Introduction

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In 2013 it became obvious what had caused the collapse of the fire salamander in The Netherlands: the newly discovered and identified chytrid fungus Batrachochytrium salamandrivorans ( Bsal ) was the culprit (Martel et al 2013). Since this fungus has a relatively low optimal temperature for growth (10 – 15 degrees) and thrives in moist environments, it was expected that soon more salamander and newt populations would fall victim to the fungus. Only salamanders and newts are susceptible to the fungus and once infection occurs the animals experience rapid mortality as a result of the erosive disease eating away at the skin (Martel et al. 2014).


NEWS

  • October 2016, France: The French Herpetological Society (FHS) initiated in response of the imminent Bsal poses to French salamanders and newts a citizen science based program in order to detect sick and dead salamanders (due to Bsal) as soon as possible. This program started as a response to the detection of Bsal in Belgium near the French border. Permits to collect (dead-) salamanders can be obtained via regional FHS coordinator José Godin. Please visit this link to read more on the program.   
  • April 2016, Belgium: a novel outbreak of Bsal was discovered in Belgium, about 70 km from previous known outbreak sites. This outbreak is very close to the French border. 
  • March 2016: a novel publication was released on the current distribution of B. salamandrivorans in Europe.
  • February 2016:letter was sent to the European commission by 17 scientists and 27 nature organisations.  Scientists and organisations asked for “the immediate implementation of the recommendation by the Standing Committee of the Bern Convention, and for the listing of Bsal as a pathogen of Union concern under the animal health legislation
  • January 2016: Deadly amphibian fungus in Europe could emerge in United States: U.S. Geological Survey (USGS) identifies research needs & management actions in a new report released on January 21st 2016
  • 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 are seen as ‘injurious’ to native salamanders. It is hoped that this ban will help prevent the introduction of Bsal to the US. More information, a FAQ and permit applications can be found here.
  • December 2015: the Standing Committee of the Bern Convention published their: Recommendation No. 176 (2015) on the prevention and control of the Batrachochytrium salamandrivorans chytrid fungus [document T-PVS (2015) 9]

B. salamandrivorans

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In Martel et al.’s (2014) major study, the impact of the fungus on dozens of amphibian species from four continents, were examined. The results indicated that salamanders and newts are extremely susceptible to the deadly fungus, while other amphibians such as frogs and toads remain unaffected.

Batrachochytrium salamandrivorans ( salamander-devouring ) kills: 

  • salamanders and newts die rapidly ( approximately 12-18 days )
  • after a short period of ataxia, anorexia and apathy.

Bsal is the second fatal chytrid fungus which parasitizes amphibians. Phylogenetic research has shown that Bsal forms a previously unknown branch which forms a group with Bd. The genetic divergence  between the two chytrid fungi is so large that Bsal can be seen as a separate species within the order Rhizophydiales.

Bsal occupies a different niche than Bd. The optimum temperature for growth of Bsal is lower (10-15 ˚C ) than that of Bd (17-25 ˚C), which means that Bsal is likely to pose a greater threat to our native salamanders and newts than Bd.

The fungus Bsal is currently on the rise in the Netherlands, Germany and Belgium and will most likely reach other countries in the very near future. Several native salamander species such as the great crested newt and the Alpine Newt are, like the fire Salamander, extremely susceptible to the fungus and once infected death ensues rapidly.

The disease is highly contagious and can be easily transferred between different species of salamanders and newts. A common mode of transmission is direct contact of the animals (skin-to-skin), the dispersal of and contact with zoospores is another possible avenue.

Origin: how it all started

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Bsal originated in Asia and is believed to have arrived in Europe via the pet trade, in particularly through the import of Asian salamanders. The importation of Asian salamanders occurs around the world and in large numbers. It was estimated that between 2001-2009 more than 2.3 million Chinese fire-bellied newts were imported into America. Asian salamander species appear to carry the fungus with little or no ill-effect. Research has shown Asian salamanders and the fungus have coexisted for many years and infection records from Asia date back to at least 1861 ( Martel et al., 2014).

Bsal: a brief introduction

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  1. Bsal infections are restricted to salamanders and newts ( Urodela ), but for this group the fungus is highly pathogenic and extremely lethal
  2. Bsal causes superficial skin erosion, deep ulcerations and skin necrosis
  3. Bsal originates from Asia
  4. Asian salamander species have lived in coexistence with Bsal for millions of years ( Bsal separated from Bd 67 million years ago)
  5. Recently Bsal arrived in Europe
  6. An ancient balance between pathogen and host has now been disturbed as a result of the transportation and importation of animals , consequently resulting in the mass mortality of several species
  7. Bsal is a chytrid fungus that literally eats away at the skin of salamanders and newts
  8. After exposure the animals die rapidly
  9. The optimum growth temperature of Bsal is between 10-15 ˚C
  10. Bsal has caused mass mortality and severe population declines in wild Fire Salamander, smooth newt and Alpine Newt populations in the Netherlands, Germany and Belgium
  11. Bsal has also been detected in captive salamanders held in Germany and England

Where has the fungus been detected?

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  • In the Netherlands the fungus was first detected at Bunderbos and at Putberg (Fire Salamanders and Alpine Newts). The first victims of Bsal were found in 2008, the cause of death however, wasn't announced until 2013. In 2014 and 2015 the fungus was also found in  Alpine newt populations and in an isolated population of smooth newts.  
  • In Belgium Bsal has been detected in Eupen (fire salamanders, December 2013 ), Robertville (fire salamanders, April 2014), Liege (fire salamanders, 2014) and in Duffel (Alpine newts). In April 2016 a novel outbreak was detected in a population fire salamanders in Dinant, close to the French border. 

The fungus was also detected in captive salamanders in the UK (Cunningham et al 2015) and in Germany (Sabino Pinto et al 2015)

How are the Dutch fire salamanders doing?

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Commissioned by the Ministry of Economic Affairs, the Province of Limburg and Staatsbosbeheer, RAVON has been monitoring the Fire Salamander population and examined whether the fungus was present in the vicinity. The Ministry of Economic Affairs has guaranteed there are opportunities for long-term research.

The Dutch Fire Salamander population is not doing well. The latest CBS trend calculations show a decline of 99.9% over the period 1997 - 2014. In 2013 (period 1997-2012 ), the decline was at 96 %, meaning the decline has not stagnated.

Nevertheless, we remain hopeful as several healthy looking adults and larvae were found earlier this year. Even in Vijlenerbos, an area where the last adult was recorded in 2013, larvae have been found.

Shouldn’t the trade of salamanders and newts be banned?

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Based on what we know so far, we do not consider banning the trade of salamanders to be a viable solution. However, both the scientific community and hobbyist groups are pleading for a ban in the trade of wild caught Asiatic salamanders that can easily be bred in captivity. Furthermore, it has been suggested that ‘health certificates’ should be issued for all individuals guaranteeing the animals have not been infected with or do not carry the Bsal fungus. It has also been recommended for salamander keepers/hobbyists to implement hygiene protocols for their own collection which may include: a quarantine period for newly acquired animals and the proper handling of water and terrarium materials. The keeping of salamanders and newts ( as a hobby or professionally) yields information on the ecology and biology of the species, which in turn benefits the protection of these species in the wild.

To find out more , please contact the Salamander Association.

ABROAD

I keep salamanders at home, how do i know if they have been infected?

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If you keep salamanders or newts in your collection , you do not want them to become infected with Bsal, or for your salamanders to spread the fungus by infecting others. Therefore,you will need to be extremely careful when adding new animals to your collection, or when you sell or give away animals to others. When acquiring a new animal, quarantine the animal for a considerable time and be careful with your waste water.

Never purchase salamanders or newts for your garden pond.

It is possible to have your animals tested for Bsal (and Bd and Ranaviruses ). To have animals tested, please contact the University of Ghent directly. If you are living in the Netherlands, RAVON can provide free Bsal testing. Please contact Annemarieke Spitzen for more information (a.spitzenATravon.nl)

Can infected animals be treated?

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Captive animals can be treated if they have been infected with Bsal. In 2015, two articles were published on this subject ( Blooi et al , 2015a ; . 2015b ).

In summary:

  • It is safe, effective and cheap to treat the infected animals by exposing them to higher temperatures
  • The animals should be kept at 25 °C for a period of 10 days
  • Not all species can survive being exposed to 25˚C temperatures for long periods of time
  • For those species, the procedure can be performed at 20˚C . Additionally, the animals will need to be treated with a combination of anti-fungal agents twice daily

What can we expect in the near future?

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We predict that more outbreaks will follow, this time also involving species other than the fire salamander. Despite encouraging information that healthy looking animals have been observed at all known outbreak sites, we fear for the long term survival of the fire salamander in these regions and eventually elsewhere in Europe; Bsal will put many amphibian species on the path toward extinction.

Fortunately, a great deal of research is currently being carried out at a number of different laboratories. Fire salamander populations where the fungus was previously detected are now being intensively monitored. Hopefully sufficient knowledge can be generated in time so effective mitigation measures can be implemented and the spread of the fungus can be limited.

Mortality as a result of Bsal infections may not be obvious at first. A few dead salamanders could easily go unnoticed and may not seem alarming. Mortality, however, may have occured as a result of a Bsal infection. So whether you find one or several dead salamanders, we recommend you contact us

Our American colleagues  launched a website on Bsal, which is interesting to have a look at so you can follow all overseas developments. There are other sites too such as the webpage from AmphibiaWeb.


Fieldwork: hygiene protocol

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It is extremely important that we ourselves when out in the field are aware that we can easily spread viruses and fungi over long distances, which is likely to contribute to the spread of Bsal. It is of the utmost importance that all materials are properly cleaned ( nets , boots , etc.) and that others in the field are also aware. On the RAVON website you can find a so-called “Hygiene protocol”.

For land managers, it is also necessary to implement a hygiene protocol. Large equipment used for cleaning ponds, logging operations or mowing can become contaminated and transfer pathogens to other areas. All equipment and materials should be disinfected before being transported to and used in other areas.

What should I do if I find a dead salamander?

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At the beginning of an outbreak, animal mortality may initially go unnoticed. We therefore call on everyone to report all findings of dead salamanders (with the exception of roadkill). RAVON is authorized to have these animals in its possession for research purposes, meaning we may ask you to collect and preserve the animal. Of course, a dead salamander does not necessarily mean Bsal is the direct cause, the animal may have died a natural death or may have become infected with Ranavirus or Amphibiocystidium.

When you notice dead or ill animals:

  • Take pictures and make notes (number of animals , species , location , date, time , etc.)
  • Contact RAVON (also to aquire an exemption for transporting dead animals)
  • Collect the dead animals ( in boxes / bags)
  • Freeze the dead animals separately from each other and include the details of each animal in the box/bag
  • Make an appointment with RAVON to organise for the animals to be collected
  • Monitor the location
  • Disinfect all materials ( including shoes and gloves) after each visit

Belgium

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The amphibian fungus has now also been detected in Belgium ( map).

Flanders
Het Agentschap voor Natuur en Bos (The Agency for Nature and Forest), together with the University of Ghent have started a research project aimed at gaining a better understanding on chytridiomycose and ranavirose infections in amphibians in Flanders.

For more information on how you can participate and organise for dead animals to be collected, please refer to: http://www.natuurenbos.be/beleid-wetgeving/overlast-schade/wildedierenziekten/surveillances/chytridiomycose-en-ranavirose-bij

Natuurpunt also has a very informative website on the fungus. This website provides information for people who are active in forest areas, own salamanders or newts or are involved in environmental policy.

The contact at ANB for chytridiomycose is: Muriel Vervaeke: muriel.vervaeke@lne.vlaanderen.be
The contact at Natuurpunt is: Dominique Verbelen (dominique.verbelen@natuurpunt.be, 0484 119 899) and Jeroen Speybroeck (jeroenspeybroeck@hotmail.com), Natuurpunt Studie (http://www.natuurpunt.be)

Wallonia
If you find animals which you suspect might have been infected, please contact Thierry Kinet or Arnaud Laudelout salamandre@natagora.be

A monitoring of the fire salamander is starting in 2016 (http://www.natagora.be)

Ghent
The laboratories of Frank Pasmans and An Martel from the University of Ghent play a central role in our research ( Faculty of Veterinary Medicine , Department of Pathology, bacteriology and poultry diseases) http://www.ugent.be/di/di05/nl

                                   






Germany

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Germany is just across the border and there’s a resonable chance the fungus will spread. If you find dead animals or animals you suspect may have been infected, please contact:

Dr. Stefan Lötters
Trier University
Faculty of Geography/Geosciences
Biogeography Department
54286 Trier, Germany
E-mail: loetters@uni-trier.de

Dr. Sebastian Steinfartz
Technische Universität Braunschweig
Zoological Institute
Mendelssohnstr. 4
38106 Braunschweig, Germany
E-mail: s.steinfartz@tu-bs.de

References

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Parrott, J. C., Shepack, A., Burkart, D., LaBumbard, B., Scimè, P., Baruch, E., & A. Catenazzi, 2016. Survey of Pathogenic Chytrid Fungi (Batrachochytrium dendrobatidis and B. salamandrivorans) in Salamanders from Three Mountain Ranges in Europe and the Americas. EcoHealth, 1-7. [Link]

Blooi, M., et al. 2015a. Treatment of urodelans based on temperature dependent infection dynamics of Batrachochytrium salamandrivorans. Scientific Reports 5: 8037. [Link]

Blooi, M., et al. 2015b. "Successful treatment of Batrachochytrium salamandrivorans infections in salamanders requires synergy between voriconazole, polymyxin E and temperature." Scientific Reports 5. [Link]

Cunningham, A.A., K. Beckmann, M. Perkins, L. Fitzpatrick, R. Cromie, J. Redbond, M. F. O’Brien, P. Ghosh, J. Shelton & M.C. Fisher, 2015. Emerging disease in UK amphibians. Veterinary record. [Link]

Grant, E.H.C., Muths, E., Katz, R.A., Canessa, Stefano, Adam, M.J., Ballard, J.R., Berger, Lee, Briggs, C.J., Coleman, Jeremy, Gray, M.J., Harris, M.C., Harris, R.N., Hossack, Blake, Huyvaert, K.P., Kolby, J.E., Lips, K.R., Lovich, R.E., McCallum, H.I., Mendelson, J.R., III, Nanjappa, Priya, Olson, D.H., Powers, J.G., Richgels, K.L.D., Russell, R.E., Schmidt, B.R., Spitzen-van der Sluijs, Annemarieke, Watry, M.K., Woodhams, D.C., and White, C.L., 2016, Salamander chytrid fungus (Batrachochytrium salamandrivorans) in the United States—Developing research, monitoring, and management strategies: U.S. Geological Survey Open-File Report 2015–1233, 16 p., http://dx.doi.org/10.3133/ofr20151233.[link]

Gray MJ, Lewis JP, Nanjappa P, Klocke B, Pasmans F, et al. (2015) Batrachochytrium salamandrivorans: The North American Response and a Call for Action. PLoS Pathog 11(12): e1005251. doi: 10.1371/journal.ppat.1005251 [Link]

Martel, A., A. Spitzen-van der Sluijs, M. Blooi, W. Bert, R. Ducatelle, M.C. Fisher, A. Woeltjes, W. Bosman, K. Chiers, F. Bossuyt & F. Pasmans, 2013. Batrachochytrium salamandrivorans sp. nov. causes lethal chytridiomycosis in amphibians. Proc Natl Acad Sci USA 110: 15325-9. [Link]

Martel, A., M. Blooi, C. Adriaensen, P. van Rooij, W. Beukema, M.C. Fisher, R.A. Farrer, B.R. Schmidt, U. Tobler, K. Goka, K.R. Lips, C. Muletz, K.R. Zamudio, J. Bosch, S. Lötters, E. Wombwell, T.W.J. Garner, A.A. Cunningham, A. Spitzen-van der Sluijs, S. Salvidio, R. Ducatelle, K. Nishikawa, T.T. Nguyen, J.E. Kolby, I. van Bocxlaer, F. Bossuyt & F. Pasmans, 2014. Recent introduction of a chytrid fungus endangers Western Palearctic salamanders. Science 346: 630-631. [Link]

Sabino-Pinto, J., M. Bletz, R. Hendrix, R.G.B. Perl, A. Martel, F. Pasmans, S. Lötters, F. Mutschmann, D.S. Schmeller, B.R. Schmidt, M. Veith, N. Wagner, M. Vences & S. Steinfartz, 2015. First detection of the emerging fungal pathogen Batrachochytrium salamandrivorans in Germany. Amphibia Reptilia. [Link]

Spitzen - van der Sluijs, A. , F. Spikmans, W. Bosman, M. de Zeeuw, T. van der Meij, E. Goverse, M. Kik, F. Pasmans & A. Martel. 2013. Rapid enigmatic decline drives the fire salamander (Salamandra salamandra) to the edge of extinction in the Netherlands. Amphibia Reptilia  34: 233-239 [link]

Spitzen-van der Sluijs A, Martel A, Asselberghs J, Bales EK, Beukema W, Bletz MC, et al. Expanding distribution of lethal amphibian fungus Batrachochytrium salamandrivorans in Europe. Emerg Infect Dis. 2016 Jul [date cited]. http://dx.doi.org/10.3201/eid2207.160109

Van Rooij, P. A. Martel, F. Haesebrouck, F. Pasmans. 2015. Amphibian chytridiomycosis: a review with focus on fungus-host interactions. Vet Res. 46. doi: 10.1186/s13567-015-0266-0. [link]


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