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Abstract

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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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
... In 2018, a disjunct Bsal outbreak was detected in the Iberian Peninsula in northeastern Spain, nearby to Europe's most threatened newt species, the Montseny brook newt (Calotriton arnoldi) [12]. Two other recent reports have reported positive qPCR results in north central Spain [13,14]. With seven genera, ten species and a high number of smallrange endemic lineages, the Iberian Peninsula is a hotspot of diversification of the family Salamandridae. ...
... Between 2015-2021, we opportunistically sampled 66 populations of 10 Iberian urodele species, with a total of 1395 individuals sampled (Table S1). Recent reports of Bsal-positive qPCRs from Asturias [13,14] resulted in more intensive sampling efforts in this region, where we resampled two localities previously reported as positive. The vast majority of samples derived from surveys of live urodeles, with 21 samples from dead animals. ...
... For all species, five or six adult specimens were inoculated with 10 3 zoospores of the Bsal type strain AMFP13/1 using an established protocol [11]. In addition, given recent positive qPCR results from the Palmate newt (Lissotriton helveticus) in northern Spain [13,14], we also infected 10 captive bred palmate newts with two additional Bsal isolates (isolates AMFP14/1 and AMFP15/1; 5 animals per isolate) to study infection dynamics in this species. An earlier infection trial has indicated that L. helveticus has low susceptibly to Bsal infection [11]. ...
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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.
... Since 2017, we have been monitoring by swabbing several caudate populations in the northern part of Spain, which have been positive for Bsal [27] or see Table 1. To collect samples for the purposes of this research, we swabbed amphibians and filtered water from the habitat where the animals were collected. ...
... To collect samples for the purposes of this research, we swabbed amphibians and filtered water from the habitat where the animals were collected. We tested the filters in the Bsal-positive localities mentioned in [27], and also in four other localities. We also sampled several Czech localities, near Staré Město, Zlín Region and Sokolov, Karlovy Vary region, where we collected eDNA samples for an evaluation of the presence of Bd. ...
... Our results have confirmed Bsal in previous positive localities from [27] and we have announced four new positive sites in Spain. Our proposed eDNA collection procedure also detects Bd. ...
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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.
... Further surveillance in wild populations of caudates has extended our knowledge of Bsal presence to Belgium and Germany, mostly in relatively adjacent areas (up to tens of kilometers) from the first disease outbreak , Stegen et al. 2017, Lötters et al. 2018. Recently, the fungus was detected in northern Spain, more than 1000 km from the area where Bsal was initially detected (Lastra González et al. 2019. Most recently, the pathogen was found in southern Germany (Bavaria) (Schmeller et al. 2020, Thein et al. 2020. ...
... Because of the lack of Bsal presence in our set of samples, no statistics were used for estimating Bsal prevalence. While it certainly is possible to calculate Bayesian credible intervals even for populations with no infection (for example, see Lastra González et al. 2019), the probability of us missing an infected individual is low. In amphibian collections, it is reasonable to assume that, due to the specific conditions within which individuals are kept (e.g. ...
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... Mycotic diseases affect multiple taxa including plants, mammals, fish, corals, and amphibians, among others (Sutherland et al., 2014). For instance, Pseudogymnoascus destructans causes white-nose syndrome (WNS) in bats Gargas et al., 2009), Batrachochytrium dendrobatidis (Bd) and B. salamandrivorans (Bsal) cause chytridiomycosis in frogs, salamanders, newts, and caecilians Chandler et al., 2019;Lastra Gonzalez et al., 2019), Aspergillus sydowii has been associated with disease in soft corals (Fisher et al., 2012), and Nosema spp. affect bees (Fisher et al., 2012). ...
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... In contrast, we did not find any individuals infected with the emerging amphibian pathogen Bsal. This is in line with a previous screening for Bsal, which did not detect the pathogen in any of approximately 300 studied salamanders from Poland (Lastra González et al. 2019). The ubiquity of Bd (and to a lesser extent Rv) suggests that recent amphibian declines in this region (Pabijan & Ogielska 2019) may not only be due to widespread habitat conversion, but may be partially attributable to previous or ongoing disease outbreaks that have gone unrecognized. ...
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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.
... Bsal was isolated in 2012 from a moribund European fire salamander (Salamandra salamandra) from a population in Bunderbos, the Netherlands, that had been declining since 2010 . Since its isolation, Bsal has been detected in captive and wild populations in six European countries (Fitzpatrick, Pasmans, Martel, & Cunningham, 2018;González et al., 2019;Sabino Pinto et al., 2015;Spitzen-van der Sluijs et al., 2016;Stegen et al., 2017). Bsal's emergence has had negative impacts on susceptible host species. ...
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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.
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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.
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Full-text available
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.
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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.
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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.
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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.
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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.
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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.
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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.
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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.
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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.
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