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Recent Findings of Potentially Lethal Salamander Fungus Batrachochytrium salamandrivorans

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

DOI:10.3201/eid2507.181001

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Authors:

David Lastra González

University of the Ryukyus

Vojtech Baláž

University of Veterinary Sciences Brno

Milič Solský

Czech University of Life Sciences Prague

Barbora Thumsová

The National Museum of Natural Sciences

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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.

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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.

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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’ Amphibian Host Species and Invasion Range

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Batrachochytrium salamandrivorans (Bsal), a species related to the destructive pathogen Batrachochytrium dendrobatidis (Bd), was found and identified in Europe in 2013. Now, a decade later, a large amount of information is available. This includes data from studies in the field, reports of infection in captive amphibians, laboratory studies testing host susceptibility, and data from prospective studies that test for Bsal ’s presence in a location. We conducted a systematic review of the published literature and compiled a dataset of Bsal tests. We identified 67 species that have been reported positive for Bsal, 20 of which have a threatened conservation status. The distribution of species that have been found with infection encompasses 69 countries, highlighting the potential threat that Bsal poses. We point out where surveillance to detect Bsal have taken place and highlight areas that have not been well monitored. The large number of host species belonging to the families Plethodontidae and Salamandridae suggests a taxonomic pattern of susceptibility. Our results provide insight into the risk posed by Bsal and identifies vulnerable species and areas where surveillance is needed to fill existing knowledge gaps.

A spatially explicit risk assessment of salamander populations to Batrachochytrium salamandrivorans in the United States

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Full-text available

Sep 2022
DIVERS DISTRIB

Aim Amphibian populations are threatened globally by anthropogenic change and Batrachochytrium dendrobatidis (Bd), a fungal pathogen causing chytridiomycosis disease to varying degrees of severity. A closely related new fungal pathogen, Batrachochytrium salamandrivorans (Bsal), has recently left its supposed native range in Asia and decimated some salamander populations in Europe. Despite being noticed initially for causing chytridiomycosis‐related population declines in salamanders, Bsal can also infect anurans and cause non‐lethal chytridiomycosis or asymptomatic infections in salamanders. Bsal has not yet been detected in the United States, but given the United States has the highest salamander biodiversity on Earth, predictive assessments of salamander risk to Bsal infection will enable proactive allocation of research and conservation efforts into disease prevention and mitigation. Location The United States, Europe and Asia. Methods We first predicted the environmental suitability for the Bsal pathogen in the United States through an ecological niche model based on the pathogen's known native range in Asia, validated on the observed invasive range in Europe using bioclimatic, land cover, elevation, soil characteristics and human modification variables. Second, we predicted the susceptibility of salamander species to Bsal infection using a machine‐learning model that correlated life history traits with published data on confirmed species infections. Finally, we mapped the geographic ranges of the subset of species that were predicted to be susceptible to Bsal infection. Results In the United States, the overlap of environmental suitability and susceptible salamander species was greatest in the Pacific Northwest, near the Gulf of Mexico, and along the Atlantic coast, and in inland states east of the Plains region. Main Conclusions The overlap of these metrics identify salamander populations that may be at risk of developing Bsal infection and suggests priorities for pre‐emptive research and conservation measures to protect at‐risk salamander species from an additional pathogenic threat.

Lack of variations in the salamander chytrid fungus, Batrachochytrium salamandrivorans, at its alleged origin: Updating its Japanese distribution with new evidence

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PLOS ONE

The chytrid fungus Batrachochytrium salamandrivorans [Bsal] is causing declines in the amphibian populations. After a decade of mapping the pathogen in Europe, where it is causing dramatic outbreaks, and North America, where its arrival would affect to the salamander’s biodiversity hotspot, little is known about its current status in Asia, from presumably is native. Japan has several species considered as potential carriers, but no regulation is implemented against Bsal spreading. Previous Bsal known presence detected various cases on the Okinawa Island, southwestern Japan. Previous studies on its sister species, B. dendrobatidis presented a high genomic variation in this area and particularly on Cynops ensicauda. Here, we have done the largest monitoring to date in Japan on the Cynops genus, focusing on Okinawa Island and updating its distribution and providing more information to unravel the still unknown origin of Bsal. Interestingly, we have provided revealing facts about different detectability depending on the used molecular techniques and changes in its Japanese distribution. All in all, the Bsal presence in Japan, together with its low variability in the sequenced amplicons, and the lack of apparent mortalities, may indicate that this part of Asia has a high diversity of chytrids.

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Metabolites of Xenorhabdus bacteria are potent candidates for mitigating amphibian chytridiomycosis

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Chytridiomycosis, caused by the chytrid fungus Batrachochytrium dendrobatidis (Bd), has caused extreme losses in amphibian biodiversity. Finding bacteria that produce metabolites with antifungal properties may turn out to be invaluable in the fight against this devastating disease. The entomopathogenic bacteria, Xenorhabdus szentirmaii and X. budapestensis produce secondary metabolites that are effective against a wide range of fungal plant pathogens. To assess whether they may also be effective against Bd, we extracted cell-free culture media (CFCM) from liquid cultures of X. szentirmaii and X. budapestensis and tested their ability to inhibit Bd growth in vitro. As a second step, using juvenile common toads (Bufo bufo) experimentally infected with Bd we also tested the in vivo antifungal efficacy of X. szentirmaii CFCM diluted to 2 and 10% (v/v), while also assessing possible malign side effects on amphibians. Results of the in vitro experiment documented highly effective growth inhibition by CFCMs of both Xenorhabdus species. The in vivo experiment showed that treatment with CFCM of X. szentirmaii applied at a dilution of 10% resulted in infection intensities reduced by ca. 73% compared to controls and to juvenile toads treated with CFCM applied at a dilution of 2%. At the same time, we detected no negative side effects of treatment with CFCM on toad survival and development. Our results clearly support the idea that metabolites of X. szentirmaii, and perhaps of several other Xenorhabdus species as well, may prove highly useful for the treatment of Bd infected amphibians.

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

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

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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.

Arousal Patterns, Fungal Loads, and Wing Damage in a Surviving Population of Little Brown Bats (Myotis lucifugus)

Thesis

Full-text available

Jul 2024

Brooke Daly

Little brown bats (Myotis lucifugus) at Tippy Dam in Michigan have shown resilience to white-nose syndrome (WNS), which is caused by the fungus Pseudogymnoascus destructans. This study evaluated the impact of environment (temperature and moisture), pathogen virulence, and host susceptibility on survival. Host response was assessed using temperature-sensitive radio transmitters (n = 37) and ultraviolet photography (n = 57), while fungal load (n = 56) was evaluated through quantitative polymerase chain reaction (qPCR). High autumn temperatures (>10°C) favored growth of the fungus, while mid-hibernation temperature (3.2°C) was unfavorable. The mean torpor bout length (TBL) was similar to bats uninfected by WNS (16.8 days). Fungal loads were near the limit of detection (4.9 genome copies), and mean infection intensity (percent of wing area fluorescence) was low (0.02–0.14%) and much less when compared to severely affected populations. These findings suggest that some aspect of the environment is inhibiting virulence of the fungus at this unusual site.

Environmental DNA ‐based detection of pathogens in trade and captive settings: Best practices and validation for Batrachochytrium salamandrivorans

Article

Full-text available

Sep 2023
Methods Ecol. Evol.

Detecting pathogens in the live animal trade is critical for tracking and preventing their movement, introduction and spillover into susceptible fauna. However, the scale of the live animal trade makes individually testing animals infeasible for all but the most economically important taxa. For instance, while the fungal pathogen, Batrachochytrium salamandrivorans ( Bsal ), threatens amphibian, particularly caudate diversity, in Europe and the Americas, screening even a fraction of the millions of live amphibians imported into the United States, alone, is impractically laborious and expensive. A promising alternative to individual‐level sampling (e.g. swabbing the skin of salamanders) is to instead collect DNA from the animals' environment (e.g. housing container or water) which allows us to screen a whole group of animals at a time. We used a series of experiments with Bsal ‐spiked water and substrates and experimentally infected rough‐skinned newts ( Taricha granulosa ) to determine which methods yield the most Bsal environmental DNA (eDNA) and evaluate the capacity of these methods to detect Bsal ‐infected animals in conditions found in captive settings and trade. We found that filtering water housing infected animals for even an hour can consistently recover detectable levels of Bsal eDNA, that there is little evidence of Bsal eDNA being clumped in housing containers or swamped or inhibited by dirty housing containers, and that eDNA‐based methods achieves an equivalent or higher chance of detecting Bsal infections in a (virtual) population of co‐housed newts with fewer samples than individual swabs. By sampling the genetic materials accumulated from a whole group of animals, eDNA‐based methods are a powerful means of detecting pathogens, such as Bsal , in shipments and captive populations. These methods bring routine pathogen surveillance into reach in many more contexts and can thus be an important tool in conservation and disease control.

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.

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

A new, yet old, threat to amphibians Globally, populations of amphibians have been severely affected by a disease caused by the fungus Batrachochytrium dendrobatidis . Recently, some European salamander populations were decimated by the emergence of a new, related chytrid fungus, B. salamandrivorans . Martel et al. screened amphibians across continents. This newly emerging threat seems to have originated in Asia and traveled to Europe with salamanders transported as part of the pet trade. Asian salamanders have evolved resistance to the pathogen, but salamanders from other parts of the world are highly susceptible. Science , this issue p. 630

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

Article

Full-text available

Nov 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

Significance Chytridiomycosis has resulted in the serious decline and extinction of >200 species of amphibians worldwide and poses the greatest threat to biodiversity of any known disease. This fungal disease is currently known to be caused by Batrachochytrium dendrobatidis , hitherto the only species within the entire phylum of the Chytridiomycota known to parasitize vertebrate hosts. We describe the discovery of a second highly divergent, chytrid pathogen, Batrachochytrium salamandrivorans sp. nov., that causes lethal skin infections in salamanders, which has resulted in steep declines in salamander populations in northwestern Europe. Our finding provides another explanation for the phenomenon of amphibian biodiversity loss that is emblematic of the current global biodiversity crisis.

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.

Recent Findings of Potentially Lethal Salamander Fungus Batrachochytrium salamandrivorans

Abstract

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