Introduction
Batrachochytrium salamandrivorans (Bsal) is an emerging fungal pathogen that has caused
recent die-offs of native salamanders in Europe and is known to be lethal to at least
some North American species in laboratory trials [1]. Bsal appears to have originated
in Asia, and may have been introduced by humans into wild populations in Europe through
commercial trade of amphibians [1]. Since the first outbreaks of Bsal in the Netherlands,
it has been the etiologic agent of mortality events in Belgium (wild) and Germany
(captivity), and was recently found in imported salamanders in the United Kingdom
[1–4]. Substantial concern has been raised about the associated risk of Bsal to native
salamanders in North America [5]. Herein, we review what policy actions are occurring
in North America and elsewhere, and call for creation of a North American Bsal Strategic
Plan.
How Does Bsal Kill Its Host and Differ from B. dendrobatidis (Bd)?
Bsal parasitizes the epidermal cells of salamanders (order Urodela), causing skin
ulcerations with significant degradation of the epidermis, which is sometimes visible
macroscopically (Fig 1) and very obvious histologically (Fig 2). Loss of epidermal
integrity with subsequent impairment of vital skin functions (e.g., electrolyte homeostasis,
fluid balance, gas exchange, barrier against opportunistic pathogens) leads to death
in susceptible species within two to three weeks after exposure [1,2]. Death is generally
preceded by a brief episode of abnormal body posture and behavior. Species susceptibility
correlates with the ability of Bsal to invade the epidermis, and is species- and developmental-stage–dependent
[6]. Whereas some species succumb quickly to chytridiomycosis after Bsal infection,
others have been shown to tolerate and eventually clear infection, suggesting the
development of acquired immunity [1]. Although experimental exposure to Bsal zoospores
leads to mortality in a wide range of salamander species, mortality events in wild
salamander populations have been reported only in a single species (fire salamander,
Salamandra salamandra). Mortality events in other species may have gone unnoticed
due to the secretive nature of salamanders.
10.1371/journal.ppat.1005251.g001
Fig 1
Fire salamander (Salamandra salamandra) covered with Bsal ulcerations, which are visible
as black spots (photo credit = F. Pasmans).
10.1371/journal.ppat.1005251.g002
Fig 2
Bsal infection in the skin of a fire salamander (Salamandra salamandra), characterized
by extensive epidermal necrosis, presence of high numbers of intra-epithelial colonial
chytrid thalli, and loss of epithelial integrity (H&E staining, scale bar = 50 μm;
photo credit = A. Martel and F. Pasmans).
Like its sister species, B. dendrobatidis (Bd), Bsal infects the epidermal cells of
amphibian skin; however, Bd appears to be more pathogenic to frogs (order Anura),
whereas Bsal seems to be more pathogenic to salamanders. The clinical signs of infection
for both Bd and Bsal are excessive skin shedding, lethargy, anorexia, abnormal posture,
and death. However, the lesions produced by each fungus are different. While Bd mainly
causes epidermal hyperplasia and hyperkeratosis [7,8], but only rarely skin ulcerations
[9], Bsal typically causes skin ulcerations with significant destruction of the epidermis.
Modes of Bsal transmission are unknown, but probably include direct contact between
individuals and exposure to contaminated water or soil, similar to Bd [10].
Why Do We Care?
North America is a global hotspot for salamander biodiversity, accounting for about
50% of species worldwide [11]. In particular, Mexico and the Appalachian Mountains
are collectively home to more than 100 species of lungless salamanders (family Plethodontidae).
Both of these areas, along with the Pacific Northwest, are known for their regionally
endemic and relictual salamander species. In North American forests, the biomass of
salamanders can exceed the biomass of all other vertebrate species [12,13]. Salamanders
are centrally nested in aquatic and terrestrial food webs, as predators of various
insects (including hosts of human pathogens [14]) and prey for higher-order predators
such as reptiles, birds, and mammals (e.g., [15]). Indeed, salamanders are vital components
of ecosystems, significantly affecting various ecological processes, energy flow,
and trophic-level interactions, which ultimately contributes to environmental quality.
Salamanders not only perform significant ecological functions, but also provide a
variety of ecosystem services for human benefit [16]. In addition to their aesthetic
value and use as pets and educational tools, salamanders serve as metrics of biotic
integrity and play a role in carbon cycling [13,17,18], which helps buffer climate
change. Additionally, many salamander species have biomedical value, with the ability
to regenerate limbs [19] and skin that produces chemicals with antibiotic, anesthetic,
and analgesic properties [20]. Salamanders also are used as models to understand animal
physiology [21]. Due to its apparent pathogenicity to many salamander taxa, if Bsal
is introduced into North America, it could have serious ecological and economic impacts,
including potential extinction of species. Salamander communities in the southern
Appalachian Mountains, southeastern and northwestern United States, southwestern Canada,
and central Mexico may be at greatest risk [11], yet salamanders in any location could
be vulnerable to Bsal, and increased awareness overall is warranted.
Past Lessons and Initial Responses
Introduced pathogens have significant impact on native wildlife. The related amphibian
fungal pathogen, Bd, has had dire effects on its hosts worldwide [22]. The pathogen
that causes white-nose syndrome, Pseudogymnoascus destructans, recently introduced
from Europe to North America, has decimated many bat populations [23]. The chestnut
blight fungus, Cryphonectria parasitica, introduced to North America from Asia in
the early 1900s, caused the functional extinction of the American chestnut tree (Castanea
dentata), forever changing eastern North American forest ecosystems. As with many
invasive species, what we have learned from the emergence of these fungal pathogens
in North America is that preventing introduction is the best way to protect populations,
and if introduction occurs, rapid response is essential [24].
Recognizing the threat of Bsal to salamander species across the globe, a coalition
of organizations and individuals submitted letters to the US Fish and Wildlife Service
(USFWS) requesting that the agency take emergency action to prevent the spread of
Bsal into the US. Current USFWS regulations allow them to impose import restrictions
on animal species that may be injurious to native species, but not microorganisms
such as pathogens. Additionally, although animal health certificates are required
by the US Department of Agriculture for imported domesticated animals that are hosts
of pathogens listed as notifiable by the World Organisation for Animal Health (OIE),
evidence of pathogen-free shipments is not required for imported wildlife. These policy
gaps have created challenges in efforts to reduce the risk of Bsal introduction into
the US. Currently, the USFWS, working under the authority of the Lacey Act (18 U.S.C.
42), is considering listing salamander species that could be hosts of Bsal, as injurious.
Salamanders represented 5.5% of the amphibians imported into the US from 2004 to 2014,
and 95% of those belong to four genera: Cynops, Paramesotriton, Salamandra, and Tylototriton
(Fig 3). These genera contain at least one species known to be susceptible to Bsal
infection [1]. Cynops and Paramesotriton comprise more than 90% of U.S. imported salamanders;
hence, these genera may be the greatest threat. Chinese newts (Pachytriton) comprise
approximately 4.5% of live salamanders imported into the US (S1 Table); their susceptibility
to Bsal has not been tested [1]. We estimated the total market value was US$924,707
for salamanders imported into the US in 2014 if all animals imported that year were
sold at the median market value (Table 1).
10.1371/journal.ppat.1005251.g003
Fig 3
Number of live salamanders from four genera (Cynops, Paramesotriton, Salamandra, Tylototriton)
imported into the US from 2004 to 2014 (USFWS Law Enforcement Management Information
System [LEMIS]); these genera comprise 95% of all legally traded salamander imports.
10.1371/journal.ppat.1005251.t001
Table 1
Estimated annual value (USD) of salamanders imported into the US based on 2014 imports
(see S1 Table) and a range of market values (low, median, and high).
Genus
Number Imported
Low Price
Median Price
High Price
Low Value
Median Value
High Value
Cynops
113,187
$4
$7
$10
$452,748
$792,309
$1,131,870
Pachytriton
2,908
$10
$15
$20
$29,080
$43,620
$58,160
Paramesotriton
2,536
$10
$15
$20
$25,360
$38,040
$50,720
Salamandra
1,027
$20
$32.5
$45
$20,540
$33,378
$46,215
Tylototriton
434
$30
$40
$50
$13,020
$17,360
$21,700
Total:
$540,748
$924,707
$1,308,665
If Bsal arrives in the US, several partners are working together to outline appropriate
actions. Partners in Amphibian and Reptile Conservation (PARC) formed a National Disease
Task Team in January 2015, with one of the initial objectives to help facilitate the
development of a strategic plan for Bsal. The US Geological Survey (USGS) held a Bsal
workshop in June 2015, with the goal of developing an objective decision-making process
to guide Bsal response actions. Twenty-nine professionals from four countries with
expertise in disease ecology and natural resource management participated in the USGS
workshop. A key outcome was the organization of a Bsal National Task Force for the
US, which is composed of a Technical Advisory Committee (TAC) and seven working groups.
The working groups are composed of experts focused on priority topics: (1) response
(to Bsal detection); (2) surveillance and monitoring; (3) research; (4) diagnostics;
(5) decision support; (6) data management; and (7) communication and outreach. The
working groups are developing products that are intended to become part of a larger
Bsal strategic plan. Chairpersons of the working groups are members of the TAC, which
meets monthly to share progress on various assigned tasks. Professionals interested
in contributing to Bsal working group tasks can contact one of the TAC co-chairs (Deanna
Olson, US Forest Service; Jennifer Ballard, USFWS).
Others are also responding to the threat of Bsal in North America. For example, the
PARC National Disease Task Team is assembling a regional list of professionals in
the US to contact if an amphibian mass mortality event is encountered and disease
suspected. This list will help formalize disease response and enable enhanced communication
with Bsal working groups who can provide guidance on response procedures and post-outbreak
monitoring actions. The Amphibian Survival Alliance (ASA), which holds a seat on the
TAC, is taking on ancillary tasks, such as leading development of a Bsal website to
disseminate information produced by the Bsal National Task Force and others as it
develops. Amphibiaweb.org hosts a website on Bsal (http://amphibiaweb.org/chytrid/Bsal.html)
and is currently developing a global Bsal reporting portal inspired by the Global
Ranavirus Reporting System (https://mantle.io/grrs) and Bd-maps (http://www.bd-maps.net;
M. Koo, University of California–Berkeley, personal communication). University of
California–Berkeley also created a LISTSERV for Bsal postings (bsal@lists.berkeley.edu);
subscribing can be done at https://calmail.berkeley.edu/manage/list/listinfo/bsal@lists.berkeley.edu.
Smaller regional efforts are occurring, too. For example, PARC and the ASA hosted
a Bsal meeting in Asheville, North Carolina, US, in August 2015 to inform and engage
regional biologists and the public. An outcome of this meeting was the creation of
a southern Appalachian Bsal task force, which is organized by Caleb Hickman (Eastern
Band of the Cherokee Indians).
State, provincial, and territorial fish and wildlife agencies in the US and Canada
have been engaging with Bsal through standing committees of the Association of Fish
and Wildlife Agencies (AFWA) to recommend policy actions based on the risk to native
salamanders. AFWA is also working with the TAC to develop a Bsal rapid response plan
that can be customized by local, state, or federal management entities. Along with
the ASA, AFWA is collaborating with various nongovernmental and commercial industry
partners, as well as with contacts in the US Congress, to examine various policy options
and solutions.
The Canadian government is actively working to reduce the risk of Bsal introduction
through import control. Environment Canada is exploring emergency measures similar
to those being considered in the US to prevent entry of the pathogen. The Canadian
Wildlife Health Cooperative recently identified diagnostic laboratories capable of
testing for Bsal infection in Canada, and is leading efforts for national surveillance
of the pathogen and outreach education to increase awareness. Policy responses to
Bsal have been slow in Mexico; however, scientists in Mexico and the US are collaborating
in laboratory experiments to test susceptibility of their native salamander species
to Bsal. Researchers in all three countries are independently testing wild and captive
animals for Bsal as part of ongoing pathogen surveillance studies. Clearly, a collaborative,
trilateral approach to Bsal surveillance, research, and response is essential to ensure
salamander resources in North America are protected.
In Europe, policy actions are limited to individual European states. In Belgium and
the Netherlands, abatement plans are being developed, mainly focused on raising public
awareness and developing emergency action plans. Recently, the Swiss Federal Food
Safety and Veterinary Office established a ban on the importation of all salamander
species into Switzerland (B. Schmidt, KARCH and University of Zurich, personal communication).
The only European transnational initiative currently consists of a draft recommendation
on prevention and control of Bsal, which will be proposed to the Standing Committee
of the Bern Convention in December 2015. This recommendation stresses the importance
of transnational and coordinated actions to limit spread and impact of Bsal in Europe,
but also to prevent introduction into naïve regions such as North America. We are
unaware of any additional countries currently involved in policy actions to prevent
the spread of Bsal.
What Can We Do in North America?
Due to the potential threat of Bsal to North American salamanders, creation of a North
American Strategic Plan for Bsal is warranted. Several good examples exist of strategic
plans for wildlife diseases, such as for white-nose syndrome [25] and Bd [26]. At
a minimum, components should include:
identification of possible routes of Bsal entry into the US, Canada, and Mexico;
strategies to prevent or reduce the risk of Bsal entry into the US, Canada, and Mexico;
surveillance and biosecurity strategies in the wild, the pet trade, and zoological
facilities;
diagnostic assays, reference laboratories, and approaches for confirmation of positive
samples;
response and disease intervention strategies if Bsal is detected in North America;
and
development of an information portal for communication, outreach, and education.
Additionally, a prioritized list of essential research directions is needed. Some
urgent research directions include: (1) estimating susceptibility of North American
amphibian species to Bsal; (2) determining the most efficient modes of Bsal transmission;
(3) identifying minimum concentrations of standard disinfectants to inactivate Bsal;
(4) validating Bsal diagnostic procedures; and (5) determining the interactive effects
of Bsal with stressors and other pathogens.
Conclusions
All evidence suggests that we are at a critical time of action to protect global amphibian
biodiversity by swift policy actions to prevent the translocation of Bsal (Box 1).
Bsal’s potential effects are broad taxonomically, geographically, ecologically, and
across a variety of ecosystem services. Hence, response to the threat of Bsal calls
for a cooperative effort across nongovernmental organizations, government agencies,
academic institutions, zoos, the pet industry, and concerned citizens to avoid the
potential catastrophic effects of Bsal on salamanders outside of the pathogen’s endemic
regions. Communication, collaboration, and expedited action are key to ensure that
Bsal does not become established in North America and decimate wild salamander populations.
The template developed for North America may inform similar strategic policy planning
for Bsal elsewhere.
Box 1. A North American Call for Action against Bsal
We know Bsal was likely introduced to Europe,
and is negatively impacting native salamanders there [1,2].
We know Bsal is lethal to many salamander species [1].
We know there is support for policy action
among governmental, nongovernmental, and industry partners.
We know timely preventative actions can reduce
the risk of catastrophic losses of North American salamanders due to Bsal [24].
The question remains: “Will sufficient policy action occur before it is too late?”
Supporting Information
S1 Table
Number of live salamanders imported by taxa into the USA, 2004 to 2014 (source = USFWS
LEMIS).
USFWS LEMIS data (S1 Table) for live salamander imports into the US available at:
http://www.amphibians.org/resources/tradedata/. Data requested in May 2015 under the
US Freedom of Information Act.
(PDF)
Click here for additional data file.