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Successful elimination of a lethal wildlife infectious disease in nature

DOI:10.1098/rsbl.2015.0874
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Jaime Bosch at Biodiversity Research Institute (IMIB)
Jaime Bosch
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Eva Sánchez-Tomé at Centro Nacional de Investigaciones Oncológicas
Eva Sánchez-Tomé
Andrés Fernández-Loras
Andrés Fernández-Loras
Joan A Oliver
Joan A Oliver
Joan A Oliver
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Abstract

Methods to mitigate the impacts of emerging infectious diseases affecting wildlife are urgently needed to combat loss of biodiversity. However, the successful mitigation of wildlife pathogens in situ has rarely occurred. Indeed, most strategies for combating wildlife diseases remain theoretical, despite the wealth of information available for combating infections in livestock and crops. Here, we report the outcome of a 5-year effort to eliminate infection with Batrachochytrium dendrobatidis affecting an island system with a single amphibian host. Our initial efforts to eliminate infection in the larval reservoir using a direct application of an antifungal were successful ex situ but infection returned to previous levels when tadpoles with cleared infections were returned to their natal sites. We subsequently combined antifungal treatment of tadpoles with environmental chemical disinfection. Infection at four of the five pools where infection had previously been recorded was eradicated, and remained so for 2 years post-application.
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Research
Cite this article: Bosch J, Sanchez-Tome
´
E,
Ferna
´
ndez-Loras A, Oliver JA, Fisher MC, Garner
TWJ. 2015 Successful elimination of a lethal
wildlife infectious disease in nature. Biol. Lett.
11: 20150874.
http://dx.doi.org/10.1098/rsbl.2015.0874
Received: 18 October 2015
Accepted: 28 October 2015
Subject Areas:
health and disease and epidemiology
Keywords:
chytridiomycosis, Batrachochytrium
dendrobatidis, mitigation, Alytes muletensis,
Mallorca
Author for correspondence:
Jaime Bosch
e-mail: bosch@mncn.csic.es
†
These authors contributed equally to this
study.
Electronic supplementary material is available
at http://dx.doi.org/10.1098/rsbl.2015.0874 or
via http://rsbl.royalsocietypublishing.org.
Conservation biology
Successful elimination of a lethal wildlife
infectious disease in nature
Jaime Bosch
1,†
, Eva Sanchez-Tome
´
1
, Andre
´
s Ferna
´
ndez-Loras
1
, Joan A. Oliver
2
,
Matthew C. Fisher
3
and Trenton W. J. Garner
4,†
1
Museo Nacional de Ciencias Naturales, CSIC, Jose
´
Gutie
´
rrez Abascal 2, Madrid 28006, Spain
2
Conselleria de Medi Ambient i Mobilitat, Govern de les Illes Balears, Gremi Corredors 10, Polı
´
gon Son Rossinyol,
Palma 07009, Spain
3
Department of Infectious Disease Epidemiology, Imperial College London, St Mary’s Hospital, Norfolk Place,
London W2 1PG, UK
4
Institute of Zoology, Regent’s Park, London NW1 4RY, UK
Methods to mitigate the impacts of emerging infectious diseases affecting
wildlife are urgently needed to combat loss of biodiversity. However, the
successful mitigation of wildlife pathogens in situ has rarely occurred.
Indeed, most strategies for combating wildlife diseases remain theoretical,
despite the wealth of information available for combating infections in live-
stock and crops. Here, we report the outcome of a 5-year effort to eliminate
infection with Batrachochytrium dendrobatidis affecting an island system with
a single amphibian host. Our initial efforts to eliminate infection in the larval
reservoir using a direct application of an antifungal were successful ex situ
but infection returned to previous levels when tadpoles with cleared
infections were returned to their natal sites. We subsequently combined anti-
fungal treatment of tadpoles with environmental chemical disinfection.
Infection at four of the five pools where infection had previously been
recorded was eradicated, and remained so for 2 years post-application.
1. Introduction
Emerging infections are on the increase, incurring extraordinary economic and
health costs and globally degrading our natural capital. In response, several
efforts to eradicate animal pathogens are underway, however with few suc-
cesses reported [1,2]. Research on livestock pathogens predominates and
provides insight as to how pure wildlife pathogens may be combated for host
conservation purposes [1,2]. Delivery of an efficient and practical intervention
is a cornerstone of any scheme to eliminate infectious diseases, and the direct
application of antimicrobials to infected hosts or immunization can be used
effectively to control pathogen replication within a host and to reduce the like-
lihood of transmission to susceptible individuals [3]. However, for these types
of interventions to be effective, control of environmental reservoirs of (re)infec-
tion must also be achieved. Local control of pathogens through the use of
environmental chemical treatments has been effectively used to disinfect
areas where environmental transmission of parasites can occur, but the
impact of chemical treatment on transmission and maintenance of infection
in concert with antimicrobial treatments has rarely been examined [4].
Amphibian chytridiomycosis, a disease predominantly caused by the aquatic
chytrid fungus Batrachochytrium dendrobatidis (Bd) has driven population declines,
local extirpations and species extinctions across five continents [5]. The pathogen
is an extreme generalist, infecting over 700 amphibian species (http://www.bd-
maps.net). Strategies developed to ameliorate the impacts of chytridiomycosis are
predominantly geared towards disease-free maintenance of captive assurance
colonies, and multiple methods have been developed to treat captive amphibians
&
2015 The Author(s) Published by the Royal Society. All rights reserved.
on November 19, 2015http://rsbl.royalsocietypublishing.org/Downloaded from
against infection with Bd [6–8]; however, most attempts at
immunization have failed [9]. The remaining approaches that
hold promise for in situ control include bioaugmentation
with bacteria, direct application of antifungal drugs and
environmental application of anti-Bd chemicals. Although
not without promise, research on the application of bioaug-
mentation so far describes complex interactions between
host, beneficial bacteria, the broader microbiota and pathogen
that are strongly dependent upon environmental context and
amphibian community structure [10,11]. For this reason,
bioaugmentation strategies are unlikely to converge on an
intervention that can be generalized across amphibian commu-
nities and ecosystems. The immediacy of the epizootic of
chytriomycosis calls for an intervention that can be applied
across systems, so we chose to explore direct application of
antifungal drugs to infected hosts and environmental appli-
cation of chemicals as strategies to eliminate Bd from a
simple, single host system [12].
2. Material and methods
Biannual surveys at five permanent ponds (3 Torrent des Fer-
rerets, 2 Coco
´
de sa Bova; Mallorca, Spain) were undertaken
from 2008 and are ongoing. We sampled Mallorcan midwife
toad (Alytes muletensis) tadpoles, as terrestrial stages are rarely
captured as they take refuge in inaccessible locations. Tadpoles
of this and other Alytes sp. are recognized as reservoirs of infec-
tion [13,14]. To sample, we swabbed tadpole mouthparts
following established protocols [12,13]. All ponds affected by
chytridiomycosis on the island were included in the study and
none was left as untreated controls owing to conservation
requirements. However, chemical disinfection efforts at Torrent
de Ferrerets preceded those at Coco
´
de sa Bova, affording us
the opportunity to compare across sites.
Swabs were processed according to standard extraction and
quantitative PCR (qPCR) methods [15] in duplicate and run
against negative controls and positive controls (0.1, 1, 10 and
100 zoospore genomic equivalents, GE).
For antifungal treatments, tadpoles were collected and trans-
ported in plastic bottles containing pond water. We used air
pumps and tubes with aeration stones to ensure tadpole survival
during the outward hikes. Tadpoles were then transported to the
laboratory and kept in several cooled, glass aquaria. All tadpoles
were bathed daily for 7 days in aged tapwater containing
1.0 mg l
21
itraconazole (Sporanox, Janssen-Cilag Inc.) and
returned to aquaria after each treatment. Aquaria water was
replaced every day during the 7 days treatment. After treatment,
tadpoles were returned to the collection sites by helicopter, either
immediately if ponds were not drained or after ponds were
refilled by autumn rain. In these cases, subsets of 40 tadpoles
from each aquarium were swab-sampled 15 days post-treatment.
Environmental disinfection was done using Virkon S
(DuPont Inc.) at 1% final concentration and a single application
applied ad libitum to the environment. The disinfectant was lib-
erally applied to all rock, gravel, crevice and vegetated areas that
surrounded the immediate environs of each breeding site.
3. Results
W e initially attempted mitigation by trea ting in 2009 A. muletensis
tadpoles inhabiting two permanent pond sites in one of the
two infected drainages, Coco
´
de sa Bova (electronic sup-
plementary material, figure S1), with the antifungal
itraconazole. We used a treatment protocol previously
shown to eliminate infection in tadpoles [7]. Treatments
were applied ex situ, and prior to post-treatment release the
two ponds were completely drained of water and naturally
dried by the arid environment that typifies Mallorca. We
had previously determined that Bd is absent from the other
two ephemeral water bodies in this drainage, and environ-
mental Bd is not thought to persist during periods of
drying [16]. The two ponds naturally refilled during the
autumn rainy season. At no point during this prolonged
period of captivity did we detect any evidence of infection
in the treated tadpoles. The following spring, qPCR analysis
showed that all treated animals had contracted infections not
significantly different from what had been recorded at the
location before treatment [17] (figure 1). Repeating the proto-
col in the spring of 2012, this time without draining the
breeding sites, and with tadpole release only 7 days after
treatment, was again not associated with reduction in the
prevalence of infection or reduced burdens of infection in
the following spring (figure 1).
In contrast, at three breeding sites used by the species in the
second drainage, Torrent des Ferrerets (electronic supplemen-
tary mate rial, figure S2), we could not detect infection in any
animals sampled in 2013 after trea tment of tadpoles and wha t-
ever terrestrial A. muletensis life stages we could capture with
itra conazole, draining the sites and then treating the environ-
ment with Virkon S (electronic supplementary material, figures
S3 and S4; figure 1). Replication of this pr otocol a t Coco
´
de sa
Bova in 2013 and applica tion of Virkon S solution to the rock cre-
vices located around the ponds where metamorphosed
A. muletensis reside again cleared infection in the larger popu-
lation of tadpoles resident in the larger pond at this location.
Residual infection was detected in tadpoles occupying the smal-
ler permanent pond site. Data fr om samples take n at Torrent des
Ferrerets 2 y ears a ft er chemical disinfection showed tha t the
effect of environmental application of Virkon S twinned with
itra conazole treatment of tadpoles carried over across years, as
again no evidence of infection was detected in 2014 (figure 1).
4. Discussion and conclusion
W e cannot sa y with certainty why dir ect trea tm ent of tadpoles
with antifungals without environmental disinfection failed
to resolve infection at Coco
´
de sa Bova, but the most likely
explana tion is that infection reinvaded tadpoles from post-
metamorphic animals that we could not a ccess in their
terres trial refuges. We do occasionally discover corpses of juven-
iles exhibiting a str ong molecular signal of infection. Lik e other
amphibian species, Alytes spp. tadpoles scavenge from corpses,
and this process is presumed to be a factor in transmission of Bd
from corpses to tadpoles in another species [18,19]. Irrespectiv e of
this, our application of Virko n S at Torr ent des F err er ets pro vided
proof-of-principle that environmental application of fungicides
and other chemical treatments may be a better approa ch when
combined with antimicrobial trea tment of infected hosts. This
initial conclusion was reinfor ced when we recapitulated our
result by clearing infection in C oco
´
de sa Bova the following
year. In our case, combining chemical disinfection twinned
with antifungal treatment of tadpoles pro v ed the better stra tegy,
eliminating infection and prev enting spill-back over the short
term at four of the five pools where we attempted mitigation.
The development of disinfection strategies alone cannot
eliminate the threat of chytridiomycosis, as evidence
rsbl.royalsocietypublishing.org Biol. Lett. 11: 20150874
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continues to accumulate that lethal amphibian-associated
chytrid fungi are frequently being introduced into Europe
and beyond [12,20]. Clearing site-level infection is no guaran-
tee against pathogen reintroduction or the introduction of
novel pathogens. However, to cope with the existing, recur-
ring and future threats of chytridiomycosis, rapid response
strategies require cheap, simple and transferrable methods
for mitigating infection that can be employed as soon as the
threat has been identified. We acknowledge that Virkon S is
a controversial chemical to use environmentally and our
use of it was driven by the urgency of midwife decline on
Mallorca [21]. Virkon S is only one of several chemical treat-
ments known to have antifungal properties against chytrid
fungi [22,23] and antifungal treatments do not require exten-
sive investment in time and effort. We argue that research
informing efforts to combat chytridiomycosis should include
in-depth investigations of the impact of antifungals and anti-
Bd chemicals on amphibian health without discarding
attempts to develop immunization and other methods of dis-
ease control. Research on the application of these chemicals
for control of wildlife diseases must also include investigation
of the potential impacts of chemical application to other bio-
diversity, the environment and associated ecosystem services.
Ethics.
The work was carried out under the Govern de les Illes
Balears’s permit no. CEP 43/2015.
Data accessibility. Data are available in the electronic supplementary
material.
Authors’ contributions. J.B., T.W.J.G. and M.C.F. designed and wrote the
paper, with contributions from E.S.-T. Data were collected and/
or analysed by E.S.-T., A.F.-L. and J.A.O; all authors provided
intellectual input and edited/approved the manuscript.
Competing interests. We declare we have no competing interests.
Funding. This work was funded by Fundacio
´
n General CSIC, Banco
Santander and BiodivERsA project RACE.
Acknowledgements. We thank S. Pinya, X. Manzano, C. Serrano,
A. Dı
´
az-Guerra, E. M. Albert, S. F. Walker, D. Daversa,
S. Ferna
´
ndez-Beaskoetxea, J. Vo
¨
ro
¨
s, B. R. Schmidt, B. Tapley and
J. Bielby for field assistance, the people working at Paratge Natural
de la Serra de Tramuntana and Conselleria de Medi Ambient
(especially J. Mayol and E. Moragues), and the owner of the Mossa
property for field site access.
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Article
  • Jan 2022
By the late 1980s, widespread dramatic declines in amphibian populations were causing alarm. The culprit was identified as Batrachochytrium dendrobatidis (Bd), a chytrid fungus that infects the skin of various amphibian hosts, particularly anurans (frogs), and the first example of a chytridiomycete parasitising vertebrates. The disease, chytridiomycosis, has spread globally and is linked to the decline and extinction of many amphibian species. This review summarises the discovery of Bd, its emergence as a panzootic pathogen, and some current mitigation strategies to conserve amphibians.
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... Although available mitigation strategies in-situ are scarce and complex (Pabijan et al. 2020), our findings indicate the urgent need to initiate conservation measures to prevent the population collapse, increasing the opportunity for this adaptation. For example, Hudson et al. (2016) found that in-situ itraconazole treatments of adult amphibians increased their probability of survival, and modified strategies from Bosch et al. (2015) using chemical mitigation at the pond-scale are now being tested at the study National Park. At present, though, this population of spiny common toads has an uncertain future, even when the species has not been considered until now to be threaten by chytridiomycosis (sensu Scheele et al. 2019). ...
Amphibian survival compromised by long-term effects of chytrid fungus
Article
Full-text available
Chytridiomycosis, the disease caused by the fungal pathogen Batrachochytrium dendrobatidis (Bd), has been unambiguously implicated in the decline of amphibian populations worldwide. However, the impact of this devastating infectious disease can be difficult to gauge without empirical data on the population-level effects of Bd. Often, assessments of the amphibian chytridiomycosis panzootic are based primarily on expert opinions; as a result, declines in tropical areas are promptly attributed to Bd while its impact on temperate species not suffering from adult mass mortalities is frequently overlooked. Here, we investigated the survival probability in an amphibian species from a temperate area that until now has not been considered to be severely impacted by the disease. Specifically, we related individual survival to Bd infection status using long-term capture-mark-recapture data of male spiny common toads (Bufo spinosus) in Sierra de Guadarrama National Park in central Spain. Even though the study population has demonstrated potential for adaptation to Bd and die-offs of adult individuals have not been recorded, our results clearly indicated that the probability of survival was lower for Bd-positive individuals. Moreover, the probability of becoming Bd-positive was higher than the probability of clearance, driving the population to a slow but certain decline. These results are consistent with other indicators of a negative population trend and suggest that the impact of Bd on temperate species of less concern may be greater than previously thought.
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... Although small in number, PIs conducted to date have involved a range of species, pathogens, regions and purposes and provide an informative evidence base to draw from ( Figure 1). Data from published PIs demonstrate their worth for disease management across diverse scenarios; for example, oral praziquantel baiting of red foxes Vulpes vulpes reduced Echinococcus multilocularis egg contamination among urban areas in Switzerland (Hegglin et al., 2003); topical Pseudomonas fluorescens application protected Myotis lucifugus bats from white nose syndrome (WNS) associated mortality in North America (Hoyt et al., 2019); and, itraconazole treatment of Alytes muletensis tadpoles and environmental disinfection eradicated Batrachochytrium dendrobatidis (Bd) from ponds in Spain (Bosch et al., 2015). Lessons learned can also inform future improvements (Langwig et al., 2015). ...
Time to consider pharmacological interventions against infectious disease in wildlife
Article
Full-text available
  • Nov 2022
Interventions against infectious disease in wildlife are increasingly necessary but remain problematic. Dissimilar to public and domestic animal health, pharmacological interventions (PIs) are rarely used against disease in wildlife populations. However, drugs can combat a range of pathogen‐types while aligning with positive ethical, epidemiological, evolutionary, and socio‐economic outcomes. We discuss how recent conceptual and technological advances could overcome barriers, improve safety, and begin a new era of contemporary wildlife management that embraces PIs. We then provide a framework that supports objective comparison of intervention suitability, including PIs. We find numerous directions for PI optimisation through innovation and transdisciplinary collaboration, and demonstrate the utility of the framework for judging the appropriateness of a PI. Synthesis and applications: Interrogating how and when pharmacological interventions can be used to greatest effect reduces risks and improves outcomes for wildlife, while empowering decision makers to draw from the full suite of intervention methods to find the most appropriate disease management solutions.
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... Strategies for mitigating the impact of chytridiomycosis on wild amphibian populations would also be valuable. Diverse avenues have been explored, such as antifungal treatment of tadpoles coupled with environmental disinfection (Bosch et al. 2015), and probiotic therapy through bioaugmentation of microbes that confer defense against chytrids (Bletz et al. 2013;Kearns et al. 2017;Woodhams et al. 2020); but the broad applicability and scalability of these methods have yet to be determined. Additional strategies discussed by the group included biological control using mycoviruses, which has been applied against the fungal agent responsible for chestnut blight (Rigling and Prospero 2018), and the introduction of nonpathogenic chytrid lineages to outcompete virulent lineages. ...
The future of fungi: threats and opportunities
Article
Full-text available
  • Sep 2022
The fungal kingdom represents an extraordinary diversity of organisms with profound impacts across animal, plant, and ecosystem health. Fungi simultaneously support life, by forming beneficial symbioses with plants and producing life-saving medicines, and bring death, by causing devastating diseases in humans, plants, and animals. With climate change, increased antimicrobial resistance, global trade, environmental degradation, and novel viruses altering the impact of fungi on health and disease, developing new approaches is now more crucial than ever to combat the threats posed by fungi and to harness their extraordinary potential for applications in human health, food supply, and environmental remediation. To address this aim, the Canadian Institute for Advanced Research (CIFAR) and the Burroughs Wellcome Fund convened a workshop to unite leading experts on fungal biology from academia and industry to strategize innovative solutions to global challenges and fungal threats. This report provides recommendations to accelerate fungal research and highlights the major research advances and ideas discussed at the meeting pertaining to 5 major topics: (1) Connections between fungi and climate change and ways to avert climate catastrophe; (2) Fungal threats to humans and ways to mitigate them; (3) Fungal threats to agriculture and food security and approaches to ensure a robust global food supply; (4) Fungal threats to animals and approaches to avoid species collapse and extinction; and (5) Opportunities presented by the fungal kingdom, including novel medicines and enzymes.
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... It is also possible that Virkon ® Aquatic could be used to treat the environment. In an isolated aquatic system in Spain, Bd was eradicated by treating tadpoles with itraconazole and the environment with 1% Virkon ® S (Syndel, Ferndale, WA, USA) [80]. However, similar to plant-derived fungicides, the toxicity of Virkon ® Aquatic on amphibians and other aquatic organisms needs to be evaluated [81,82]. ...
Efficacy of Plant-Derived Fungicides at Inhibiting Batrachochytrium salamandrivorans Growth
Article
Full-text available
The emerging fungal amphibian pathogen, Batrachochytrium salamandrivorans (Bsal), is currently spreading across Europe and given its estimated invasion potential, has the capacity to decimate salamander populations worldwide. Fungicides are a promising in situ management strategy for Bsal due to their ability to treat the environment and infected individuals. However, antifungal drugs or pesticides could adversely affect the environment and non-target hosts, thus identifying safe, effective candidate fungicides for in situ treatment is needed. Here, we estimated the inhibitory fungicidal efficacy of five plant-derived fungicides (thymol, curcumin, allicin, 6-gingerol, and Pond Pimafix®) and one chemical fungicide (Virkon® Aquatic) against Bsal zoospores in vitro. We used a broth microdilution method in 48-well plates to test the efficacy of six concentrations per fungicide on Bsal zoospore viability. Following plate incubation, we performed cell viability assays and agar plate growth trials to estimate the minimum inhibitory concentration (MIC) and minimum fungicidal concentration (MFC) of each fungicide. All six fungicides exhibited inhibitory and fungicidal effects against Bsal growth, with estimated MIC concentrations ranging from 60 to 0.156 μg/mL for the different compounds. Allicin showed the greatest efficacy (i.e., lowest MIC and MFC) against Bsal zoospores followed by curcumin, Pond Pimafix®, thymol, 6-gingerol, and Virkon® Aquatic, respectively. Our results provide evidence that plant-derived fungicides are effective at inhibiting and killing Bsal zoospores in vitro and may be useful for in situ treatment. Additional studies are needed to estimate the efficacy of these fungicides at inactivating Bsal in the environment and treating Bsal-infected amphibians.
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Impact of home improvements and health education on the transmission of Trypanosoma cruzi Chagas in a rural area of western Mexico
Article
Chagas disease is one of the most important vector-borne diseases in Latin America. Instituting home improvement preventive measures and increasing health education contribute to successful control of the triatomine insect vector. The impact of home and road improvements and health education upon the inhabitants of 37 human dwellings in three small towns in western Mexico were studied. Initially, few house roofs were made of concrete and few walls were cement-lined. Almost all houses initially lacked metal window screens and none used barbed wire fences. One year after the intervention, all of these measures were more common, and almost 100% of houses continued to use window screens and barbed wire fences ten years post-intervention. By ten years post-intervention, >75% of houses had cement-lined walls. Initially, 24.3% of human dwellings were infested with Triatoma longipennis Usinger; at one and ten years post-intervention, only 2.7% of dwellings were infested. The abundance of peridomestic opossums decreased after intervention and remained low ten years later. Approximately 10% of dogs were infected in both surveys. Human infections decreased from 2.98% to zero by 13 years post-intervention. Implementation of these intervention measures led to the successful control of Trypanosoma cruzi Chagas transmission in these towns.
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Reducing environmentally mediated transmission to moderate impacts of an emerging wildlife disease
Preprint
  • Jul 2022
Emerging infectious diseases are a serious threat to wildlife communities, and the ability of pathogens to survive in the environment can exacerbate disease impacts on hosts and increase the likelihood of species extinction. Targeted removal or control of these environmental reservoirs could provide an effective mitigation strategy for reducing disease impacts but is rarely used in wildlife disease control. We examined the effectiveness of managing environmental transmission to reduce impacts of an emerging infectious disease of bats, white-nose syndrome. We used a chemical disinfectant, chlorine dioxide (ClO 2 ), to experimentally reduce Pseudogymnoascus destructans , the fungal pathogen causing WNS, in the environment. We conducted laboratory experiments followed by three years of field trials at four abandoned mines to determine whether ClO 2 could effectively reduce P. destructans in the environment, reduce host infection, and limit population impacts. ClO 2 was effective at killing P. destructans in vitro across a range of concentrations. In field settings, higher concentrations of ClO 2 treatment sufficiently reduced viable P. destructans conidia in the environment. The reduction in the environmental reservoir at treatment sites resulted in lower fungal loads on bats compared to untreated control populations. Survival following treatment was higher in little brown bats ( Myotis lucifugus ), and trended higher for tricolored bats ( Perimyotis subflavus ) compared to untreated sites. These findings support the management of environmental reservoirs as an effective control strategy for wildlife disease and provide a valuable tool for ongoing conservation efforts. More broadly, these results highlight how the intensity of environmental reservoirs can have cascading impacts on host infection and population declines.
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Recent introduction of a chytrid fungus endangers Western Palearctic salamanders
Article
Full-text available
  • Oct 2014
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.
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Recent introduction of a chytrid fungus endangers Western Palearctic salamanders
Article
Full-text available
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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Recent introduction of a chytrid fungus endangers Western Palearctic salamanders
Article
Full-text available
  • Oct 2014
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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Impact of Plant Cover on Fitness and Behavioural Traits of Captive Red-Eyed Tree Frogs (Agalychnis callidryas)
Article
Full-text available
Despite the importance of ex situ conservation programmes as highlighted in the Amphibian Conservation Action Plan, there are few empirical studies that examine the influence of captive conditions on the fitness of amphibians, even for basic components of enclosure design such as cover provision. Maintaining the fitness of captive amphibian populations is essential to the success of ex situ conservation projects. Here we examined the impact of plant cover on measures of fitness and behaviour in captive red-eyed tree frogs (Agalychnis callidryas). We found significant effects of plant provision on body size, growth rates and cutaneous bacterial communities that together demonstrate a compelling fitness benefit from cover provision. We also demonstrate a strong behavioural preference for planted rather than non-planted areas. We also assessed the impact of plant provision on the abiotic environment in the enclosure as a potential driver of these behavioural and fitness effects. Together this data provides valuable information regarding enclosure design for a non-model amphibian species and has implications for amphibian populations maintained in captivity for conservation breeding programmes and research.
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Context-dependent amphibian host population response to an invading pathogen
Article
Full-text available
Amphibian chytridiomycosis, caused by the chytrid fungus Batrachochytrium dendrobatidis (Bd), is an emerging infectious disease that widely threatens amphibian biodiversity. However, population-level outcomes following the introduction of the pathogen are highly context dependent and are mediated by a broad suite of biotic and abiotic variables. Here, we examine the effect of the introduction of Bd on native island populations of the IUCN red-listed amphibian species Alytes muletensis, the Mallorcan midwife toad. We show that the outcome of pathogen introduction is not only dependent on biotic factors, but also environmental factors that vary across local scales. Our experimental infections confirm that the genotype of Bd occurring on Mallorca is hypovirulent in A. muletensis when compared against the lineage found occurring on mainland Iberia. Long-term population data shows that A. muletensis populations on the island are increasing overall, but trends in highly infected populations are conflicting. We use mathematical models and field data to demonstrate that this divergence in population response to infection can be explained by local environmental differences between infected sites, whereas pathogen genetics, host genetics, and intrinsic epidemiological dynamics driven by fungal load are less likely to be the cause of these differing population trajectories. Our results illustrate the need to take into account the appropriate environmental scale and context when assessing the risk that an emerging pathogen presents to a naı¨venaı¨ve population or species.
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Assessing Risk and Guidance on Monitoring of Batrachochytrium dendrobatidis in Europe through Identification of Taxonomic Selectivity of Infection
Article
Full-text available
Amphibians are globally threatened, but not all species are affected equally by different threatening processes. This is true for the threat posed by the chytridiomycete fungus (Batrachochytrium dendrobatidis). We compiled a European data set for B. dendrobatidis to analyze the trends of infection in European amphibians. The risk of infection was not randomly distributed geographically or taxonomically across Europe. Within countries with different prevalence, infection was nonrandom in certain amphibian taxa. Brown frogs of the genus Rana were unlikely to be infected, whereas frogs in the families Alytidae and Bombinatoridae were significantly more likely to be infected than predicted by chance. Frogs in the 2 families susceptible to B. dendrobatidis should form the core of attempts to develop spatial surveillance studies of chytridiomycosis in Europe. Ideally, surveys for B. dendrobatidis should be augmented by sampling the widespread genus Pelophylax because this taxon exhibits geographically inconsistent overinfection with B. dendrobatidis and surveillance of it may facilitate recognition of factors causing spatial variability of infection intensity. Several European amphibian taxa were not represented in our data set; however, surveillance of unsampled species should also occur when warranted. Evaluación de Riesgo y Orientación para el Monitoreo de Batrachochytrium dendrobatidis en Europa Mediante la Identificación de la Selectividad Taxonómica de la Infección.
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Interventions for Reducing Extinction Risk in Chytridiomycosis-Threatened Amphibians: Reducing Extinction Risk in Amphibians
Article
  • Jun 2014
Wildlife diseases pose an increasing threat to biodiversity and are a major management challenge. A striking example of this threat is the emergence of chytridiomycosis. Despite diagnosis of chytridiomycosis as an important driver of global amphibian declines 15 years ago, researchers have yet to devise effective large-scale management responses other than biosecurity measures to mitigate disease spread and the establishment of disease-free captive assurance colonies prior to or during disease outbreaks. We examined the development of management actions that can be implemented after an epidemic in surviving populations. We developed a conceptual framework with clear interventions to guide experimental management and applied research so that further extinctions of amphibian species threatened by chytridiomycosis might be prevented. Within our framework, there are 2 management approaches: reducing Batrachochytrium dendrobatidis (the fungus that causes chytridiomycosis) in the environment or on amphibians and increasing the capacity of populations to persist despite increased mortality from disease. The latter approach emphasizes that mitigation does not necessarily need to focus on reducing disease-associated mortality. We propose promising management actions that can be implemented and tested based on current knowledge and that include habitat manipulation, antifungal treatments, animal translocation, bioaugmentation, head starting, and selection for resistance. Case studies where these strategies are being implemented will demonstrate their potential to save critically endangered species.
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The amphibian skin-associated microbiome across species, space and life history stages
Article
Skin-associated bacteria of amphibians are increasingly recognized for their role in defence against pathogens, yet we have little understanding of their basic ecology. Here, we use high-throughput 16S rRNA gene sequencing to examine the host and environmental influences on the skin microbiota of the cohabiting amphibian species Anaxyrus boreas, Pseudacris regilla, Taricha torosa and Lithobates catesbeianus from the Central Valley in California. We also studied populations of Rana cascadae over a large geographic range in the Klamath Mountain range of Northern California, and across developmental stages within a single site. Dominant bacterial phylotypes on amphibian skin included taxa from Bacteroidetes, Gammaproteobacteria, Alphaproteobacteria, Firmicutes, Sphingobacteria and Actinobacteria. Amphibian species identity was the strongest predictor of microbial community composition. Secondarily, within a given amphibian species, wetland site explained significant variation. Amphibian-associated microbiota differed systematically from microbial assemblages in their environments. Rana cascadae tadpoles have skin bacterial communities distinct from postmetamorphic conspecifics, indicating a strong developmental shift in the skin microbes following metamorphosis. Establishing patterns observed in the skin microbiota of wild amphibians and environmental factors that underlie them is necessary to understand skin symbiont community assembly, and ultimately, the role skin microbiota play in the extended host phenotype including disease resistance.
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Context-dependent amphibian host population response to an invading pathogen
Article
Amphibian chytridiomycosis, caused by the chytrid fungus Batrachochytrium dendrobatidis (Bd), is an emerging infectious disease that widely threatens amphibian biodiversity. However, population-level outcomes following the introduction of the pathogen are highly context dependent and are mediated by a broad suite of biotic and abiotic variables. Here, we examine the effect of the introduction of Bd on native island populations of the IUCN red-listed amphibian species Alytes muletensis, the Mallorcan midwife toad. We show that the outcome of pathogen introduction is not only dependent on biotic factors, but is also dependent on environmental factors that vary across local scales. Our experimental infections confirm that the genotype of Bd occurring on Mallorca is hypovirulent in A. muletensis when compared against the lineage found occurring on mainland Iberia. Long-term population data show that A. muletensis populations on the island are increasing overall, but trends in highly infected populations are conflicting. We use mathematical models and field data to demonstrate that this divergence in population response to infection can be explained by local environmental differences between infected sites, whereas pathogen genetics, host genetics, and intrinsic epidemiological dynamics driven by fungal load are less likely to be the cause of these differing population trajectories. Our results illustrate the need to take into account the appropriate environmental scale and context when assessing the risk that an emerging pathogen presents to a naive population or species.
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