovery

Fire salamander with skin ulcers caused by Batrachochytrium salamandrivorans

Between 2010 and 2013, the fire salamander population in the Netherlands decreased by 96 percent. Dead fire salamanders were found in the affected areas. As part of a program to save the Dutch fire salamanders from extinction, 39 animals were captured in order to set up a conservation breed with them. Between November and December 2012, half of these animals died. Its investigation to known pathogens of amphibians , especially Batrachochytrium dendrobatidis , yielded no positive results. However, a previously unknown fungus was found in the skin lesions of the dead salamanders.

A phylogenetic investigation involving other chytridiomycetes revealed that the new pathogen is a close relative of the chytrid fungus and forms a clade with it. Compared to this, it shows clear genetic differences, while the chytrid fungi investigated so far show only a low genetic variability. Hence the description of a new species was justified.

Pathogenicity

Batrachochytrium salamandrivorans is highly contagious to several species of tailed amphibians. Sexually mature individuals who could contribute to a population recovery after the collapse of a population fall disproportionately often to the disease. This is justified by the fact that adult individuals interact with one another more frequently than juveniles , and that females always return to the same possibly contaminated location for reproduction. In addition, diseases only run more slowly with a low pathogen load or at unfavorably low temperatures, but they are always fatal.

The infection process is characterized by the fact that the infestation of a population leads to its almost complete extinction within a very short time. A recovery of the population after an epidemic, which can be observed in other infectious diseases, does not occur because an infection that has been overcome does not leave the survivors immune to new infections.

The permanent spores of Batrachochytrium salamandrivorans can survive for a long time in water and soil. Infection is highly contagious and species of amphibians that develop no or only weak symptoms of the disease can act as a reservoir for the pathogen and contribute to its spread.

Clinical picture

Clinical picture and pathology of an infection with Batrachochytrium salamandrivorans .
a) Fire salamander ( Salamandra salamandra ), in an outbreak in Robertville, Belgium, with multiple ulcers (white arrows) and pronounced skin lesions (black dots on yellow skin);
b) extensive ulcers (white arrows) on the ventral side of an infected fire salamander;
c) the skin cross-section through an ulcer shows numerous colony-forming thalli in all skin layers; immunohistochemical staining with polyclonal antibodies for Batrachochytrium dendrobatidis , scale 10 μm;
d) Enlargement of the intracellular thalli from picture c), scale 10 μm.

In the laboratory, an infection of fire salamanders with Batrachochytrium salamandrivorans leads to extensive skin lesions and deep ulcers spread over the entire body . The animals die within twelve to 18 days of infection or about seven days after the first symptoms, after a one to two day phase of anorexia , apathy and ataxia .

With the formation of ulcers, infections with Batrachochytrium salamandrivorans differ significantly from those with the chytrid fungus, which causes hyperplasia and hyperkeratosis in infected frogs .

The affected keratinocytes to be detected at the edges of the lesions are necrotic and contain a thallus in the middle , which is usually divided and contains several sporangia. The ulcers are superficially colonized with bacteria .

While infection in fire salamanders is invariably fatal, experimental infection in midwife toads failed to cause symptoms. However, the infected toads could still transmit pathogens to fire salamanders after weeks. In mountain newts, the course of the disease depended on the dose of pathogen involved in the infection. A high dose led to illness and death within a few weeks. No symptoms occurred after the administration of a small dose of pathogens, but the newts released pathogens into the environment for months. The newts do not develop immunity and are susceptible to repeated infections.

diagnosis

Taking a sample of skin cells for testing for Batrachochytrium salamandrivorans , Portland , Oregon , 2016

A reliable detection of an infection with Batrachochytrium salamandrivorans is only possible through a molecular genetic examination. For this purpose, a primer was developed at an early stage with which the DNA of the pathogen is replicated in a species-specific polymerase chain reaction . The use of the primer led to the identification of the pathogen in all salamanders found dead or infected in the laboratory, while healthy salamanders and midwife toads certainly did not give positive results. The analysis of samples taken in 2010 from 33 salamanders from the population of the type locality gave 13 positive test results, while 55 samples from a healthy population in Belgium did not produce any results.

A duplex qPCR test now exists that detects the DNA of both Batrachochytrium salamandrivorans and the chytrid fungus and is used extensively to control endangered amphibian populations for infections. Sampling can be done by swabbing the skin of a living animal. The duplex test provides reliable identification of the pathogen and can also be used for mixed infections. Since molecular genetic testing methods cannot be used with older formalin collection copies due to the damaged or destroyed DNA of the collection material, an ELISA is used in these cases . A limitation of all test methods is the post-infection latency period, which can be several weeks and which do not give positive results during samples from infected animals.

therapy

Treatment of infected tail amphibians can only be carried out in animal facilities. In Batrachochytrium salamandrivorans, terbinafine has a significantly lower minimum inhibitory concentration of 0.2 μg / ml than that of the chytrid fungus with 6 μg / ml. In frogs infected with the chytrid fungus, it has been shown that some species do not respond to therapy with terbinafine because their skin structure prevents the fungus from being exposed to a therapeutically effective concentration of the antifungal agent.

Infected salamanders from animal husbandry or from nature could be cured by keeping them at a temperature of more than 25 ° C for a period of at least ten days. A combination of the active ingredients voriconazole and polymyxin E has also proven to be effective when the temperature is raised at the same time.

Threat to biodiversity

The infectious disease chytridiomycosis is considered to be the most important cause of the global decline in amphibian populations and the extinction of frogs that has been observed for a few decades . More than 200 species are affected. This makes chytridiomycosis the world's greatest known threat to biodiversity from an infectious disease. So far it has been assumed that it is only caused by the chytrid fungus ( Batrachochytrium dendrobatidis ), which mainly affects frogs, but also tail amphibians and sneak amphibians . However, not all decline in the amphibian population could be attributed to this pathogen.

With the discovery of Batrachochytrium salamandrivorans , a second chytridiomycosis pathogen has been identified which, like the chytrid fungus, causes fatal skin infections in amphibians, is highly contagious and can extinguish entire populations within a very short time.

Ecologists have described the emergence and the feared rapid spread of Batrachochytrium salamandrivorans in the populations of western European tailed amphibians , which are already threatened and cannot offer immunity to infestation with the pathogen, as the perfect storm . There is concern that numerous populations across Europe will be wiped out.

No antidotes are known to prevent the spread of Batrachochytrium salamandrivorans , and infested tailed amphibian populations must be considered lost. Work is currently underway to set up a European warning system to monitor the spread of the pathogen. A program to save threatened populations ex situ is under development. In the Netherlands, more than 100 fire salamanders have already been taken from nature and put into a conservation breeding program. For Europe there is only hope that within the species of the genera Salamandra , Euproctus , Neurergus , Pleurodeles and Lissotriton italicus , which are particularly susceptible to infections, a balanced relationship between pathogens and hosts will be established over time.

The appearance of Batrachochytrium salamandrivorans in Western Europe has given rise to concern in other regions as well. Where Batrachochytrium salamandrivorans does not yet occur, preventing its introduction is the aim of species protection. The situation in the USA is perceived as particularly threatening. The east coast states of the USA have the world's greatest diversity of salamanders and numerous endemic species also live on the Pacific coast and in Mexico.

The aggressiveness of the pathogen, its ability to be spread over long distances in the form of permanent spores, and its occurrence in terrariums and in pet shops have led the American United States Fish and Wildlife Service to import 201 species of salamanders in January 2016 banned into the United States. Canada and Switzerland have also already issued import bans on amphibians from Asia. The European Union, into which approximately 620,000 salamanders were legally imported between 2005 and 2015, is also considering an import ban.

Confirmed and potential hosts of Batrachochytrium salamandrivorans


Fire salamander populations ( left ) have been significantly decimated in the Netherlands. For the rough-skinned yellow-bellied newt from North America ( center ), the pathogen was fatal in the laboratory. The Japanese fire-bellied newt ( right ) is resistant to a certain extent and could be one of the species with which the pathogen was introduced to Europe.

literature

  • Vojtech Balàž et al .: Scientific and technical assistance concerning the survival, establishment and spread of Batrachochytrium salamandrivorans (Bsal) in the EU . In: EFSA Journal 2017, Volume 15, No. 2, Document 4739, doi : 10.2903 / j.efsa.2017.4739 .
  • Lutz Dalbeck et al .: The salamander plague and its pathogen Batrachochytrium salamandrivorans (Bsal): current status in Germany . In: Zeitschrift für Feldherpetologie 2018, Volume 25, No. 1, pp. 1–22, ISSN  0946-7998 .
  • Trenton W. Garner et al .: Mitigating amphibian chytridiomycoses in nature . In: Philosophical Transactions of the Royal Society of London B 2016, Volume 371, No. 1709, pp. 371–379, doi : 10.1098 / rstb.2016.0207 .
  • Evan H. Campbell Grant et al .: Salamander chytrid fungus (Batrachochytrium salamandrivorans) in the United States - Developing research, monitoring, and management strategies . US Geological Survey Open-File Report 2015–1233. US Geological Survey, Reston, VA 2016, doi : 10.3133 / ofr20151233 .
  • To Martel et al .: Batrachochytrium salamandrivorans sp. nov. causes lethal chytridiomycosis in amphibians . In: Proceedings of the National Academy of Sciences 2013, Volume 110, No. 38, pp. 15325-15329, doi : 10.1073 / pnas.1307356110 (first description).
  • To Martel et al .: Recent introduction of a chytrid fungus endangers Western Palearctic salamanders . In: Science 2014, Volume 346, No. 6209, pp. 630-631, doi : 10.1126 / science.1258268 .
  • Pascale van Rooij et al .: Amphibian chytridiomycosis: a review with focus on fungus-host interactions . In: Veterinary Research 2015; Volume 46, Article 137, doi : 10.1186 / s13567-015-0266-0 .
  • Gwij Stegen et al .: Drivers of salamander extirpation mediated by Batrachochytrium salamandrivorans . In: Nature 2017; Volume 544, pp. 353-356 and Appendix Methods , doi : 10.1038 / nature22059 .
  • Tiffany A. Yap et al .: Batrachochytrium salamandrivorans and the Risk of a Second Amphibian Pandemic . In: EcoHealth 2017, Volume 14, No. 4, pp. 851-864, doi : 10.1007 / s10393-017-1278-1 .

Web links

Commons : Batrachochytrium salamandrivorans  - Collection of images, videos and audio files

Individual evidence

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  3. ↑ a b c d e To Martel et al .: Batrachochytrium salamandrivorans sp. nov. causes lethal chytridiomycosis in amphibians , p. 15327.
  4. ↑ Gwij Stegen et al .: Drivers of salamander extirpation mediated by Batrachochytrium salamandrivorans , pp. 354–355.
  5. ↑ a b Lutz Dalbeck et al .: The salamander plague : current status in Germany , p. 4.
  6. ↑ Anke Geeraerts: Nieuwe uitbraak van salamanderdodende ziekte in Dinant . natuurpunt.be , May 11, 2016, accessed April 8, 2018.
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  9. ↑ Lutz Dalbeck et al .: The salamander plague : current status in Germany , p. 1.
  10. ↑ Lutz Dalbeck et al .: The salamander plague : current status in Germany , p. 17.
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  15. ↑ Alexandra E. Laking et al .: Batrachochytrium salamandrivorans is the predominant chytrid fungus in Vietnamese salamanders . In: Scientific Reports 2017, Volume 7, Article 44443, doi : 10.1038 / srep44443 .
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  18. ↑ Zhiyong Yuan et al .: Widespread occurrence of an emerging fungal pathogen in heavily traded Chinese urodelan species . In: Conservation Letters , March 1, 2018, Article e12436, doi : 10.1111 / conl.12436 .
  19. ↑ Annemarieke Spitzen-van der Sluijs et al .: Post-epizootic salamander persistence in a disease-free refugium suggests poor dispersal ability of Batrachochytrium salamandrivorans . In: Scientific Reports 2018, Volume 8, Article 3800, doi : 10.1038 / s41598-018-22225-9 .
  20. ↑ To Martel et al .: Recent introduction of a chytrid fungus endangers Western Palearctic salamanders , p. 630.
  21. ↑ a b To Martel et al .: Batrachochytrium salamandrivorans sp. nov. causes lethal chytridiomycosis in amphibians , p. 15328.
  22. ↑ a b c d Gwij Stegen et al .: Drivers of salamander extirpation mediated by Batrachochytrium salamandrivorans , p. 353.
  23. ↑ a b c Gwij Stegen et al .: Drivers of salamander extirpation mediated by Batrachochytrium salamandrivorans , p. 356.
  24. ↑ a b To Martel et al .: Batrachochytrium salamandrivorans sp. nov. causes lethal chytridiomycosis in amphibians , p. 15326.
  25. ↑ To Martel et al .: Batrachochytrium salamandrivorans sp. nov. causes lethal chytridiomycosis in amphibians , pp. 15326-15327.
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