ArticlePDF Available

Recent Findings of Potentially Lethal Salamander Fungus Batrachochytrium salamandrivorans

July 2019
Emerging Infectious Diseases 25(7):1416-1418

DOI:10.3201/eid2507.181001

Project: Batrachochytrium salamandrivorans

Authors:

David Lastra González

Czech University of Life Sciences Prague

Vojtech Baláž

University of Veterinary Sciences Brno

Milič Solský

Czech University of Life Sciences Prague

Barbora Thumsová

The National Museum of Natural Sciences

Show all 11 authorsHide

The distribution of the chytrid fungus Batrachochytrium salamandrivorans continues to expand in Europe. During 2014-2018, we collected 1,135 samples from salamanders and newts in 6 countries in Europe. We identified 5 cases of B. salamandrivorans in a wild population in Spain but none in central Europe or the Balkan Peninsula.

Content uploaded by David Lastra González

Content may be subject to copyright.

through routine sequencing of all enteroviruses detected in clinical

materials from 2008 to 2015. J Clin Microbiol. 2016;54:2306–14.

http://dx.doi.org/10.1128/JCM.00207-16

3. Grard G, Drexler JF, Lekana-Douki S, Caron M, Lukashev A,

Nkoghe D, et al. Type 1 wild poliovirus and putative enterovirus

109 in an outbreak of acute accid paralysis in Congo, October–

November 2010. Euro Surveill. 2010;15:pii=19723.

4. Richter J, Tryfonos C, Panagiotou C, Nikolaou E, Koliou M,

Christodoulou C. Newly emerging C group enteroviruses may

elude diagnosis due to a divergent 5′-UTR. Int J Infect Dis.

2013;17:e1245–8.

5. Todd A, Taylor S, Huang QS. Identication of enterovirus C105

for the rst time in New Zealand. Western Pac Surveill Response J.

2015;6:60–2. http://dx.doi.org/10.5365/wpsar.2014.5.4.003

6. Zhang T, Ren L, Luo M, Li A, Gong C, Chen M, et al. Enterovirus

D68–associated severe pneumonia, China, 2014. Emerg Infect Dis.

2015;21:916–8. http://dx.doi.org/10.3201/eid2105.150036

7. Nix WA, Oberste MS, Pallansch MA. Sensitive, seminested PCR

amplication of VP1 sequences for direct identication of all

enterovirus serotypes from original clinical specimens. J Clin Micro-

biol. 2006;44:2698–704. http://dx.doi.org/10.1128/JCM.00542-06

8. Oberste MS, Penaranda S, Rogers SL, Henderson E, Nix WA.

Comparative evaluation of Taqman real-time PCR and semi-nested

VP1 PCR for detection of enteroviruses in clinical specimens.

J Clin Virol. 2010;49:73–4.

9. Barnadas C, Midgley SE, Skov MN, Jensen L, Poulsen MW,

Fischer TK. An enhanced enterovirus surveillance system allows

identication and characterization of rare and emerging respiratory

enteroviruses in Denmark, 2015–16. J Clin Virol. 2017;93:40–4.

Address for correspondence: Fang Huang, Beijing Center for Disease

Prevention and Control, Institute for Communicable Disease Control

and Prevention, No. 16, Hepingli Middle Av, Dongcheng District,

Beijing 100013, China; email: hhxdd@126.com

Recent Findings of Potentially

Lethal Salamander Fungus

Batrachochytrium

salamandrivorans

David Lastra González, Vojtech Baláž,

Milič Solský, Barbora Thumsová,

Krzysztof Kolenda, Anna Najbar,

Bartłomiej Najbar, Matej Kautman, Petr Chajma,

Monika Balogová, Jiří Vojar

Author aliations: Czech University of Life Sciences, Prague,

Czech Republic (D. Lastra González, M. Solský, B. Thumsová,

P. Chajma, J. Vojar); University of Veterinary and Pharmaceutical

Sciences, Brno, Czech Republic (V. Baláž, M. Kautman);

University of Wrocławski, Wroclaw, Poland (K. Kolenda,

A. Najbar); University of Zielona Góra, Lubuskie, Poland

(B. Najbar); Slovak Academy of Sciences, Košice, Slovakia

(M. Kautman); Pavol Jozef Šafárik University in Košice, Košice

(M. Balogová)

DOI: https://doi.org/10.3201/eid2507.181001

The distribution of the chytrid fungus Batrachochytrium

salamandrivorans continues to expand in Europe. During

2014–2018, we collected 1,135 samples from salamanders

and newts in 6 countries in Europe. We identied 5 cases of

B. salamandrivorans in a wild population in Spain but none

in central Europe or the Balkan Peninsula.

Chytridiomycosis, an amphibian disease caused by the

chytrid fungi Batrachochytrium dendrobatidis and B.

salamandrivorans, is responsible for declines of amphib-

ian populations worldwide (1). The recently discovered B.

salamandrivorans (2) is severely impacting salamanders

and newts in Europe (3,4). This emerging fungal pathogen

infects the skin of caudates and causes lethal lesions (2). It

most likely was introduced to Europe by the pet salamander

trade from Southeast Asia (3). In Europe, the Netherlands,

Belgium, and Germany have conrmed B. salamandriv-

orans in wild caudates; the United Kingdom, Germany,

and Spain have conrmed the fungus in captive animals

(5,6). Several countries have established trade regulations

(5) and a recent European Union decision, no. 2018/320,

implements measures to protect against the spread of B.

salamandrivorans via traded salamanders (7). The World

Organisation for Animal Health listed infection with B.

salamandrivorans as a notiable disease in 2017. In ad-

dition to controlling the amphibian pet trade, surveillance

of the pathogen is urgently needed to establish disease in-

tervention strategies in aected areas and prevention in B.

salamandrivorans–free regions.

During 2014–2018, we collected 1,135 samples directly

for the detection of B. salamandrivorans or as a part of unre-

lated studies. Samples came from 10 amphibian species at 47

sites in 6 countries in Europe. Most samples came from the

re salamander, Salamandra salamandra, which is a known

suitable host for B. salamandrivorans (3), and the palmate

newt, Lissotriton helveticus, which is known to be resistant

to B. salamandrivorans (Appendix Table 1, http://wwwnc.

cdc.gov/EID/article/25/7/18-1001-App1.pdf).

Most samples were skin swabs collected by following

the standard procedure for sampling of amphibian chytrid

fungi (8). A smaller portion of samples was toe clippings

(Appendix Table 2). We extracted genomic DNA following

the protocol of Blooi et al. (9), and 2 laboratories with dif-

ferent equipment tested for B. salamandrivorans. Samples

from Spain and the Czech Republic initially were analyzed

at the Czech University of Life Sciences (Prague, Czech

1416 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 25, No. 7, July 2019

RESEARCH LETTERS

Republic) by standard PCR with B. salamandrivorans–

specic primers STerF and STerR, as described by Martel

et al. (2), with subsequent electrophoresis on the ampli-

ed target. We reanalyzed samples that produced positive

or equivocal results by using duplex quantitative PCR

(qPCR) for B. dendrobatidis and B. salamandrivorans (9)

at the University of Veterinary and Pharmaceutical Scienc-

es (Brno, Czech Republic). Trenton Garner of the Institute

of Zoology, Zoological Society of London (London, Eng-

land), provided DNA for quantication standards of the B.

dendrobatidis GPL lineage, strain IA042, and An Martel

of Ghent University (Ghent, Belgium) provided quantica-

tion standards of B. salamandrivorans.

We directly analyzed samples from other countries by

qPCR. We used negative and positive controls for standard

PCR analyses and quantication standards for qPCR analy-

ses. For B. dendrobatidis– or B. salamandrivorans–posi-

tive sites, we estimated prevalence and Bayesian 95% CIs

using 3 parallel Markov chains with 2,000 iterations each,

a burn-in of 1,000 iterations, and no thinning (Appendix

Table 1). We performed all statistical analyses in R 3.3.1

using the R2WinBUGS package and WinBUGS 1.4.3 (10).

Samples from 5 L. helveticus newts tested positive

for B. salamandrivorans, implying that this species is

not resistant to this fungus as previously indicated by ex-

perimental exposures (3). The positive cases were found

in populations from an isolated area encompassing 2 dif-

ferent regions in northern Spain, Cantabria and Asturias,

with remote human populations. Four cases were found in

livestock drinking troughs located 150–1,000 m above sea

level, and 1 case was found in a pond in a private garden,

30 km from the nearest recorded case. We did not nd B.

salamandrivorans–positive cases in consecutive locations

during our monitoring.

Although B. salamandrivorans cases have been re-

ported in captive salamanders (6), our reported cases were

>1,000 km from any area of known B. salamandrivorans

occurrence (7). We also detected B. dendrobatidis by du-

plex qPCR in 11 samples from 3 newt species (L. helve-

ticus, L. vulgaris, and Triturus cristatus) from Spain and

Montenegro and 1 captive Cynops ensicauda newt from the

Czech Republic. The B. dendrobatidis–positive cases did

not involve co-infection with B. salamandrivorans.

We conrmed that the known distribution of B. sala-

mandrivorans continues to expand in Europe, indicating

that this fungus might be capable of dispersing over long

distances (4), might be introduced by humans, or might

even have been circulating in this geographic range with

no detected deaths. Our results should alert the research

and conservation community and motivate urgent action to

identify regions with early emergence of the disease and

implement mitigation measures to prevent further spread

of this deadly pathogen.

Acknowledgments

We thank the Cantabria delegation of SEO/Birdlife; Fundación

Zoo Santillana del Mar; workers from Marismas de Santoña,

Victoria y Joyel Natural Park, with special thanks to

Carlos Rubio; Pepo Nieto, Pedro Barreda, and his family;

Elena Kulikova and Wiesław Babik; and also our friends

Daniel Koleška, Kamila Šimůnková, Tomáš Holer, and

Daniela Budská for eldwork.

This work was performed with permission from the Nature

Conservation Agency of the Czech Republic; Agency for Nature

and Environment Protection of Montenegro permit no. 02 Broj

UPI–321/4; Ministry of Environment of the Slovak Republic,

permit no. 4924/2017–6.3; the Endangered Species Section of

Environmental Service of Cantabria, Spain, permit no. EST–

419/2017–SEP; the Environmental Service of Castilla y León,

Spain, permit no. EP/LE/233/2017; Department of Nature

Conservation of Poland, permit nos. DZP-WG.6401.02.7.2014.

JRO, WPN.6401.211.2015.MR.2, 78/2014, and 68/2015; the

Ministry of Protection of Environment of Croatia, permit no.

UP/I–612–07/169–48/68; and agreements from other agencies,

including Red Cambera, special thanks to Sergio Tejón and Tomás

González; Fondo para la Protección de los Animales Salvajes; and

Fundación Naturaleza y Hombre, Spain. The study was supported

by the Czech University of Life Sciences, Prague, Czech Republic

(grant nos. 20174218 and 20184247) and the Internal Grant

Agency of the University of Veterinary and Pharmaceutical

Sciences, Brno, Czech Republic (grant no. 224/2016/FVHE).

K.K. was supported by MNiSW grant for Young Scientists no.

0420/1408/16; A.N. was supported by grant no. DS 1076/S/

IBŚ/2014 and MNiSW grant for Young Scientists no. 0420/1409/16.

About the Author

Mr. Lastra González is a PhD candidate at Czech University

of Life Sciences, Prague. His research focuses on amphibian

conservation and emerging infectious diseases that aect them.

References

1. Berger L, Roberts AA, Voyles J, Longcore JE, Murray KA,

Skerratt LF. History and recent progress on chytridiomycosis in

amphibians. Fungal Ecol. 2016;19:89–99. http://dx.doi.org/

10.1016/j.funeco.2015.09.007

2. Martel A, Spitzen-van der Sluijs A, Blooi M, Bert W,

Ducatelle R, Fisher MC, et al. Batrachochytrium salamandrivorans

sp. nov. causes lethal chytridiomycosis in amphibians. Proc Natl

Acad Sci U S A. 2013;110:15325–9. http://dx.doi.org/10.1073/

pnas.1307356110

3. Martel A, Blooi M, Adriaensen C, Van Rooij P, Beukema W,

Fisher MC, et al. Recent introduction of a chytrid fungus endangers

Western Palearctic salamanders. Science. 2014;346:630–1.

http://dx.doi.org/10.1126/science.1258268

4. Stegen G, Pasmans F, Schmidt BR, Rouaer LO, Van Praet S,

Schaub M, et al. Drivers of salamander extirpation mediated by

Batrachochytrium salamandrivorans. Nature. 2017;544:353–6.

http://dx.doi.org/10.1038/nature22059

Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 25, No. 7, July 2019 1417

RESEARCH LETTERS

5. European Food Safety Authority Panel on Animal Health and

Welfare, More S, Angel Miranda M, Bicout D, Bøtner A,

Butterworth A, et al. Risk of survival, establishment and spread of

Batrachochytrium salamandrivorans (Bsal) in the EU. EFSA

Journal. 2018;16:5259. http://dx.doi.org/10.2903/j.efsa.2018.5259

6. Fitzpatrick LD, Pasmans F, Martel A, Cunningham AA.

Epidemiological tracing of Batrachochytrium salamandrivorans

identies widespread infection and associated mortalities in private

amphibian collections. Sci Rep. 2018;8:13845. http://dx.doi.org/

10.1038/s41598-018-31800-z

7. Commission Implementing Decision (EU) 2018/320 of 28

February 2018 on certain animal health protection measures for

intra-Union trade in salamanders and the introduction into the

Union of such animals in relation to the fungus Batrachochytrium

salamandrivorans. Ocial Journal of the European Union.

2018;L62:18–33 [cited 2018 Jun 1]. http://data.europa.eu/eli/

dec_impl/2018/320/oj

8. Hyatt AD, Boyle DG, Olsen V, Boyle DB, Berger L, Obendorf D,

et al. Diagnostic assays and sampling protocols for the detection of

Batrachochytrium dendrobatidis. Dis Aquat Organ. 2007;73:175–

92. http://dx.doi.org/10.3354/dao073175

9. Blooi M, Pasmans F, Longcore JE, Spitzen-van der Sluijs A,

Vercammen F, Martel A. Duplex real-time PCR for rapid

simultaneous detection of Batrachochytrium dendrobatidis and

Batrachochytrium salamandrivorans in amphibian samples. J Clin

Microbiol. 2013;51:4173–7. http://dx.doi.org/10.1128/JCM.02313-13

10. Lunn DJ, Thomas A, Best N, Spiegelhalter D. WinBUGS–

a Bayesian modelling framework: concepts, structure, and

extensibility. Stat Comput. 2000;10:325–37. http://dx.doi.org/

10.1023/A:1008929526011

Address for correspondence: David Lastra González, Faculty of

Environmental Sciences, Czech University of Life Sciences,

Kamýcká 129, 165 21 Prague–Suchdol, Czech Republic;

email: lastra_gonzalez@fzp.czu.cz

Crimean-Congo Hemorrhagic

Fever Virus Genome in Tick

from Migratory Bird, Italy

Elisa Mancuso, Luciano Toma, Andrea Polci,

Silvio G. d’Alessio, Marco Di Luca,

Massimiliano Orsini, Marco Di Domenico,

Maurilia Marcacci, Giuseppe Mancini,

Fernando Spina, Maria Goredo,

Federica Monaco

Author aliations: Istituto Zooprolattico Sperimentale

dell’Abruzzo e del Molise “G. Caporale,” Teramo, Italy

(E. Mancuso, A. Polci, S.G. d’Alessio, M. Orsini,

M. Di Domenico, M. Marcacci, G. Mancini, M. Goredo,

F. Monaco); Istituto Superiore di Sanità, Rome, Italy (L. Toma,

M. Di Luca); Istituto Superiore per la Protezione e la Ricerca

Ambientale, Bologna, Italy (F. Spina)

DOI: https://doi.org/10.3201/eid2507.181345

We detected Crimean-Congo hemorrhagic fever virus in a

Hyalomma rupes nymph collected from a whinchat (Saxi-

cola rubetra) on the island of Ventotene in April 2017. Partial

genome sequences suggest the virus originated in Africa.

Detection of the genome of this virus in Italy conrms its

potential dispersion through migratory birds.

Crimean-Congo hemorrhagic fever virus (CCHFV) is a

vectorborne virus responsible for severe illness in hu-

mans, whereas other mammals usually act as asymptomatic

reservoirs. The virus is transmitted through tick bites or by

direct contact with blood or body uids of infected verte-

brate hosts. CCHFV, an Orthonairovirus within the Nairo-

viridae family, has a negative-sense tripartite RNA genome

characterized by high genetic diversity. The sequences of

the circulating strains cluster in 6 genotypes (I–VI) reect-

ing their geographic origin; worldwide distribution is the

result of ecient dispersion through migratory birds, hu-

man travelers, and the trade and movement of livestock and

wildlife (1,2). In Europe, CCHFV distribution was limited

to the Balkan region until 2010, when the virus was iden-

tied in ticks collected from a red deer (Cervus elaphus)

and, 6 years later, in 2 autochthonous human cases in the

same region of Spain (3). Sequences from the Iberia strains

clustered in the Africa genotype III (4), supporting the hy-

pothesis of CCHFV dispersion through ticks hosted by mi-

grating birds.

The role of birds in the potential spread of the virus

was conrmed by CCHFV detection in ticks collected from

migratory birds in Greece in 2009 (5) and Morocco in 2011

(6). Because Italy hosts an intense passage of birds migrat-

ing along major routes connecting winter quarters in Africa

and breeding areas in Europe, the country is potentially

exposed to the risk for virus introduction. We report the

detection of CCHFV RNA in a tick collected in Italy from

a migratory bird.

We conducted tick sampling during March–May 2017

on the island of Ventotene, where a ringing station has been

operating since 1988 as part of the Small Islands Project, a

large-scale and long-term eort to monitor spring migra-

tions of birds across the central and western Mediterranean.

We ringed 5,095 birds and checked ≈80% for ectoparasites.

We collected 14 adults, 330 nymphs, and 276 larvae from

268 passerines belonging to 28 species; 18 species were

trans-Saharan migrants. We stored ticks in 70% ethanol

until morphologic identication and assignment to a genus

or, whenever possible, a species (7). We then individually

1418 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 25, No. 7, July 2019

RESEARCH LETTERS

Batrachochytrium salamandrivorans Threat to the Iberian Urodele Hotspot

Article

Full-text available

Aug 2021
J. Fungi

The recent introduction of the chytrid fungus Batrachochytrium salamandrivorans into northeastern Spain threatens salamander diversity on the Iberian Peninsula. We assessed the current epidemiological situation with extensive field sampling of urodele populations. We then sought to delineate priority regions and identify conservation units for the Iberian Peninsula by estimating the susceptibility of Iberian urodeles using laboratory experiments, evidence from mortality events in nature and captivity and inference from phylogeny. None of the 1395 field samples, collected between 2015 and 2021 were positive for Bsal and no Bsal-associated mortality events were recorded, in contrast to the confirmed occurrence of Bsal outbreak previously described in 2018. We classified five of eleven Iberian urodele species as highly susceptible, predicting elevated mortality and population declines following potential Bsal emergence in the wild, five species as intermediately susceptible with variable disease outcomes and one species as resistant to disease and mortality. We identified the six conservation units (i.e., species or lineages within species) at highest risk and propose priority areas for active disease surveillance and field biosecurity measures. The magnitude of the disease threat identified here emphasizes the need for region-tailored disease abatement plans that couple active disease surveillance to rapid and drastic actions.

Dual Detection of the Chytrid Fungi Batrachochytrium spp. with an Enhanced Environmental DNA Approach

Article

Full-text available

Mar 2021
J. Fungi

Environmental DNA (eDNA) is becoming an indispensable tool in biodiversity monitoring, including the monitoring of invasive species and pathogens. Aquatic chytrid fungi Batrachochytrium dendrobatidis (Bd) and B. salamandrivorans (Bsal) are major threats to amphibians. However, the use of eDNA for detecting these pathogens has not yet become widespread, due to technological and economic obstacles. Using the enhanced eDNA approach (a simple and cheap sampling protocol) and the universally accepted qPCR assay, we confirmed the presence of Bsal and Bd in previously identified sites in Spain, including four sites that were new for Bsal. The new approach was successfully tested in laboratory conditions using manufactured gene fragments (gBlocks) of the targeted DNA sequence. A comparison of storage methods showed that samples kept in ethanol had the best DNA yield. Our results showed that the number of DNA copies in the Internal Transcribed Spacer region was 120 copies per Bsal cell. Eradication of emerging diseases requires quick and cost-effective solutions. We therefore performed cost-efficiency analyses of standard animal swabbing, a previous eDNA approach, and our own approach. The procedure presented here was evaluated as the most cost-efficient. Our findings will help to disseminate information about efforts to prevent the spread of chytrid fungi.

Surveying for presence of salamander-killer fungus in Spanish captive collections of amphibians

Article

Dec 2020

ABSTRACT: Batrachochytrium salamandrivorans (Bsal), a pathogenic fungus causing the fatal disease chytridiomycosis in amphibians, was likely introduced to Europe through the trade in pet salamanders from Asia and then escaped into wild populations. Among European countries, Spain has a large number of private breeders and keepers of pet salamanders, and cases of Bsal in wild and captive populations already have been confirmed there. However, surveillance for the pathogen in Spanish collections of amphibians is sparse. Therefore, assisted by private owners and breeders, we surveyed 10 amphibian collections and analysed a total of 317 samples for presence of Bsal. All of our analyses yielded negative results. However, this apparent lack of Bsal cases in captivity should not encourage relaxation of vigilance, quarantine efforts or good practices. Because amphibian collections represent highly dynamic environments (animals are coming in and out), the pathogen could easily be introduced into a collection by new individuals. Any case of Bsal infection in captive animals could lead to its further spread to wild populations of susceptible species, potentially decimating them, and thus should be prevented.

Detection of Ophidiomyces ophidiicola in a wild Burmese python (Python bivittatus) in Hong Kong SAR, China.

Article

Full-text available

Dec 2021

Ophidiomycosis (also referred to as snake fungal disease) is an emerging infectious disease caused by Ophidiomyces ophidiicola (Oo). PCR was used to detect Oo in a Burmese python (Python bivittatus) with skin lesions submitted to a rescue center in Hong Kong. This is the first report of this disease in this species. More research is needed in Asia to determine the prevalence of this fungus, its relationship with other species, and its ecological importance. These findings also highlight the significant role wildlife rescue centers play in monitoring wildlife diseases and ecosystem health.

Emerging infectious diseases of amphibians in Poland: distribution and environmental drivers

Article

Nov 2021

Emerging infectious diseases are a threat to biodiversity and have taken a large toll on amphibian populations worldwide. The chytrid fungi Batrachochytrium dendrobatidis ( Bd ) and B. salamandrivorans ( Bsal ), and the iridovirus Ranavirus ( Rv ), are of concern as all have contributed to amphibian declines. In central and eastern Europe, their geographical and host distributions and main environmental drivers determining prevalence are poorly known. We screened over 1000 amphibians from natural and captive populations in Poland for the presence of Bd , Bsal and Rv . In wild amphibian populations, we found that Bd is widespread, present in 46 out of 115 sampled localities as well as 2 captive colonies, and relatively common with overall prevalence at 14.4% in 9 species. We found lower prevalence of Rv at 2.4%, present in 11 out of 92 sampling sites, with a taxonomic breadth of 8 different amphibian species. Bsal infection was not detected in any individuals. In natural populations, Pelophylax esculentus and Bombina variegata accounted for 75% of all Bd infections, suggesting a major role for these 2 species as pathogen reservoirs in Central European freshwater habitats. General linear models showed that climatic as well as landscape features are associated with Bd infection in Poland. We found that higher average annual temperature constrains Bd infection, while landscapes with numerous water bodies or artificial elements (a surrogate for urbanization) increase the chances of infection. Our results show that a combination of climatic and landscape variables may drive regional and local pathogen emergence.

Conservation risk of Batrachochytrium salamandrivorans to endemic lungless salamanders

Article

Full-text available

Sep 2019

The emerging fungal pathogen, Batrachochytrium salamandrivorans (Bsal), is a significant conservation threat to salamander biodiversity in Europe, although its potential to affect North American species is poorly understood. We tested the susceptibility of two genera (Eurycea and Pseudotriton) and three populations of lungless salamanders (Plethodontidae) to Bsal. All species became infected with Bsal and two (Pseudotriton ruber and Eurycea wilderae) developed chytridiomycosis. We also documented that susceptibility of E. wilderae differed among populations. Regardless of susceptibility, all species reduced feeding when exposed to Bsal at the highest zoospore dose, and P. ruber and one population of E. wilderae used cover objects less. Our results indicate that Bsal invasion in eastern North America could have significant negative impacts on endemic lungless salamander populations. Future conservation efforts should include surveillance for Bsal in the wild and in captivity, and championing legislation that requires and subsidizes pathogen‐free trade of amphibians.

Pandemie wśród płazów

Article

Full-text available

Dec 2021

Płazy to jedna z najbardziej zagrożonych grup zwierząt na świecie, głównie ze względu na niszczenie ich siedlisk przez człowieka. W dobie koronawirusowej pandemii warto wspomnieć również o chorobach, z którymi ta grupa kręgowców mierzy się już od wielu lat. Choroby zakaźne wywołane przez mikroskopijne grzyby pasożytnicze Batrachochytrium dendrobatidis i B. salamandrivorans, a także różne formy ranawirusów (Ranavirus) stanowią ogromne zagrożenie dla płazów, dziesiątkując ich populacje na całym świecie, także w Europie. Przedstawiamy najnowsze doniesienia na temat rozmieszczenia najważniejszych patogenów płazów, w tym także z Polski, oraz perspektywy zachowania płazów w obliczu trwających pandemii. Podsumowujemy również najistotniejsze działania prewencyjne, ograniczające rozprzestrzenianie się patogenów, a także przytaczamy przykłady działań mających eliminować chorobotwórcze organizmy ze środowiska. Artykuł ma na celu zwiększenie świadomości społecznej dotyczącej patogenów, mogącej wpłynąć na podjęcie skutecznych działań zmniejszających negatywne skutki pandemii wśród płazów.

Emerging infectious disease threats to European herpetofauna

Article

Full-text available

Oct 2019
HERPETOL J

In the past decade, infectious disease threats to European herpetofauna have become better understood. Since the 1990s, three major emerging infections in amphibians have been identified (Batrachochytrium dendrobatidis, B. salamandrivorans, and ranaviruses) as well as at least one of unknown status (herpesviruses), while two major emerging infections of reptiles (Ophidiomyces ophiodiicola and ranaviruses) have been identified in wild European populations. The effects of emerging infections on populations have ranged from non-existent to local extirpation. In this article, we review these major infectious disease threats to European herpetofauna, including descriptions of key mortality and/or morbidity events in Europe of their emergence, and address both the distribution and the host diversity of the agent. Additionally, we direct the reader to newly developed resources that facilitate the study of infectious agents in herpetofauna and again stress the importance of an interdisciplinary approach to examining these infectious diseases.

Emerging infectious disease threats to European herpetofauna

Article

Full-text available

Oct 2019
HERPETOL J

Epidemiological Tracing of Batrachochytrium Salamandrivorans Identifies Widespread Infection and Associated Mortalities in Private Amphibian Collections

Article

Full-text available

Sep 2018

The amphibian chytrid fungus Batrachochytrium salamandrivorans (Bsal) infects newts and salamanders (urodele amphibians), in which it can cause fatal disease. This pathogen has caused dramatic fire salamander population declines in Belgium, the Netherlands and Germany since its discovery in 2010. Thought to be native to Asia, it has been hypothesised that Bsal was introduced to Europe with the importation of infected amphibians for the commercial pet trade. Following the discovery of Bsal in captive amphibians in the United Kingdom in 2015, we used contact-tracing to identify epidemiologically-linked private amphibian collections in Western Europe. Of 16 linked collections identified, animals were tested from 11 and urodeles tested positive for Bsal in seven, including the identification of the pathogen in Spain for the first time. Mortality of Bsal-positive individuals was observed in five collections. Our results indicate that Bsal is likely widespread within the private amphibian trade, at least in Europe. These findings are important for informing policy regarding Bsal control strategies.

Risk of survival, establishment and spread of Batrachochytrium salamandrivorans (Bsal) in the EU

Article

Full-text available

Apr 2018

Batrachochytrium salamandrivorans (Bsal) is an emerging fungal pathogen of salamanders. Despite limited surveillance, Bsal was detected in kept salamanders populations in Belgium, Germany, Spain, the Netherlands and the United Kingdom, and in wild populations in some regions of Belgium, Germany and the Netherlands. According to niche modelling, at least part of the distribution range of every salamander species in Europe overlaps with the climate conditions predicted to be suitable for Bsal. Passive surveillance is considered the most suitable approach for detection of Bsal emergence in wild populations. Demonstration of Bsal absence is considered feasible only in closed populations of kept susceptible species. In the wild, Bsal can spread by both active (e.g. salamanders, anurans) and passive (e.g. birds, water) carriers; it is most likely maintained/spread in infected areas by contacts of salamanders or by interactions with anurans, whereas human activities most likely cause Bsal entry into new areas and populations. In kept amphibians, Bsal contamination via live silent carriers (wild birds and anurans) is considered extremely unlikely. The risk‐mitigation measures that were considered the most feasible and effective: (i) for ensuring safer international or intra‐EU trade of live salamanders, are: ban or restrictions on salamander imports, hygiene procedures and good practice manuals; (ii) for protecting kept salamanders from Bsal, are: identification and treatment of positive collections; (iii) for on‐site protection of wild salamanders, are: preventing translocation of wild amphibians and release/return to the wild of kept/temporarily housed wild salamanders, and setting up contact points/emergency teams for passive surveillance. Combining several risk‐mitigation measures improve the overall effectiveness. It is recommended to: introduce a harmonised protocol for Bsal detection throughout the EU; improve data acquisition on salamander abundance and distribution; enhance passive surveillance activities; increase public and professionals’ awareness; condition any movement of captive salamanders on Bsal known health status.

Drivers of salamander extirpation mediated by Batrachochytrium salamandrivorans

Article

Full-text available

Apr 2017
NATURE

The recent arrival of Batrachochytrium salamandrivorans in Europe was followed by rapid expansion of its geographical distribution and host range, confirming the unprecedented threat that this chytrid fungus poses to western Palaearctic amphibians. Mitigating this hazard requires a thorough understanding of the pathogen's disease ecology that is driving the extinction process. Here, we monitored infection, disease and host population dynamics in a Belgian fire salamander (Salamandra salamandra) population for two years immediately after the first signs of infection. We show that arrival of this chytrid is associated with rapid population collapse without any sign of recovery, largely due to lack of increased resistance in the surviving salamanders and a demographic shift that prevents compensation for mortality. The pathogen adopts a dual transmission strategy, with environmentally resistant non-motile spores in addition to the motile spores identified in its sister species B. dendrobatidis. The fungus retains its virulence not only in water and soil, but also in anurans and less susceptible urodelan species that function as infection reservoirs. The combined characteristics of the disease ecology suggest that further expansion of this fungus will behave as a 'perfect storm' that is able to rapidly extirpate highly susceptible salamander populations across Europe.

History and recent progress on chytridiomycosis in amphibians

Article

Full-text available

Feb 2016
FUNGAL ECOL

Batrachochytrium dendrobatidis (Bd) emerged in the 1970s in Australia and the Americas, causing rapid and catastrophic declines and extinctions of naïve amphibian populations as it spread through remote rainforest and alpine regions. The description of chytridiomycosis in 1998 stimulated a large and diverse global research effort, including studies on phylogeny, distribution, ecology, and virulence - but mitigating its effect remains a major challenge. In 2010 a second Batrachochytrium species, B. salamandrivorans (Bsal), emerged after spreading to Europe from Asia and has decimated fire salamanders in the Netherlands and Belgium. Bsal appears to be restricted to salamanders and newts whereas Bd can infect all amphibian orders. These cases show that despite the current advanced state of globalisation, severe pathogens are still spreading and some may currently be excluded by geographic barriers, hence biosecurity still has potential to mitigate spread of undiscovered and unpredictable pathogens of wildlife.

Recent introduction of a chytrid fungus endangers Western Palearctic salamanders

Article

Full-text available

Oct 2014
SCIENCE

Emerging infectious diseases are reducing biodiversity on a global scale. Recently, the emergence of the chytrid fungus Batrachochytrium salamandrivorans resulted in rapid declines in populations of European fire salamanders. Here, we screened more than 5000 amphibians from across four continents and combined experimental assessment of pathogenicity with phylogenetic methods to estimate the threat that this infection poses to amphibian diversity. Results show that B. salamandrivorans is restricted to, but highly pathogenic for, salamanders and newts (Urodela). The pathogen likely originated and remained in coexistence with a clade of salamander hosts for millions of years in Asia. As a result of globalization and lack of biosecurity, it has recently been introduced into naïve European amphibian populations, where it is currently causing biodiversity loss.and remained in coexistence with a clade of salamander hosts for millions of years in Asia. As a result of globalization and lack of biosecurity, it has recently been introduced into naïve European amphibian populations, where it is currently causing biodiversity loss.

Recent introduction of a chytrid fungus endangers Western Palearctic salamanders

Article

Full-text available

Oct 2014

Duplex Real-Time PCR for Rapid Simultaneous Detection of Batrachochytrium dendrobatidis and Batrachochytrium salamandrivorans in Amphibian Samples

Article

Full-text available

Oct 2013
J CLIN MICROBIOL

Chytridiomycosis is a lethal fungal disease contributing to declines and extinctions of amphibian species worldwide. The currently used molecular screening tests for chytridiomycosis fail to detect the recently described species Batrachochytrium salamandrivorans. In this study, we present a duplex real-time PCR that allows the simultaneous detection of B. salamandrivorans and Batrachochytrium dendrobatidis. With B. dendrobatidis- and B. salamandrivorans-specific primers and probes, detection of the two pathogens in amphibian samples is possible, with a detection limit of 0.1 genomic equivalent of zoospores of both pathogens per PCR. The developed real-time PCR shows high degrees of specificity and sensitivity, high linear correlations (r2 > 0.995), and high amplification efficiencies (>94%) for B. dendrobatidis and B. salamandrivorans. In conclusion, the described duplex real-time PCR can be used to detect DNA of B. dendrobatidis and B. salamandrivorans with highly reproducible and reliable results.

Batrachochytrium salamandrivorans sp. nov. causes lethal chytridiomycosis in amphibians

Article

Full-text available

Sep 2013
P NATL ACAD SCI USA

The current biodiversity crisis encompasses a sixth mass extinction event affecting the entire class of amphibians. The infectious disease chytridiomycosis is considered one of the major drivers of global amphibian population decline and extinction and is thought to be caused by a single species of aquatic fungus, Batrachochytrium dendrobatidis. However, several amphibian population declines remain unexplained, among them a steep decrease in fire salamander populations (Salamandra salamandra) that has brought this species to the edge of local extinction. Here we isolated and characterized a unique chytrid fungus, Batrachochytrium salamandrivorans sp. nov., from this salamander population. This chytrid causes erosive skin disease and rapid mortality in experimentally infected fire salamanders and was present in skin lesions of salamanders found dead during the decline event. Together with the closely related B. dendrobatidis, this taxon forms a well-supported chytridiomycete clade, adapted to vertebrate hosts and highly pathogenic to amphibians. However, the lower thermal growth preference of B. salamandrivorans, compared with B. dendrobatidis, and resistance of midwife toads (Alytes obstetricans) to experimental infection with B. salamandrivorans suggest differential niche occupation of the two chytrid fungi.

Diagnostic assay and sampling protocols for the detection of Batrachochytrium dendrobatidis

Article

Full-text available

Feb 2007

Batrachochytrium dendrobatidis is a fungus belonging to the Phylum Chytridiomycota, Class Chytridiomycetes, Order Chytridiales, and is the highly infectious aetiological agent responsible for a potentially fatal disease, chytridiomycosis, which is currently decimating many of the world's amphibian populations. The fungus infects 2 amphibian orders (Anura and Caudata), 14 families and at least 200 species and is responsible for at least 1 species extinction. Whilst the origin of the agent and routes of transmission are being debated, it has been recognised that successful management of the disease will require effective sampling regimes and detection assays. We have developed a range of unique sampling protocols together with diagnostic assays for the detection of B. dendrobatidis in both living and deceased tadpoles and adults. Here, we formally present our data and discuss them in respect to assay sensitivity, specificity, repeatability and reproducibility. We suggest that compliance with the recommended protocols will avoid the generation of spurious results, thereby providing the international scientific and regulatory community with a set of validated procedures which will assist in the successful management of chytridiomycosis in the future.

WinBUGS - A Bayesian modeling framework: Concepts, structure and extensibility

Article

Oct 2000

WinBUGS is a fully extensible modular framework for constructing and analysing Bayesian full probability models. Models may be specified either textually via the BUGS language or pictorially using a graphical interface called DoodleBUGS. WinBUGS processes the model specification and constructs an object-oriented representation of the model. The software offers a user-interface, based on dialogue boxes and menu commands, through which the model may then be analysed using Markov chain Monte Carlo techniques. In this paper we discuss how and why various modern computing concepts, such as object-orientation and run-time linking, feature in the software's design. We also discuss how the framework may be extended. It is possible to write specific applications that form an apparently seamless interface with WinBUGS for users with specialized requirements. It is also possible to interface with WinBUGS at a lower level by incorporating new object types that may be used by WinBUGS without knowledge of the modules in which they are implemented. Neither of these types of extension require access to, or even recompilation of, the WinBUGS source-code.