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Chytridiomycosis

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Chytridiomycosis

Summary

  • Last modified
  • 14 July 2018
  • Datasheet Type(s)
  • Animal Disease
  • Preferred Scientific Name
  • Chytridiomycosis
  • Overview
  • Chytridiomycosis is the disease state that results from a sustained cutaneous infection by Batrachochytrium dendrobatidis; it is an emerging infectious disease of amphibians causing mass mortality and populat...

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Pictures

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PictureTitleCaptionCopyright
Chytridiomycosis; swabbing a North American bullfrog, farmed for the food trade in China, to test for Batrachochytrium dendrobatidis infection.
TitleSwabbing
CaptionChytridiomycosis; swabbing a North American bullfrog, farmed for the food trade in China, to test for Batrachochytrium dendrobatidis infection.
Copyright©Lisa M. Schloegel
Chytridiomycosis; swabbing a North American bullfrog, farmed for the food trade in China, to test for Batrachochytrium dendrobatidis infection.
SwabbingChytridiomycosis; swabbing a North American bullfrog, farmed for the food trade in China, to test for Batrachochytrium dendrobatidis infection.©Lisa M. Schloegel
Chytridiomycosis; swabbing the hindfoot webbing of a North American bullfrog. to test for infection by the fungus Batrachochytrium dendrobatidis.
TitleSwabbing
CaptionChytridiomycosis; swabbing the hindfoot webbing of a North American bullfrog. to test for infection by the fungus Batrachochytrium dendrobatidis.
Copyright©Lisa M. Schloegel
Chytridiomycosis; swabbing the hindfoot webbing of a North American bullfrog. to test for infection by the fungus Batrachochytrium dendrobatidis.
SwabbingChytridiomycosis; swabbing the hindfoot webbing of a North American bullfrog. to test for infection by the fungus Batrachochytrium dendrobatidis.©Lisa M. Schloegel
Chytridiomycosis; North American bullfrogs in Taiwan, farmed for the international food trade.
TitleNorth American bullfrogs in culture
CaptionChytridiomycosis; North American bullfrogs in Taiwan, farmed for the international food trade.
Copyright©Lisa M. Schloegel
Chytridiomycosis; North American bullfrogs in Taiwan, farmed for the international food trade.
North American bullfrogs in cultureChytridiomycosis; North American bullfrogs in Taiwan, farmed for the international food trade.©Lisa M. Schloegel
Chytridiomycosis; North American bullfrogs in Taiwan, farmed for the international food trade.
TitleNorth American bullfrogs in culture
CaptionChytridiomycosis; North American bullfrogs in Taiwan, farmed for the international food trade.
Copyright©Lisa M. Schloegel
Chytridiomycosis; North American bullfrogs in Taiwan, farmed for the international food trade.
North American bullfrogs in cultureChytridiomycosis; North American bullfrogs in Taiwan, farmed for the international food trade.©Lisa M. Schloegel
Chytridiomycosis; a chytrid-infected frog showing symptoms of Bd.
TitleSymptoms
CaptionChytridiomycosis; a chytrid-infected frog showing symptoms of Bd.
Copyright©Forrest Brem - This image was published in a Public Library of Science journal. PLoS journals are published under a CC BY 2.5 license
Chytridiomycosis; a chytrid-infected frog showing symptoms of Bd.
SymptomsChytridiomycosis; a chytrid-infected frog showing symptoms of Bd.©Forrest Brem - This image was published in a Public Library of Science journal. PLoS journals are published under a CC BY 2.5 license
Chytridiomycosis; close view of north American bullfrogs in Taiwan, farmed for the international food trade.
TitleNorth American bullfrogs in culture
CaptionChytridiomycosis; close view of north American bullfrogs in Taiwan, farmed for the international food trade.
Copyright©Lisa M. Schloegel
Chytridiomycosis; close view of north American bullfrogs in Taiwan, farmed for the international food trade.
North American bullfrogs in cultureChytridiomycosis; close view of north American bullfrogs in Taiwan, farmed for the international food trade.©Lisa M. Schloegel

Identity

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Preferred Scientific Name

  • Chytridiomycosis

International Common Names

  • English: Bd disease

Local Common Names

  • Brazil: quitridio
  • Germany: Chytridiomykose
  • Netherlands: chytridiomycose

Overview

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Chytridiomycosis is the disease state that results from a sustained cutaneous infection by Batrachochytrium dendrobatidis; it is an emerging infectious disease of amphibians causing mass mortality and population declines worldwide.

Amphibian populations have been declining globally since the 1970s/1980s (McDonald, 1994; Laurance, 1996; Lips, 1999; Hero and Morrison, 2003); a global assessment by Stuart et al. (2004) revealed that one third of species were endangered. Various hypotheses have been proposed to explain the observed declines, including climate change, species introductions, habitat destruction, UV-B radiation, and pollution (Hayes and Jennings, 1986; Blaustein and Wake, 1990; Richards et al., 1993; Pounds and Crump, 1994). Of growing concern, however, were the mounting number of “enigmatic declines”. Later investigations of sick and dead adult anurans from the rainforests of Queensland and Panama revealed infection by a fungus; this infection was later described as chytridiomycosis, caused by Batrachochytrium dendrobatidis, or Bd (Berger et al., 1998; Longcore et al., 1999). Since that time, it has been reported in North America, South America, Africa, Europe and Asia. Bd is the first species of the phylum Chytridiomycota known to parasitize a vertebrate host. The fungus feeds on the keratin present in the epidermal layer of the skin. It infects a wide range of amphibian species and is increasingly implicated in the declines and extinctions of numerous amphibian species worldwide. In 2008, it was added to the OIE’s (World Organization for Animal Health) list of notifiable diseases due to increasing evidence of the spread of the pathogen through the live amphibian trade.

Hosts/Species Affected

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Bd has been found to infect more than 350 species of amphibians (Fisher et al., 2009b). This number continues to grow each year as surveillance efforts expand. It is still unclear why certain species are more susceptible to disease than others, but it appears that a number of environmental factors may be involved. For example, while experimental infections of Bd can be lethal in the White’s tree frog (Litoria caerulea) in captivity, infected populations of this species in the wild appear to be stable (Daszak et al., 1999). There can also be differences between countries and regions -- for example, Bufo bufo dies from chytridiomycosis in Spain, but no mortality has been observed in other countries (A. Spitzen, RAVON, Netherlands, personal communication, 2011). Furthermore, while Bd is capable of causing death and disease in the lab and in the wild in a number of amphibian species, pushing many to the brink of extinction, others appear to be resistant to the adverse effects of infection (e.g. Rana catesbeiana [Lithobates catesbeianus]) (Daszak et al., 2003). 

While Bd can be found in a wide range of environments, it appears to be most prevalent in stream-dwelling species in cooler climates. Berger et al. (2005b) found that species with low clutch sizes and restricted geographic ranges were often the most impacted. In the wet tropics of Queensland, Australia, prevalence of Bd infections was found to be highest during the cool, dry months and at higher elevations (600-800 m), suggesting regulation by climatic conditions such as temperature and precipitation (Woodhams and Alford, 2005). Temperate amphibian fauna, on the other hand, appear to be more susceptible to lethal infections at low elevations than are tropical frogs (Kriger et al., 2007). Kriger et al. (2007) also found that prevalence and intensity of infections appeared to be greatest at locales with high rainfall and cool temperatures. Analyses of die-offs in Central America suggest that those species with a high degree of endemism are heavily selected for extinction, significantly reducing amphibian biodiversity at a regional and global scale (Smith et al., 2009). Data also provide evidence that the amount of direct contact with other infectious animals, water or substrates could be a predictor of individual or species survival (Rowley et al., 2007). 

The composition of biota found on a frog’s skin has been implicated as a determining factor between life and death. Experimental studies found an increased survival rate, for instance, in amphibians with a high concentration on their skin of violacein, an antifungal metabolite produced by the betaproteobacterium Janthinobacterium lividum, which is a normal inhabitant on the skin of a number of amphibian species (Becker et al., 2009). Amphibians are also known to secrete a variety of antimicrobial peptides as an innate immune defense, some of which are more effective at inhibiting the growth of Bd than others (Rollins-Smith et al., 2005; Tenneson et al., 2009). Woodhams et al. (2006) found that the antimicrobial peptides secreted by an array of amphibians at a stream site in Panama varied greatly, and that those with an inherent immunologic defense were more likely to survive an outbreak of Bd. Woodhams et al. (2007b) suggest that symbiotic bacteria with the ability to persist in the presence of mucosal peptides may inhibit infection and colonization of the skin by Bd and increase the effectiveness of innate defense mechanisms in the skin. Savage and Zamudio (2011) found that MHC genotypes were associated with resistance or susceptibility to the disease.

Distribution

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At the time of its discovery in 1998, Bd had already achieved a global distribution and its presence has since been confirmed on every major continent except Antarctica (where amphibian fauna are not present) (Fisher et al., 2009b), although the presence of infection does not necessarily indicate the presence of the disease (A. Spitzen, RAVON, Netherlands, personal communication, 2011). It is now known to infect more than 350 of the more than 5000 recognized amphibian species (Fisher et al., 2009b). The number of infected species is likely to be an underestimate of the true number infected by the pathogen (owing to a lack of surveys in many regions of the world). The distribution of the fungus in Asia, for instance, is still largely un-assessed. New studies, however, are beginning to reveal the presence of Bd in this region of the world (e.g. Japan, Indonesia, Taiwan), both past and present (Kusrini et al., 2008; Goka et al., 2009; L. Schloegel et al., Wildlife Trust, New York, USA, unpublished data). Goka et al. (2009), for instance, reported the presence of Bd in preserved specimens of Andrias japonicus (Japanese giant salamander) from Japan in 1902, the earliest record known to date.

The origin of Bd is still largely disputed. Histological analysis of preserved museum specimens has aided researchers in assessing the historical presence of the pathogen in some areas. Until reports by Goka et al. (2009), the oldest known record of Bd was found in a Xenopus laevis (African clawed frog) specimen from South Africa preserved in 1938 (Weldon et al., 2004), leading many to speculate that Africa was the pathogen’s place of origin. X. laevis was heavily traded for use in human pregnancy testing in the 1930s and 1940s, and is still the most widely used species for research today. Invasive populations of this amphibian have been documented in many areas. Further support for the hypothesis of African Xenopus spp. being the original source of Bd is provided by Soto-Azat et al. (2009), who studied museum specimens of frogs from Africa and South America and found Bd only in Xenopus from Africa. The distribution of X. laevis populations, however, appears to be inconsistent with the nature of Bd outbreaks, indicating that additional hosts must play a role in the spread of this disease to new locales (Rachowicz et al., 2005).

The current distribution of B. dendrobatidis is mapped on the website http://www.spatialepidemiology.net/bd/.

Distribution Table

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The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.

Continent/Country/RegionDistributionLast ReportedOriginFirst ReportedInvasiveReferenceNotes

Asia

ArmeniaDisease not reportedOuellet et al., 2005
ChinaPresentBai et al., 2012
-Hong KongDisease not reportedRowley et al., 2007
-SichuanPresentZeng et al., 2011
IndiaPresentPresent based on regional distribution.
-KeralaLocalisedIntroducedNair et al., 2011
IndonesiaPresentPresent based on regional distribution.
-JavaPresent2007Kusrini et al., 2008Mount Gede Pangrango National Park
IranDisease not reportedOuellet et al., 2005
JapanWidespreadIntroducedGoka et al., 2009
-HonshuPresent only in captivity/cultivation2007IntroducedUne et al., 2008Tokyo
Korea, Republic ofPresentYang et al., 2009
MalaysiaPresentPresent based on regional distribution.
-Peninsular MalaysiaPresentSavage et al., 2011
ThailandDisease not reportedMcLeod et al., 2008

Africa

CameroonAbsent, unreliable recordDoherty-Bone et al., 2008; Soto-Azat et al., 2009
Congo Democratic RepublicPresentGreenbaum et al., 2008Kahuzi Biega National Park, South Kivu Province
GabonPresentBell et al., 2011
KenyaWidespreadOuellet et al., 2005; Kielgast et al., 2010
MadagascarDisease not reportedWeldon et al., 2008
MalawiAbsent, unreliable recordSoto-Azat et al., 2009
MoroccoLocalisedEl-Mouden et al., 2011
South AfricaWidespreadNativeWeldon et al., 2004
SwazilandPresentWeldon et al., 2004
UgandaPresent2006Goldberg et al., 2007Kibale National Park, Western Uganda

North America

CanadaPresentPresent based on regional distribution.
-British ColumbiaWidespreadGarner et al., 2006
-ManitobaDisease not reportedOuellet et al., 2005
-Northwest TerritoriesPresentSchock et al., 2010
-OntarioWidespreadGarner et al., 2006
MexicoLocalised2006Frías-Alvarez et al., 2008
USAPresentPresent based on regional distribution.
-AlabamaPresent2006Byrne et al., 2008
-AlaskaPresentReeves and Green, 2006
-ArizonaWidespread2006Schlaepfer et al., 2007; Picco and Collins, 2008
-ArkansasWidespread2006Rothermel et al., 2008
-CaliforniaWidespreadIntroduced Invasive Padgett-Flohr and Hopkins, 2009
-ColoradoWidespread2004Muths et al., 2008
-FloridaDisease not reportedRothermel et al., 2008
-GeorgiaWidespread2008Rothermel et al., 2008
-HawaiiWidespread2004IntroducedBeard and O'Neill, 2005
-IdahoWidespread2004Muths et al., 2008
-IndianaPresent1970sOuellet et al., 2005
-KansasDisease not reportedOuellet et al., 2005
-LouisianaWidespread2006Rothermel et al., 2008
-MaineWidespreadLongcore et al., 2007National wildlife refuges and federal lands
-MarylandPresentGrant et al., 2008Chesapeake and Ohio Canal National Historic Park
-MassachusettsWidespreadLongcore et al., 2007Federal refuges
-MichiganDisease not reportedOuellet et al., 2005
-MinnesotaPresent1980sOuellet et al., 2005
-MississippiDisease not reportedRothermel et al., 2008
-MissouriPresent1990-2001Ouellet et al., 2005
-MontanaWidespread2004Muths et al., 2008
-New HampshireWidespreadLongcore et al., 2007Federal refuges
-New YorkWidespreadLongcore et al., 2007
-North CarolinaWidespread2006Rothermel et al., 2008
-North DakotaDisease not reportedOuellet et al., 2005
-OregonWidespread2006Pearl et al., 2007
-PennsylvaniaPresentRaffel et al., 2010
-South CarolinaWidespread2006Rothermel et al., 2008
-TennesseeDisease not reportedRothermel et al., 2008
-TexasPresentGaertner et al., 2009Central Texas
-VermontWidespreadLongcore et al., 2007Federal refuges
-VirginiaWidespread2006Rothermel et al., 2008
-WashingtonWidespread2006Pearl et al., 2007
-WisconsinPresent1980sOuellet et al., 2005
-WyomingWidespread2008Murphy et al., 2009

Central America and Caribbean

BarbadosDisease not reportedOuellet et al., 2005
Costa RicaWidespreadPuschendorf et al., 2009
CubaPresentDíaz et al., 2007Central Cuba
DominicaPresentMalhotra et al., 2007
El SalvadorPresentLawson et al., 2011
GuatemalaPresentMendelson et al., 2004
HondurasPresentPuschendorf et al., 2006
PanamaWidespread2007Introduced Invasive Woodhams et al., 2008b; Brem and Lips, 2008
Puerto RicoPresentBurrowes et al., 2004
Trinidad and TobagoWidespreadAlemu et al., 2008Tobago

South America

ArgentinaWidespreadHerrera et al., 2005; Barrionuevo and Ponssa, 2008
BoliviaPresentBarrionuevo and Ponssa, 2008Huayramayu River, Carrasco National Park, Cochabamba
BrazilPresentPresent based on regional distribution.
-GoiasPresentGarner et al., 2006Brasilia
-Minas GeraisPresent2005Garner et al., 2006
-ParaPresent only in captivity/cultivation2008Schloegel et al., 2009
-PernambucoPresentCarnaval et al., 2006
-Rio de JaneiroPresentCarnaval et al., 2006
-Sao PauloPresent2006Schloegel et al., 2009
ChileLocalisedSolís et al., 2010
ColombiaPresent2005Ruiz and Rueda-Almonacid, 2008
EcuadorPresent1998Santiago and Merino, 2000
PeruPresent2003Seimon et al., 2007
UruguayPresent, few occurrencesMazzoni et al., 2003; Borteiro et al., 2009
VenezuelaWidespread2006Sánchez et al., 2008

Europe

AustriaPresentSztatecsny, 2008; Sztatecsny and Glaser, 2011
BelgiumPresent, few occurrencesMutschmann et al., 2000; Pasmans et al., 2010
DenmarkPresentScalera et al., 2008
FranceWidespreadGarner et al., 2006
GermanyPresentMutschmann et al., 2000; Ohst et al., 2011
ItalyWidespreadSimoncelli et al., 2005
JerseyAbsent, confirmed by surveyCunningham and Minting, 2008
LatviaDisease not reportedOuellet et al., 2005
LuxembourgLocalisedWood et al., 2009
NetherlandsPresent only in captivity/cultivationSpitzen-van der Sluijs et al., 2011
PortugalWidespread2004Garner et al., 2005
Russian FederationDisease not reportedOuellet et al., 2005
SpainWidespread2004Garner et al., 2005
SwitzerlandWidespread2004Garner et al., 2005
UKPresentGarner et al., 2006; Cunningham and Minting, 2008

Oceania

AustraliaPresentPresent based on regional distribution.
-New South WalesWidespread2007Kriger et al., 2007
-QueenslandWidespread2006Kriger and Hero, 2008; North and Alford, 2008
FijiDisease not reportedOuellet et al., 2005
New ZealandPresent2001Bell et al., 2004
Papua New GuineaDisease not reportedOuellet et al., 2005

Diagnosis

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Clinical signs of disease in adults include lethargy, excessive shedding of the skin and death (Nichols et al., 2001). In tadpoles, infection is limited to the mouthparts and often causes de-pigmentation (also known as missing mouthparts) as a result of de-keratinization. Infection can be confirmed using PCR or histological analyses.

Histology

Toe clips are the preferred tissue sample for adults (although skin from the drink patch area may also be used). In tadpoles, infection can be found in the mouthparts. All tissue samples are preserved in 70% ethanol until they are processed for histology using a haematoxylin and eosin stain. 

Infection in histological samples is verified by the presence of clusters of spherical zoosporangia in the outer layer of the epidermis. Bd zoosporangia can be characterized by a refractive cell wall, visible zoospores within the mature sporangium, discharge papillae, internal septa and thickening of the epidermis. In some instances only one or two of the defining characteristics may be present. Histological preparation of samples is invasive to the amphibian, but has the benefit of determining whether an infection is light and focal or heavy and widespread. 

PCR

A real-time Taqman PCR assay has been developed to detect Bd infection using skin tissue or skin swabs (Boyle et al., 2004) and is a more reliable method than histological means (Kriger et al., 2006). The swab method is capable of sampling a larger area of an amphibian than using tissue samples. In frogs known to have light and often focal infections (e.g. the North American bullfrog), use of a skin swab may be preferable to a tissue sample. PCR detection of Bd is very sensitive (capable of detecting the presence of a single zoospore), so extreme caution should be taken during sample collection to avoid contamination. A fresh pair of gloves should be used with each individual animal and any equipment should be sterilized between specimens; this can be done by bleaching and flaming, but the disinfectant Virkon S is recommended as it is less toxic to the environment (RACE, 2010). While testing costs for PCR are high (approximately US$20 per swab), it is a more sensitive method of detecting infection. Furthermore, the use of skin swabs is non-invasive and may be beneficial when sampling live amphibians in the wild.

List of Symptoms/Signs

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SignLife StagesType
General Signs / Lack of growth or weight gain, retarded, stunted growth Sign
General Signs / Sudden death, found dead Sign
General Signs / Underweight, poor condition, thin, emaciated, unthriftiness, ill thrift Sign
General Signs / Weight loss Sign
Skin / Integumentary Signs / Hyperkeratosis, thick skin Sign
Skin / Integumentary Signs / Skin necrosis, sloughing, gangrene Sign

Disease Course

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Chytridiomycosis causes widespread infection of the skin resulting in hyperkeratosis, sloughing and erosions of the epidermis, and occasional ulcerations (Berger et al., 1998; Nichols et al., 2001). Excessive shedding of the skin may be visible approximately 12-15 days after exposure and may result in death in 1-4 weeks post-exposure (Nichols et al., 2001). Heavy infections appear to disrupt the transport of electrolytes (i.e. plasma sodium and potassium) across the epidermal layer, reducing electrolyte concentrations in cell plasma, and resulting in asystolic cardiac arrest and death. This disruption of cutaneous function may be the mechanism through which Bd cayses morbidity and mortality across a wide range of phylogenetically distinct amphibian taxa (Voyles et al., 2009).

Carver et al. (2010) found evidence of inhibited rehydration through the skin in frogs (Litoria raniformis) showing clinical signs of chytridiomycosis, but not in those that recovered and remained infected without symptoms (as 5 of their 6 infected subjects did, suggesting an adaptive immune response to infection).

Different Bd isolates vary in their virulence (Fisher et al., 2009a).

Epidemiology

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Animals can pick up infection through direct contact with another infected amphibian (Rachowicz and Vredenberg, 2004). Bd can also be carried through water. Johnson and Speare (2003) showed that viable zoospores were capable of surviving (without a host) in tap and deionized water for 3-4 weeks and lake water for up to 7 weeks. An experiment looking at sterile, moist sand and sterile bird feathers suggest that these substrates could also serve to disperse the pathogen, but additional studies are required to validate these results in the wild (Johnson and Speare, 2005). The role of additional vectors and/or substrates in the spread of Bd is still being investigated. 

There is increasing data to support the notion that the anthropogenic trade in, or the introduction of, amphibians is responsible for the recent spread of Bd, with papers reporting the presence of the fungus in the pet trade, zoological collections, introduced species and the laboratory animal trade, among others (Nichols et al., 2001; Daszak et al., 2003; Une et al., 2008; Schloegel et al., 2009). The North American bullfrog (Rana catesbeiana [Lithobates catesbeianus]) is thought to be a carrier of Bd, exhibiting no clinical signs when experimentally or naturally infected with the fungus (Daszak et al., 2004); it is a globally traded commodity, and is sold live in markets throughout the world (Schlaepfer et al., 2005; Schloegel et al., 2009). It is thought that the international movement of R.catesbeiana has served as a pathway of introduction in many regions of the world.

The pattern of amphibian declines (Daszak et al., 1999), and genetic studies (Daszak et al., 2003; Morehouse et al., 2003) support the hypothesis that Bd has been recently introduced into native populations, at least in Central America and Australia. Goka et al. (2009) suggest that a combination of the ‘novel pathogen hypothesis’ and the ‘endemic pathogen hypothesis’ explain the current pandemic.

Research in Central and South America suggests that the pathogen is invasive in this region (Lips et al., 2006, 2008). The mode of introduction and timing of introductions are still unknown in many regions, however; it is thought that sequencing data of Bd isolates will help to unravel this mystery. 

It is becoming evident that there is still much that is not known about the current and historical distribution of Bd. It is hoped that a catalogue of global isolates for comparative analyses will shed light on its origin and subsequent spread.

A number of studies show that the prevalence of chytridiomycosis in a population of frogs can vary dramatically throughout the year, with disease levels closely tracking temperature changes, being at their highest at cooler times of year, including early spring, when many amphibians are most likely to be exposed to the waterborne zoospores when they enter the water to breed (Spitzen-van der Sluijs and Zollinger, 2010).

The review by Spitzen-van der Sluijs and Zollinger (2010) also contains further discussion of the ways in which Bd is dispersed.

Impact

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Economic Impact 

Amphibians make up a large proportion of the biomass in many tropical regions of the world. With their vibrant colours and unique life history traits, they can be a draw for many tourists. The loss of so many of the world’s anurans, and the effects of that loss on the surrounding environment, could have implications for the tourism industry upon which many people base their livelihoods (although Wollenberg et al. (2010) found that ecotourists in Madacascar, with little prior knowledge of the disease, were happy to follow preventive measures and were correctly not worried about it as a threat to their own health).

The economic impact of Bd on trade routes through the development of national and international policy is also impending. In May, 2008, the World Organization for Animal Health (OIE) listed Bd as a notifiable disease. The guidelines set forth by the OIE serve to increase awareness but may also be used as a basis for the implementation of policy in countries trading in amphibians. Efforts are already underway to incorporate OIE guidelines for Bd into legislation in the USA. Should legislation pass, it could mean that all live anuran imports would need to undergo routine quarantine and testing, among other things. With millions of amphibians imported into the USA each year (Schlaepfer et al., 2005; Gratwicke et al., 2009; Schloegel et al., 2009), the costs incurred by the implementation of quarantine standards could have a negative impact on the trade.

The economic costs of restoring disrupted ecosystems are likely to be higher than the costs of preventive or curative measures. Amphibians are important in the food chain, and their loss is detrimental to all ecosystems. For example they eat insects in large numbers, so their disappearance can cause significant problems in agriculture or human health. The costs of such losses are almost impossible to calculate, but should be taken into account (A. Spitzen, RAVON, Netherlands, personal communication, 2011).

Social Impact

The various antimicrobial peptide (AMP) secretions from amphibians are thought to have numerous applications to human medicine. Many species are in decline due to infection with Bd; along with the disappearances of these species go any hopes of using their unique abilities that could greatly benefit human health. 

For example, epibatidine, extracted from the Ecuadorian poison frog (Epipedobates anthonyi) is thought to be an effective non-narcotic pain reliever (Garraffo et al., 2009) and a peptide extracted from the Chinese brown frog (Rana chensinensis) could have uses as an antimicrobial agent (Jin et al., 2009). Perhaps one of the most significant advances so far is the discovery of a series of peptides found to be effective at inhibiting HIV infection of T cells, the implications of which could be ground-breaking (Scott et al., 2005). 

Researchers believe that the Australian southern and northern gastric brooding frogs (Rheobatrachus silus and R. vitellinus) could have held a cure for the common ulcer. The fertilized eggs of these species were swallowed by the adult frogs. The gastric juices of the frog’s stomach could be halted during development, allowing the larval stage to grow without harm. These species are currently listed as extinct by the IUCN Red List of Endangered Species (Meyer et al., 2004; Hero et al., 2004).

Apart from any practical use of amphibian species, many people are likely to be distressed by their decline or disappearance (A. Spitzen, RAVON, Netherlands, personal communication, 2011). 

Environmental Impact

Impact on habitats

The presence of Bd is likely to have a significant impact on natural habitats through the loss of amphibian biodiversity. Amphibians are both aquatic and terrestrial, and any changes in their abundance will likely affect both systems. Tadpoles typically feed on algae, detritus and other animals (Whiles et al., 2006), and changes in abundance or species composition are known to alter algal community structure (Kupferberg, 1997). The presence of amphibians can impact nutrient cycling and leaf litter decomposition, plant communities and arthropod biomass (Beard et al., 2002). It is also thought that amphibians contribute to ecosystem recovery and resilience following events such as a hurricane (Beard et al., 2002). Amphibians are also an important prey item. A study in the Sierra Nevada, California, found that the presence of the Garter snake (Thamnophis elegans) is highly dependent on the availability of its primary prey item, amphibians (Jennings et al., 1992).

Impact on biodiversity

Current estimates indicate that 32% of amphibian species (1856 out of 5743) are threatened with extinction (Stuart et al., 2004). Not all the declines are Bd-related, but enigmatic declines (including disease) appear to be on the rise and are of major concern (Stuart et al., 2004). Smith et al. (2009) analyzed the patterns of amphibian declines in tropical American amphibians (an area known to have Bd-associated declines). The data indicate that those species most likely to be extirpated were those with low occupancy and a high degree of endemism. The resulting assemblage of amphibian fauna post-decline is a homogenization of species across a range of sites, thereby reducing biodiversity at the regional and global levels. There have been 9 amphibian species extinctions since 1980, an additional 113 are thought to be extinct and many more are considered to be threatened with extinction (Ron et al., 2005). These numbers are on the rise as Bd spreads into new regions and more data come to light.

Vredenburg et al. (2010) studied the dynamics of invasion of previously unexposed populations and found that it was the high growth rate and virulence of Bd that enabled it to reach high densities in all host individuals and cause population crashes before its spread was limited by reduced density of hosts.

The threatened species table in the Batrachochytrium dendrobatidis datasheet contains those species for which: (1) there is a documented link between infection with Bd and declines and (2) the species is listed as threatened by the IUCN Red List of Endangered Species (i.e. Near Threatened, Vulnerable, Endangered, Critically Endangered, Extinct in the Wild or Extinct). Those species that filled the criteria for number 1, but for which an IUCN listing could not be found, were also included. There are many more species for which infection and/or dead and dying frogs have been documented, or which are in decline presumably due to chytridiomycosis, but detailed data linking disease with declines are lacking. Skerratt et al. (2007), for instance, state that Bd may be implicated in the decline or extinction of up to 200 species of amphibians (the most spectacular loss of vertebrate biodiversity due to disease in recorded history).

Further discussion of the importance of the impact of Bd on amphibian populations can be found in articles by Heard et al. (2011) and Duffus (2009).

Zoonoses and Food Safety

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Bd is known to infect only amphibian fauna and is not known to pose a threat to human health via contact or consumption. The presence of Bd in live animals in the food trade (markets and farms) has been identified and could have a negative impact on native amphibians should infected individuals escape into the wild (Hanselmann et al., 2004; Schloegel et al., 2009; Schloegel et al., 2010). It is also possible that the disposal of water wastes could transport viable zoospores into the surrounding environment (Johnson and Speare, 2003). While a large percentage of frogs intended for the food trade are shipped internationally as a live commodity, many are also exported in the form of frozen frogs’ legs. The general consensus is that the combined processes of removing the skin (the primary organ infected) and the subsequent freezing of the legs are enough to eliminate and/or kill the fungus. Shipments of frozen frogs’ legs should therefore present little, if any, danger of pathogen transport.

While chemical treatments of live individuals to cure Bd infections are available, it is unknown whether they leave food animals safe for consumption. The antimicrobial chloramphenicol has been shown to be effective in curing Bd infections (Bishop et al., 2009), but there is much controversy surrounding the Acceptable Daily Intake (ADI) of chloramphenicol and its use in animals intended for human consumption  (Hanekamp and Calabrese, 2007; Wongtavatchai et al., 2009). Furthermore, both the chemical and non-chemical (i.e. heat) treatments available are costly and not practical when applied to the large quantities of animals present in the food trade.

Disease Treatment

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Treatments of individuals for Bd include the topical application of various chemical agents including the antifungal drug itraconazole (immersion in a 0.01% solution, 5 minutes per day for 8-11 days) and the antibacterial chloramphenicol (5 day treatment with solution or ointment) (Nichols and Lamirande, 2001; Bishop et al., 2009). Short-term (less than 16 hours) elevated body temperature (37°C) has also proven successful (Retallick and Miera, 2007; Woodhams et al., 2008a; Garner et al., 2009). Experimental trials of these treatments, however, have been conducted in only a small number of the amphibians known to harbour Bd infections, and additional studies are required to assess the efficacy in a broad range of species. Furthermore, these methods have not been developed into regimes that are able to treat large populations of amphibians, particularly for frogs in the food and pet trade. While captive individuals can be cured of infection, there are no protocols for eradicating the pathogen from amphibians in the wild.

Further information on treatment can be found in Berger et al. (2010), Martel et al. (2011), Johnson et al. (2003), Forzán et al. (2008), Cashins et al. (2008), Garner et al. (2009) and Schmidt et al. (2009).

Prevention and Control

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At present, disease surveillance for amphibians in the international trade is minimal, but efforts are underway to address the issue. In May 2008, the OIE (World Organization for Animal Health) World Assembly of Delegates unanimously approved the addition of Batrachochytrium dendrobatidis to the OIE list of aquatic animal diseases. This was subsequently implemented in the 2008 edition of the Aquatic Code, effectively making Bd a notifiable disease (World Organization for Animal Health, 2008). A notifiable disease is one whose detection must be notified by the competent veterinary authority to the OIE. It is required that the presence or absence of this disease in OIE member countries be reported on a semi-annual basis and that disease surveillance programs be employed to validate any claims of freedom from disease. 

The OIE provides a set of standards and guidelines for minimizing the spread of listed pathogens through the trade. In the case of Bd, such measures include the treatment of infected individuals and proper sanitation of wastes, or the direct delivery of infected animals to a lifelong holding, biosecure facility (http://www.oie.int/eng/normes/fcode/a_summry.htm). It is recommended that animals transported for the food trade be immediately shipped to a processing facility and quarantined until they can be slaughtered and converted into a product that neutralizes the disease agent, such as canned or dried products, leather products and skinned carcasses or legs. Any wastes and/or surfaces that come into contact with an amphibian should be sterilized with an over-the-counter bleach solution (sodium hypochlorite concentration of 1% and above) (Johnson et al., 2003; Webb et al., 2007). Any reduction in trade due to increased costs of quarantine and control measures might itself reduce the risk of the infection being spread (A. Spitzen, RAVON, Netherlands, personal communication, 2011.

The pet industry is becoming increasingly aware of the potential dangers of spreading Bd through the live amphibian trade and voluntary actions are gaining momentum. The United States’ Pet Industry Joint Advisory Council’s (PIJAC) Bd Free 'Phibs campaign (www.pijac.org/projects/project.asp?p=26), for instance, promotes safe husbandry practices and is open to participation from all clientele maintaining amphibian populations ex-situ.   

At present, the frog farming industry has no known mandated or voluntary practices to prevent cross-farm contamination or disease transmission amongst captive and wild populations. Unfortunately, large-scale eradication of Bd in farmed amphibians is not likely as the available cures are expensive, not applicable to large-scale populations, and not yet proven safe for the animals or for human consumption. New farm startups should be given careful attention. Enclosures should be built to limit any potential interaction between captive and wild anurans. Disease-free populations should be established and carefully maintained in captivity to provide stock animals. Water filtration systems should also be examined closely to ensure that they are effective at neutralizing fungal contaminants.

Although activities such as nature watching and scientific fieldwork can potentially spread the infection, simple disinfection measures are effective in decontaminating equipment, clothing and people (RACE, 2010). Wollenberg et al. (2010) found that ecotourists in Madacascar were happy to follow preventive measures.

References

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Alemu I JB; Cazabon MNE; Dempewolf L; Hailey A; Lehtinen RM; Mannette RP; Naranjit KT; Roach ACJ, 2008. Presence of the chytrid fungus Batrachochytrium dendrobatidis in populations of the Critically Endangered frog Mannophryne olmonae in Tobago, West Indies. EcoHealth, 5(1):34-39. http://www.springerlink.com/content/c505v7r5464t1314/?p=5ae3c4890b264f18862333799e2f34b1&pi=6

Bai ChangMing; Liu Xuan; Fisher MC; Garner TWJ; Li YiMing, 2012. Global and endemic Asian lineages of the emerging pathogenic fungus Batrachochytrium dendrobatidis widely infect amphibians in China. Diversity and Distributions, 18(3):307-318. http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1472-4642

Barrionuevo JS; Aguayo R; Lavilla EO, 2008. First record of chytridiomycosis in Bolivia (Rhinella quechua; Anura: Bufonidae). Diseases of Aquatic Organisms, 82(2):161-163. http://www.int-res.com/abstracts/dao/v82/n2/p161-163/

Barrionuevo JS; Ponssa LM, 2008. Decline of three species of the genus Telmatobius (Anura: Leptodactylidae) from Tucumán Province, Argentina. Herpetologica, 64(1):47-62. http://www.bioone.org/perlserv/?request=get-document&doi=10.1655%2F06-057.1

Beard KH; O'Neill EM, 2005. Infection of an invasive frog Eleutherodactylus coqui by the chytrid fungus Batrachochytrium dendrobatidis in Hawaii. Biological Conservation, 126(4):591-595.

Beard KH; Vogt KA; Kulmatiski A, 2002. Top-down effects of a terrestrial frog on forest nutrient dynamics. Oecologia, 133(4):583-593.

Becker MH; Brucker RM; Schwantes CR; Harris RN; Minbiole KPC, 2009. The Bacterially Produced Metabolite Violacein Is Associated With Survival of Amphibians Infected with a Lethal Fungus. Applied and Environmental Microbiology, 75(21):6635-6638.

Bell BD; Carver S; Mitchell NJ; Pledger S, 2004. The recent decline of a New Zealand endemic: how and why did populations of Archey's frog Leiopelma archeyi crash over 1996-2001? Biological Conservation, 120(2):189-199.

Bell RC; Gata Garcia AV; Stuart BL; Zamudio KR, 2011. High Prevalence of the Amphibian Chytrid Pathogen in Gabon. EcoHealth. http://dx.doi.org/10.1007/s10393-010-0364-4

Berger L; Hyatt AD; Speare R; Longcore JE, 2005. Life cycle stages of the amphibian chytrid Batrachochytrium dendrobatidis. Diseases of Aquatic Organisms, 68(1):51-63. http://www.int-res.com/abstracts/dao/v68/n1/p51-63/

Berger L; Marantelli G; Skerratt LF; Speare R, 2005. Virulence of the amphibian chytrid fungus Batrachochytrium dendrobatidis varies with the strain. Diseases of Aquatic Organisms, 68(1):47-50. http://www.int-res.com/abstracts/dao/v68/n1/p47-50/

Berger L; Speare R; Daszak P; Green DE; Cunningham AA; Goggin CL; Slocombe R; Ragan MA; Hyatt AD; McDonald KR; Hines HB; Lips KR; Marantelli G; Parkes H, 1998. Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. Proceedings of the National Academy of Sciences of the United States of America, 95(15):9031-9036.

Berger L; Speare R; Pessier A; Voyles J; Skerratt LF, 2010. Treatment of chytridiomycosis requires urgent clinical trials. Diseases of Aquatic Organisms, 92(2/3):165-174. http://www.int-res.com/abstracts/dao/v92/n2-3/p165-174/

Bishop PJ; Speare R; Poulter R; Butler M; Speare BJ; Hyatt A; Olsen V; Haigh A, 2009. Elimination of the amphibian chytrid fungus Batrachochytrium dendrobatidis by Archey's frog Leiopelma archeyi. Diseases of Aquatic Organisms, 84(1):9-15. http://www.int-res.com/articles/dao_oa/d084p009.pdf

Blaustein AR; Wake DB, 1990. Declining amphibian populations: a global phenomenon. Trends in Ecology and Evolution, 5:203-204.

Borteiro C; Cruz JC; Kolenc F; Aramburu A, 2009. Chytridiomycosis in frogs from Uruguay. Diseases of Aquatic Organisms, 84(2):159-162. http://www.int-res.com/abstracts/dao/v84/n2/p159-162/

Bovero S; Sotgiu G; Angelini C; Doglio S; Gazzaniga E; Cunningham AA; Garner TWJ, 2008. Detection of chytridiomycosis caused by Batrachochytrium dendrobatidis in the endangered Sardinian newt (Euproctus platycephalus) in southern Sardinia, Italy. Journal of Wildlife Diseases, 44(3):712-715. http://www.wildlifedisease.org

Boyle DG; Boyle DB; Olsen V; Morgan JAT; Hyatt AD, 2004. Rapid quantitative detection of chytridiomycosis (Batrachochytrium dendrobatidis) in amphibian samples using real-time Taqman PCR assay. Diseases of Aquatic Organisms, 60(2):141-148. http://www.int-res.com/abstracts/dao/v60/n2/p141-148.html

Brem FMR; Lips KR, 2008. Batrachochytrium dendrobatidis infection patterns among Panamanian amphibian species, habitats and elevations during epizootic and enzootic stages. Diseases of Aquatic Organisms, 81(3):189-202. http://www.int-res.com/abstracts/dao/v81/n3/p189-202/

Buck JC; Truong L; Blaustein AR, 2011. Predation by zooplankton on Batrachochytrium dendrobatidis: biological control of the deadly amphibian chytrid fungus? Biodiversity and Conservation, 20(14):3549-3553.

Burrowes P; Joglar R; Green DE, 2004. Potential causes for amphibian declines in Puerto Rico. Herpetologica, 60:141-154.

Byrne MW; Davie EP; Gibbons JW, 2008. Batrachochytrium dendrobatidis occurrence in Eurycea cirrigera. Southeastern Naturalist, 7(3):551-555. http://www.eaglehill.us/jsgeninf.html

Carnaval ACOD; Puschendorf R; Peixoto OL; Verdade VK; Rodrigues MT, 2006. Amphibian chytrid fungus broadly distributed in the Brazilian Atlantic Rain Forest. EcoHealth, 3(1):41-48.

Carver S; Bell BD; Waldman B, 2010. Does chytridiomycosis disrupt amphibian skin function? Copeia, No.3:487-495. http://www.bioone.org/doi/abs/10.1643/CH-09-128

Cashins SD; Skerratt LF; Alford RA, 2008. Sodium hypochlorite denatures the DNA of the amphibian chytrid fungus Batrachochytrium dendrobatidis. Diseases of Aquatic Organisms, 80(1):63-67. http://www.int-res.com/abstracts/dao/v80/n1/p63-67/

Cunningham AA; Garner TWJ; Aguilar-Sanchez V; Banks B; Foster J; Sainsbury AW; Perkins M; Walker SF; Hyatt AD; Fisher MC, 2005. Emergence of amphibian chytridiomycosis in Britain. Veterinary Record, 157(13):386-387.

Cunningham AA; Minting P, 2008. National survey of Batrachochytrium dendrobatidis infection in UK amphibians, 2008: Final report. UK: Amphibian and reptile groups of the UK, 28 pp. http://www.arguk.org/download-document/27-national-survey-of-batrachochytrium-dendrobatidis-infection-in-uk-amphibians

Daszak P; Berger L; Cunningham AA; Hyatt AD; Green DE; Speare R, 1999. Emerging infectious diseases and amphibian population declines. Emerging Infectious Diseases, 5(6):735-748.

Daszak P; Cunningham AA; Hyatt AD, 2000. Emerging infectious diseases of wildlife - threats to biodiversity and human health. Science (Washington), 287(5452):443-449.

Daszak P; Cunningham AA; Hyatt AD, 2003. Infectious disease and amphibian population declines. Diversity and Distributions, 9(2):141-150.

Daszak P; Strieby A; Cunningham AA; Longcore JE; Brown CC; Porter D, 2004. Experimental evidence that the bullfrog (Rana catesbeiana) is a carrier of chytridiomycosis, an emerging fungal disease in amphibians. Herpetological Journal, 14:201-207.

Díaz LM; Cadiz A; Chong A; Silva A, 2007. First report of chytridiomycosis in a dying toad (Anura: Bufonidae) from Cuba: A new conservation challenge for the island. EcoHealth, 4(2):172-175.

Doherty-Bone TM; Bielby J; Gonwouo NL; LeBreton M; Cunningham AA, 2008. In a vulnerable position? Preliminary survey work fails to detect the amphibian chytrid pathogen in the highlands of Cameroon, an amphibian hotspot. Herpetologial Journal, 18(2):115-118.

Duffus ALJ, 2009. Chytrid blinders: what other disease risks to amphibians are we missing? EcoHealth, 6(3):335-339. http://www.springerlink.com/content/0307k31442p4367w/?p=c25fb06dd3aa4bd0b58907d4994fdb82&pi=4

El-Mouden EH; Slimani T; Donaire D; Fernández-Beaskoetxea S; Fisher MC; Bosch J, 2011. First record of the chytrid fungus Batrachochytrium dendrobatidis in North Africa. Herpetological Review, 42(1):71-75.

Farrer RA; Weinert LAW; Bielby J; Garner TWJ; Balloux F; Clare F; Bosch J; Cunningham AA; Weldon C; Preez LH du; Anderson L; Kosakovsky Pond SL; Shahar-Golan R; Henk DA; Fisher MC, 2011. Multiple emergences of genetically diverse amphibian-infecting chytrids include a globalized hypervirulent recombinant lineage. Proceedings of the National Academy of Sciences of the United States of America, 108(46):18732-18736.

Fisher MC; Bosch J; Yin ZhiKang; Stead DA; Walker J; Selway L; Brown AJP; Walker LA; Gow NAR; Stajich JE; Garner TWJ, 2009. Proteomic and phenotypic profiling of the amphibian pathogen Batrachochytrium dendrobatidis shows that genotype is linked to virulence. Molecular Ecology, 18(3):415-429. http://www.blackwell-synergy.com/loi/mec

Fisher MC; Garner TW; Walker SF, 2009. Global emergence of Batrachochytrium dendrobatidis and amphibian chytridiomycosis in space, time, and host. Annual Review of Microbiology, 63:291-310.

Fisher MC; Garner TWJ, 2007. The relationship between the emergence of Batrachochytrium dendrobatidis, the international trade in amphibians and introduced amphibian species. Fungal Biology Reviews, 21(1):2-9. http://www.sciencedirect.com/science?_ob=MImg&_imagekey=B8G3K-4NR12N0-2-7&_cdi=41797&_user=6686535&_orig=browse&_coverDate=02%2F28%2F2007&_sk=999789998&view=c&wchp=dGLbVlW-zSkzk&md5=c10b86312aaee592fb92afc802bb9bf8&ie=/sdarticle.pdf

Forzán MJ; Gunn H; Scott P, 2008. Chytridiomycosis in an aquarium collection of frogs: diagnosis, treatment, and control. Journal of Zoo and Wildlife Medicine, 39(3):406-411.

Frías-Alvarez P; Vredenburg VT; Familiar-López M; Longcore JE; González-Bernal E; Santos-Barrera G; Zambrano L; Parra-Olea G, 2008. Chytridiomycosis survey in wild and captive Mexican amphibians. EcoHealth, 5(1):18-26. http://www.springerlink.com/content/p0g0684212137126/?p=5ae3c4890b264f18862333799e2f34b1&pi=4

Gaertner JP; Forstner MRJ; O'Donnell L; Hahn D, 2009. Detection of Batrachochytrium dendrobatidis in endemic salamander species from Central Texas. EcoHealth, 6(1):20-26. http://www.springerlink.com/content/c6273372643287g0/?p=e3dea9deafd0417f963b2806032ec3f4&pi=5

Garmyn A; Rooij P van; Pasmans F; Hellebuyck T; Broeck W van den; Haesebrouck F; Marte A, 2012. Waterfowl: Potential Environmental Reservoirs of the Chytrid Fungus Batrachochytrium dendrobatidis. PLoS ONE, 7(4):e35038.

Garner TWJ; Garcia G; Carroll B; Fisher MC, 2009. Using itraconazole to clear Batrachochytrium dendrobatidis infection, and subsequent depigmentation of Alytes muletensis tadpoles. Diseases of Aquatic Organisms, 83:257-260.

Garner TWJ; Perkins MW; Purnima Govindarajulu; Seglie D; Walker S; Cunningham AA; Fisher MC, 2006. The emerging amphibian pathogen Batrachochytrium dendrobatidis globally infects introduced populations of the North American bullfrog, Rana catesbeiana. Biology Letters, 2(3):455-459. http://www.pubs.royalsoc.ac.uk/biol_lett

Garner TWJ; Walker S; Bosch J; Hyatt AD; Cunningham AA; Fisher MC, 2005. Chytrid fungus in Europe. Emerging Infectious Diseases, 11(10):1639-1641.

Garraffo HM; Spande TF; Williams M, 2009. Epibatidine: From Frog Alkaloid to Analgesic Clinical Candidates: A Testimonial to "True Grit"!. Heterocycles,, 79:207-217.

Gewin V, 2008. Riders of a modern-day ark. PLoS Biology, 6(1):e24. http://biology.plosjournals.org/perlserv/?request=get-document&doi=10.1371%2Fjournal.pbio.0060024

Goka K; Yokoyama J; Une Y; Kuroki T; Suzuki K; Nakahara M; Kobayashi A; Inaba; S; Mizutani T; Hyatt AD, 2009. Amphibian chytridiomycosis in Japan: distribution, haplotypes and possible route of entry into Japan. Molecular Ecology, 18(23):4757-4774.

Goldberg TL; Readel AM; Lee MH, 2007. Chytrid fungus in frogs from an equatorial African montane forest in Western Uganda. Journal of Wildlife Diseases, 43(3):521-524. http://www.wildlifedisease.org

Grant EHC; Bailey LL; Ware JL; Duncan KL, 2008. Prevalence of the amphibian pathogen Batrachochytrium dendrobatidis in stream and wetland amphibians in Maryland, USA. Applied Herpetology, 5(3):233-241.

Gratwicke B; Evans MJ; Jenkins PT; Kusrini MD; Moore RD; Sevin J; Wildt DE, 2010. Is the international frog legs trade a potential vector for deadly amphibian pathogens? Frontiers in Ecology and the Environment, 8(8):438-442. http://www.esajournals.org/doi/full/10.1890/090111

Greenbaum E; Kusamba C; Aristote M; Reed KD, 2008. Amphibian chytrid fungus infections in Hyperolius (Anura: Hyperoliidae) from eastern Democratic Republic of Congo. Herpetological Review, 39:70-73.

Groff JM; Mughannam A; McDowell TS; Wong A; Dykstra MJ; Frye FL; Hedrick RP, 1991. An epizootic of cutaneous zygomycosis in cultured dwarf African clawed frogs (Hymenochirus curtipes) due to Basidiobolus ranarum. Journal of Medical and Veterinary Mycology, 29(4):215-223.

Hanekamp JC; Calabrese JC, 2007. Chloramphenicol, European Legislation and Hormesis - Commentary. Dose Response, 5(2):91-93.

Hanselmann R; Rodríguez A; Lampo M; Fajardo-Ramos L; Aguirre AA; Kilpatrick AM; Rodríguez JP; Daszak P, 2004. Presence of an emerging pathogen of amphibians in introduced bullfrogs Rana catesbeiana in Venezuela. Biological Conservation, 120(1):115-119.

Hayes MP; Jennings MR, 1986. Decline of Ranid Frog Species in Western North America: Are Bullfrogs (Rana catesbiana) Responsible? Journal of Herpetology, 20:490-509.

Heard M; Smith KF; Ripp K, 2011. Examining the evidence for chytridiomycosis in threatened amphibian species. PLoS ONE, No.August:e23150. http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0023150

Hero JM; McDonald K; Alford R; Cunningham M; Retallick R, 2004. Rheobatrachus vitellinus. IUCN Red List of Threatened Species. Version 2010.1. http://www.iucnredlist.org

Hero JM; Morrison C, 2003. Frog Declines in Australia: global implications. The Herpetological Journal, 14(4):175-186.

Herrera RA; Steciow MM; Natale GS, 2005. Chytrid fungus parasitizing the wild amphibian Leptodactylus ocellatus (Anura: Leptodactylidae) in Argentina. Diseases of Aquatic Organisms, 64(3):247-252. http://www.int-res.com/abstracts/dao/v64/n3/p247-252/

James TY; Litvintseva AP; Vilgalys R; Morgan JAT; Taylor JW; Fisher MC; Berger L; Weldon C; Preez L du; Longcore; JE, 2009. Rapid Global Expansion of the Fungal Disease Chytridiomycosis into Declining and Healthy Amphibian Populations. PLoS Pathogens, 5(5):e1000458.

Jennings WB; Bradford DF; Johnson DF, 1992. Dependence of the Garter Snake Thamnophis elegans on Amphibians in the Sierra-Nevada of California. Journal of Herpetology, 26(4):503-505.

Jin LL; Song SS; Li Qiang; Chen YH; Wang QY; Hou ST, 2009. Identification and characterisation of a novel antimicrobial polypeptide from the skin secretion of a Chinese frog (Rana chensinensis). International Journal of Antimicrobial Agents, 33(6):538-542. http://www.sciencedirect.com/science/journal/09248579

Johnson ML; Berger L; Philips L; Speare R, 2003. Fungicidal effects of chemical disinfectants, UV light, desiccation and heat on the amphibian chytrid Batrachochytrium dendrobatidis. Diseases of Aquatic Organisms, 57(3):255-260. http://www.int-res.com/abstracts/dao/v57/n3/p255-260.html

Johnson ML; Speare R, 2003. Survival of Batrachochytrium dendrobatidis in water: quarantine and disease control implications. Emerging Infectious Diseases, 9(8):922-925.

Johnson ML; Speare R, 2005. Possible modes of dissemination of the amphibian chytrid Batrachochytrium dendrobatidis in the environment. Diseases of Aquatic Organisms, 65(3):181-186. http://www.int-res.com/abstracts/dao/v65/n3/p181-186/

Kielgast J; Rödder D; Veith M; Lötters S, 2010. Widespread occurrence of the amphibian chytrid fungus in Kenya. Animal Conservation [The 6th World Congress of Herpetology, Manaus, Brazil, 7-22 August 2008.], 13(s1):36-43. http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1469-1795

Kriger KM; Hero JM, 2008. Altitudinal distribution of chytrid (Batrachochytrium dendrobatidis) infection in subtropical Australian frogs. Austral Ecology, 33(8):1022-1032. http://www.blackwell-synergy.com/loi/aec

Kriger KM; Hines HB; Hyatt AD; Boyle DG; Hero JM, 2006. Techniques for detecting chytridiomycosis in wild frogs: comparing histology with real-time Taqman PCR. Diseases of Aquatic Organisms, 71(2):141-148. http://www.int-res.com/abstracts/dao/v71/n2/p141-148/

Kriger KM; Pereoglou F; Hero JM, 2007. Latitudinal variation in the prevalence and intensity of chytrid (Batrachochytrium dendrobatidis) infection in Eastern Australia. Conservation Biology, 21(5):1280-1290.

Kupferberg SJ, 1997. Bullfrog (Rana catesbeiana) invasion of a California river: the role of larval competition. Ecology, 78(6):1736.

Kusrini MD; Skerratt LF; Garland S; Berger L; Endarwin W, 2008. Chytridiomycosis in frogs of Mount Gede Pangrango, Indonesia. Diseases of Aquatic Organisms, 82(3):187-194. http://www.int-res.com/abstracts/dao/v82/n3/p187-194/

Laurance WF, 1996. Catastrophic declines of Australian rainforest frogs: is unusual weather responsible? Biological Conservation, 77(2/3):203-212.

Lawson TD; Jones ML; Komar O; Welch AM, 2011. Prevalence of Batrachochytrium dendrobatidis in Agalychnis moreletii (Hylidae) of El Salvador and association with larval jaw sheath depigmentation. Journal of Wildlife Diseases, 47(3):544-554. http://www.jwildlifedis.org/cgi/content/full/47/3/544

Lips KR, 1998. Decline of a tropical montane amphibian fauna. Conservation Biology, 12(1):106-117.

Lips KR, 1999. Mass mortality and population declines of anurans at an upland site in western Panama. Conservation Biology, 13(1):117-125.

Lips KR; Brem F; Brenes R; Reeve JD; Alford RA; Voyles J; Carey C; Livo L; Pessier AP; Collins JP, 2006. Emerging infectious disease and the loss of biodiversity in a Neotropical amphibian community. Proceedings of the National Academy of Sciences of the United States of America, 103(9):3165-3170. http://www.pnas.org/

Lips KR; Diffendorfer J; Mendelson JR III; Sears MW, 2008. Riding the wave: reconciling the roles of disease and climate change in amphibian declines. PLoS Biology, 6(3):e72. http://biology.plosjournals.org/archive/1545-7885/6/3/pdf/10.1371_journal.pbio.0060072-S.pdf

Longcore JE; Pessier AP; Nichols DK, 1999. Batrachochytrium dendrobatidis gen. et sp. nov., a chytrid pathogenic to amphibians. Mycologia, 91(2):219-227.

Longcore JR; Longcore JE; Pessier AP; Halteman WA, 2007. Chytridiomycosis widespread in anurans of northeastern United States. Journal of Wildlife Management, 71(2):435-444. http://jwm.allentrack.net

Lowe S; Browne M; Boudjelas S; Poorter M de, 2004. 100 of the world's Worst Invasive Alien Species. A selection from the global invasive species database. 100 of the world's worst invasive alien species. A selection from the global invasive species database. Auckland, New Zealand: ISSG, 12 pp. http://issg.org/booklet.pdf

Malhotra A; Thorpe RS; Hypolite E; James A, 2007. A report on the status of the herpetofauna of the Commonwealth of Dominica, West Indies. Applied Herpetology, 4:177-194.

Marantelli G; Berger L; Speare R; Keegan L, 2004. Changes in distribution of Batrachochytrium dendrobatidis and keratin during tadpole development leading to high mortality after metamorphosis. Pacific Conservation Biology, 10:173-179.

Marca E La; Lips KR; Lötters S; Puschendorf R; Ibáñez R; Rueda-Almonacid JV; Schulte R; Marty C; Castro F; Manzanilla-Puppo J; Garcia-Perez JE; Toral E; Bolaños F; Chaves G; Pounds JA; Young B, 2005. Catastrophic population declines and extinctions in Neotropical harlequin frogs (Bufonidae: Atelopus). Biotropica, 37(2):190-201.

Martel A; Rooij P van; Vercauteren G; Baert K; Waeyenberghe L van; Debacker P; Garner TWJ; Woeltjes T; Ducatelle R; Haesebrouck F; Pasmans F, 2011. Developing a safe antifungal treatment protocol to eliminate Batrachochytrium dendrobatidis from amphibians. Medical Mycology, 49(2):143-149. http://journalsonline.tandf.co.uk/link.asp?id=101351

Mazzoni R; Cunningham AA; Daszak P; Apolo A; Perdomo E; Speranza G, 2003. Emerging pathogen of wild amphibians in frogs (Rana catesbeiana) farmed for international trade. Emerging Infectious Diseases, 9(8):995-998.

McDonald KR, 1994. Declining frog populations in the Wet Tropics. Atherton, Queensland, Australia: Conservation Strategy Branch, Queensland Department of Environment and Heritage.

McLeod DS; Sheridan JA; Jiraungkoorskul W; Khonsue W, 2008. A survey for chytrid fungus in Thai amphibians. Raffles Bulletin of Zoology, 56(1):199-204.

Mendelson JR III; Brodie ED Jr; Malone JH; Acevedo ME; Baker MA; Smatresk NJ; Campbell JA, 2004. Factors associated with the catastrophic decline of a cloudforest frog fauna in Guatemala. Revista de Biología Tropical, 52(4):991-1000. http://rbt.biologia.ucr.ac.cr/

Meyer E; Newell D; Hines H; May S; Hero JM; Clarke J; Lemckert F, 2004. Rheobatrachus silus. IUCN Red List of Threatened Species. Version 2010.1. http://www.iucnredlist.org

Morehouse EA; James TY; Ganley ARD; Vilgalys R; Berger L; Murphy PJ; Longcore JE, 2003. Multilocus sequence typing suggests the chytrid pathogen of amphibians is a recently emerged clone. Molecular Ecology, 12(2):395-403.

Morgan JAT; Vredenburg VT; Rachowicz LJ; Knapp RA; Stice MJ; Tunstall T; Bingham RE; Parker JM; Longcore JE; Moritz C; Briggs CJ; Taylor JW, 2007. Population genetics of the frog-killing fungus Batrachochytrium dendrobatidis. Proceedings of the National Academy of Sciences of the United States of America, 104(34):13845-13850. http://www.pnas.org/

Murphy PJ; St-Hilaire S; Bruer S; Corn PS; Peterson CR, 2009. Distribution and pathogenicity of Batrachochytrium dendrobatidis in boreal toads from the Grand Teton area of Western Wyoming. EcoHealth, 6(1):109-120. http://www.springerlink.com/content/e45712104538mtpk/?p=eae775bb04134f3094d680645511b316&pi=15

Muths E; Corn PS; Pessier AP; Green DE, 2003. Evidence for disease-related amphibian decline in Colorado. Biological Conservation, 110(3):357-365.

Muths E; Pilliod DS; Livo LJ, 2008. Distribution and environmental limitations of an amphibian pathogen in the Rocky Mountains, USA. Biological Conservation, 141(6):1484-1492. http://www.sciencedirect.com/science/journal/00063207

Mutschmann F; Berger L; Zwart P; Gaedicke C, 2000. Chytridiomycosis on amphibians - first report from Europe. (Chytridiomykose bei Amphibien - erstmaliger Nachweis für Europa.) Berliner und Münchener Tierärztliche Wochenschrift, 113(10):380-383.

Nair A; Daniel O; Gopalan; SV; Sanil George; Kumar KS; Merila J; Teacher AGF, 2011. Infectious disease screening of Indirana frogs from the Western Ghats biodiversity hotspot. Herpetological Review, 42(4):554-557.

Nichols DK; Lamirande EW, 2001. Successful Treatment of Chytridiomycosis. FROGLOG, 46:1.

Nichols DK; Lamirande EW; Pessier AP; Longcore JE, 2001. Experimental transmission of cutaneous chytridiomycosis in dendrobatid frogs. Journal of Wildlife Diseases, 37(1):1-11.

North S; Alford RA, 2008. Infection intensity and sampling locality affect Batrachochytrium dendrobatidis distribution among body regions on green-eyed tree frogs Litoria genimaculata. Diseases of Aquatic Organisms, 81(3):177-188. http://www.int-res.com/abstracts/dao/v81/n3/p177-188/

Ohst T; Gräser Y; Mutschmann F; Plötner J, 2011. New data about the threat to European amphibians by the skin fungus Batrachochytrium dendrobatidis. (Neue Erkentnisse zur Gefährdung europäischer Amphibien durch den Hautpilz Batrachochytrium dendrobatidis.) Zeitschrift für Feldherpetologie, 18:1-17.

OIE, 2010. Infection with Batrachochytrium dendrobatidis. In: Report of the Meeting of the OIE Aquatic Animal Health Standards Commission, Paris, France, 11-15 October 2010. Paris, France: OIE, 143-163. http://web.int/aac/eng/FDC%20reports/Oct%202010%20%28English%29

Ouellet M; Mikaelian I; Pauli BD; Rodrigue J; Green DM, 2005. Historical evidence of widespread chytrid infection in North American amphibian populations. Conservation Biology, 19(5):1431-1440. http://www.blackwell-synergy.com/servlet/useragent?func=showIssues&code=cbi

Padgett-Flohr GE; Hopkins RL, 2009. Batrachochytrium dendrobatidis, a novel pathogen approaching endemism in central California. Diseases of Aquatic Organisms, 83(1):1-9.

Parker PM, 2004. The World Market for Frogs' Legs: A 2005 Global Trade Perpective. San Diego, California, USA: ICON Group Ltd, 39 pp.

Pasmans F; Muijsers M; Maes S; Rooij P van; Brutyn M; Ducatelle R; Haesebrouck F; Martel A, 2010. Chytridiomycosis related mortality in a midwife toad (Alytes obstetricans) in Belgium. Vlaams Diergeneeskundig Tijdschrift, 79(6):460-462. HTTP://VDT.UGENT.BE

Pearl CA; Bull EL; Green DE; Bowerman J; Adams MJ; Hyatt A; Wente WH, 2007. Occurrence of the amphibian pathogen Batrachochytrium dendrobatidis in the Pacific Northwest. Journal of Herpetology, 41(1):145-149. http://www.bioone.org/perlserv/?request=get-document&doi=10.1670%2F0022-1511%282007%2941%5B145%3AOOTAPB%5D2.0.CO%3B2

Pessier AP; Nichols DK; Longcore JE; Fuller MS, 1999. Cutaneous chytridiomycosis in poison dart frogs (Dendrobates spp.) and White's tree frogs (Litoria caerulea). Journal of Veterinary Diagnostic Investigation, 11(2):194-199.

Picco AM; Collins JP, 2008. Amphibian commerce as a likely source of pathogen pollution. Conservation Biology, 22(6):1582-1589. http://www.blackwell-synergy.com/loi/cbi

Piotrowski JS; Annis SL; Longcore JE, 2004. Physiology of Batrachochytrium dendrobatidis, a chytrid pathogen of amphibians. Mycologia, 96(1):9-15.

Pounds JA; Crump ML, 1994. Amphibian Declines and Climate Disturbance - the Case of the Golden Toad and the Harlequin Frog. Conservation Biology, 82(1):72-85.

Puschendorf R; Carnaval AC; VanDerWal J; Zumbado-Ulate H; Chaves G; Bolaños F; Alford RA, 2009. Distribution models for the amphibian chytrid Batrachochytrium dendrobatidis in Costa Rica: proposing climatic refuges as a conservation tool. Diversity and Distributions, 15(3):401-408. http://www.blackwell-synergy.com/loi/ddi

Puschendorf R; Castaneda F; McCranie JR, 2006. Chytridiomycosis in wild frogs from Pico Bonito National Park, Honduras. EcoHealth, 3(3):178-181.

RACE (Risk assessment of Chytridiomycosis to European Amphibian Biodiversity), 2010. Hygiene protocol to contain the spread of Chytridiomycosis during fieldwork. RACE (Risk assessment of Chytridiomycosis to European Amphibian Biodiversity), 4 pp. https://secure.fera.defra.uk/nonnativespecies/downloadDocument.cfm?id=341

Rachowicz LJ; Hero JM; Alford RA; Taylor JW; Morgan JAT; Vredenburg VT; Collins JP; Briggs CJ, 2005. The novel and endemic pathogen hypotheses: competing explanations for the origin of emerging infectious diseases of wildlife. Conservation Biology, 19(5):1441-1448. http://www.blackwell-synergy.com/servlet/useragent?func=showIssues&code=cbi

Rachowicz LJ; Knapp RA; Morgan JAT; Stice MJ; Vredenburg VT; Parker JM; Briggs CJ, 2006. Emerging infectious disease as a proximate cause of amphibian mass mortality. Ecology, 87(7):1671-1683.

Rachowicz LJ; Vredenburg VT, 2004. Transmission of Batrachochytrium dendrobatidis within and between amphibian life stages. Diseases of Aquatic Organisms, 61(1/2):75-83. http://www.int-res.com/abstracts/dao/v61/n1-2/p75-83.html

Raffel TR; Michel PJ; Sites EW; Rohr JR, 2010. What drives chytrid infections in newt populations? Associations with substrate, temperature, and shade. EcoHealth, 7(4):526-536. http://www.springerlink.com/content/n7434645nm67216u/

Reeves MK; Green DE, 2006. Rana sylvatica (wood frog). Chytridiomycosis. Herpetological Review, 37(4):450.

Retallick RWR; McCallum H; Speare R, 2004. Endemic infection of the amphibian chytrid fungus in a frog community post-decline. PLoS Biology, 2(11):20351. http://biology.plosjournals.org/perlserv/?request=get-document&doi=10.1371%2Fjournal.pbio.0020351

Retallick RWR; Miera V, 2007. Strain differences in the amphibian chytrid Batrachochytrium dendrobatidis and non-permanent, sub-lethal effects of infection. Diseases of Aquatic Organisms, 75(3):201-207. http://www.int-res.com/abstracts/dao/v75/n3/p201-207/

Richards SJ; McDonald KR; Alford RA, 1993. Declines in populations of Australia's endemic tropical forest frogs. Pacific Conservation Biology, 1:66-77.

Rollins-Smith LA; Reinert LK; O'Leary CJ; Houston LE; Woodhams DC, 2005. Antimicrobial Peptide Defenses in Amphibian Skin. Integrative and Comparative Biology, 45(1):137-142.

Ron SR, 2005. Predicting the distribution of the amphibian pathogen Batrachochytrium dendrobatidis in the New World. Biotropica, 37(2):209-221. http://www.blackwell-synergy.com/servlet/useragent?func=showIssues&code=btp

Rothermel BB; Walls SC; Mitchell JC; Dodd CK Jr; Irwin LK; Green DE; Vazquez VM; Petranka JW; Stevenson DJ, 2008. Widespread occurrence of the amphibian chytrid fungus Batrachochytrium dendrobatidis in the southeastern USA. Diseases of Aquatic Organisms, 82(1):3-18. http://www.int-res.com/abstracts/dao/v82/n1/p3-18/

Rowley JJL; Alford RA, 2007. Behaviour of Australian rainforest stream frogs may affect the transmission of chytridiomycosis. Diseases of Aquatic Organisms, 77(1):1-9. http://www.int-res.com/abstracts/dao/v77/n1/p1-9/

Rowley JJL; Chan KinFung [Chan KFS]; Tang WingSze; Speare R; Skerratt LF; Alford RA; Cheung KaShing; Ho ChingYee; Campbell R, 2007. Survey for the amphibian chytrid Batrachochytrium dendrobatidis in Hong Kong in native amphibians and in the international amphibian trade. Diseases of Aquatic Organisms, 78(2):87-95. http://www.int-res.com/abstracts/dao/v78/n2/p87-95/

Ruiz A; Rueda-Almonacid JV, 2008. Batrachochytrium dendrobatidis and chytridiomycosis in anuran amphibians of Colombia. EcoHealth, 5(1):27-33. http://www.springerlink.com/content/y71k42v26085771n/?p=5ae3c4890b264f18862333799e2f34b1&pi=5

Ryan MJ; Lips KR; Eichholz MW, 2008. Decline and extirpation of an endangered Panamanian stream frog population (Craugastor punctariolus) due to an outbreak of chytridiomycosis. Biological Conservation, 141(6):1636-1647. http://www.sciencedirect.com/science/journal/00063207

Sánchez D; Chacón-Ortiz A; León F; Han BA; Lampo M, 2008. Widespread occurrence of an emerging pathogen in amphibian communities of the Venezuelan Andes. Biological Conservation, 141(11):2898-2905. http://www.sciencedirect.com/science/journal/00063207

Santiago R; Merino A, 2000. Amphibian declines in Ecuador: overview and first report of chytridiomycosis from South America. Froglog, 42:2-3.

Savage AE; Grismer LL; Anuar S; Onn CK; Grismer JL; Quah E; Muin MA; Ahmad N; Lenker M; Zamudio KR, 2011. First record of Batrachochytrium dendrobatidis infecting four frog families from Peninsular Malaysia. EcoHealth, 8(1):121-128. http://www.springerlink.com/content/u868817 g058752r2/

Savage AE; Zamudio KR, 2011. MHC genotypes associate with resistance to a frog-killing fungus. Proceedings of the National Academy of Sciences of the United States of America, 108(40):16705-16710. http://www.pnas.org/content/108/40/16705.full

Scalera R; Adams MJ; Galvan SK, 2008. Occurrence of Batrachochytrium dendrobatidis in amphibian populations in Denmark. Herpetological Review, 39(2):199-200.

Schlaepfer MA; Hoover C; Dodd CK, 2005. Challenges in evaluating the impact of the trade in amphibians and reptiles on wild populations. Bioscience, 55(3):256-264.

Schlaepfer MA; Sredl MJ; Rosen PC; Ryan MJ, 2007. High prevalence of Batrachochytrium dendrobatidis in wild populations of lowland leopard frogs Rana yavapaiensis in Arizona. EcoHealth, 4(4):421-427.

Schloegel LM; Ferreira CM; James TY; Hipolito M; Longcore JE; Hyatt AD; Yabsley M; Martins AMCRPF; Mazzoni R; Davies AJ; Daszak P, 2010. The North American bullfrog as a reservoir for the spread of Batrachochytrium dendrobatidis in Brazil. Animal Conservation [The 6th World Congress of Herpetology, Manaus, Brazil, 7-22 August 2008.], 13(s1):53-61. http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1469-1795

Schloegel LM; Hero J-M; Berger L; Speare R; McDonald K; Daszak P, 2006. The decline of the sharp-snouted day frog (Taudactylus acutirostris): The first documented case of extinction by infection in a free-ranging wildlife species? EcoHealth, 3:35-40.

Schloegel LM; Picco AM; Kilpatrick AM; Davies AJ; Hyatt AD; Daszak P, 2009. Magnitude of the US trade in amphibians and presence of Batrachochytrium dendrobatidis and ranavirus infection in imported North American bullfrogs (Rana catesbeiana). Biological Conservation, 142(7):1420-1426. http://www.sciencedirect.com/science/journal/00063207

Schmidt BR; Furrer S; Kwet A; Lötters S; Rödder D; Sztatecsny M; Tobler U; Zumbach S, 2009. Disinfection as a measure against the spread of chytridiomycosis in amphibians. (Desinfektion als Massnahme gegen die Verbreitung der Chytridiomykose bei Amphibien.) Zeitschrift für Feldherpetologie, Supplement 15:229-241. [Methoden der Feldherpetologie.]

Schock DM; Ruthig GR; Collins JP; Kutz SJ; Carrière S; Gau RJ; Veitch AM; Larter NC; Tate DP; Guthrie G; Allaire DG; Popko RA, 2010. Amphibian chytrid fungus and ranaviruses in the Northwest Territories, Canada. Diseases of Aquatic Organisms, 92(2/3):231-240. http://www.int-res.com/abstracts/dao/v92/n2-3/p231-240/

Scott E; VanCompernolle R; Taylor J; Oswald-Richter K; Jiang J; Youree BE; Bowie JH; Tyler MJ; Conlon JM; Wade D; Aiken C; Dermody TS; KewalRamani VN; Rollins-Smith LA; Unutmaz D, 2005. Antimicrobial Peptides from Amphibian Skin Potently Inhibit Human Immunodeficiency Virus Infection and Transfer of Virus from Dendritic Cells to T Cells. Journal of Virology, 79(18):11598-11606.

Seimon TA; Seimon A; Daszak P; Halloy SRP; Schloegel LM; Aguilar CA; Sowell P; Hyatt AD; Konecky B; Simmons JE, 2007. Upward range extension of Andean anurans and chytridiomycosis to extreme elevations in response to tropical deglaciation. Global Change Biology, 13(1):288-299. http://www3.interscience.wiley.com/cgi-bin/fulltext/117991464/HTMLSTART

Simoncelli F; Fagotti A; Dall'Olio R; Vagnetti D; Pascolini R; Rosa I di, 2005. Evidence of Batrachochytrium dendrobatidis Infection in Water Frogs of the Rana esculenta Complex in Central Italy. EcoHealth, 2:307-312.

Skerratt LF; Berger L; Speare R; Cashins S; McDonald KR; Phillott AD; Hines HB; Kenyon N, 2007. Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. EcoHealth, 4(2):125-134.

Smith KG; Lips KR; Chase JM, 2009. Selecting for extinction: nonrandom disease-associated extinction homogenizes amphibian biotas. Ecology Letters, 12(10):1069-1078.

Solís R; Lobos G; Walker SF; Fisher M; Bosch J, 2010. Presence of Batrachochytrium dendrobatidis in feral populations of Xenopus laevis in Chile. Biological Invasions, 12(6):1641-1646. http://www.springerlink.com/content/y3586004665h5215/?p=efd6e5bd37ae462e8f8ecbdcf0fb514e&pi=20

Soto-Azat C; Clarke BT; Poynton JC; Cunningham AA, 2009. Widespread historical presence of Batrachochytrium dendrobatidis in African pipid frogs. Diversity and Distributions, 16:126-131.

Spitzen-van der Sluijs A; Martel A; Wombwell E; Rooij P van; Zollinger R; Woeltjes T; Rendle M; Haesebrouck F; Pasmans F, 2011. Clinically healthy amphibians in captive collections and at pet fairs: A reservoir of Batrachochytrium dendrobatidis. Amphibia-Reptilia, 32:419-423.

Spitzen-van der Sluijs A; Zollinger R, 2010. Literature review on Batrachochytrium dendrobatidis. Nijmegen, Netherlands: Stichting RAVON, 37 pp.

Stuart SN; Chanson JS; Cox NA; Young BE; Rodrigues ASL; Fischman DL; Waller RW, 2004. Status and trends of amphibian declines and extinctions worldwide. Science, 306(5702):1783-1786.

Sztatecsny M, 2008. Chytridiomycosis in amphibians. Is Austria affected by this worldwide problem? (Chytridiomykose bei Amphibien: Ist Osterreich von diesem weltweiten Problem betroffen?) OGH-Aktuell, 21:5-7.

Sztatecsny M; Glaser F, 2011. From the eastern lowlands to the western mountains: first records of the chytrid fungus Batrachochytrium dendrobatidis in wild amphibian populations from Austria. Herpetological Journal, 21:87-90.

Tennessen JA; Woodhams DC; Chaurand P; Reinert LK; Billheimer D; Shyr Y; Caprioli RM; Blouin MS; Rollins-Smith LA, 2009. Variations in the expressed antimicrobial peptide repertoire of northern leopard frog (Rana pipiens) populations suggest intraspecies differences in resistance to pathogens. Developmental and Comparative Immunology, 33(12):1247-1257. http://www.sciencedirect.com/science/journal/0145305X

Une Y; Kadekaru S; Tamukai K; Goka K; Kuroki T, 2008. First report of spontaneous chytridiomycosis in frogs in Asia. Diseases of Aquatic Organisms, 82(2):157-160. http://www.int-res.com/articles/dao_oa/d082p157.pdf

Velo-Antón G; Rodríguez D; Savage AE; Parra-Olea G; Lips KR; Zamudio KR, 2012. Amphibian-killing fungus loses genetic diversity as it spreads across the New World. Biological Conservation, 146(1):213-218. http://www.sciencedirect.com/science/article/pii/S0006320711004666

Voyles J; Young S; Berger L; Campbell C; Voyles WF; Dinudom A; Cook D; Webb R; Alford RA; Skerratt LF; Speare R, 2009. Pathogenesis of Chytridiomycosis, a Cause of Catastrophic Amphibian Declines. Science, 326(5952):582-585.

Vredenburg VT; Knapp RA; Tunstall TS; Briggs CJ, 2010. Dynamics of an emerging disease drive large-scale amphibian population extinctions. Proceedings of the National Academy of Sciences of the United States of America, 107(21):9689-9694. http://www.pnas.org/

Walker SF; Bosch J; James TY; Litvintseva AP; Valls JAO; Piña S; García G; Rosa GA; Cunningham AA; Hole S; Griffiths R; Fisher MC, 2008. Invasive pathogens threaten species recovery programs. Current Biology, 18(18):R853-R854. http://www.current-biology.com

Warkentin IG; Bickford D; Sodhi NS; Bradshaw CJA, 2009. Eating Frogs to Extinction. Conservation Biology, 23(4):1056-1059.

Webb R; Mendez D; Berger L; Speare R, 2007. Additional disinfectants effective against the amphibian chytrid fungus Batrachochytrium dendrobatidis. Diseases of Aquatic Organisms, 74(1):13-16. http://www.int-res.com/abstracts/dao/v74/n1/p13-16/

Weldon C; Preez L du; Vences M, 2008. Lack of detection of the amphibian chytrid fungus (Batrachochytrium dendrobatidis) in Madagascar. In: A conservation strategy for the amphibians of Madagascar [ed. by Andreone, F.]. Torino, Italy: Museo Regionale di Scienze Naturali di Torino, 95-106. [Monografie de Museo Regionale di Scienze Naturali di Torino, XLV.]

Weldon C; Preez LH du; Hyatt AD; Muller R; Speare R, 2004. Origin of the amphibian chytrid fungus. Emerging Infectious Diseases, 10(12):2100-2105.

Weldon C; Villiers AL de; Preez LH du, 2007. Quantification of the trade in Xenopus laevis from South Africa, with implications for biodiversity conservation. African Journal of Herpetology, 56(1):77-83.

Whiles MR; Lips KR; Pringle CM; Kilham SS; Bixby RJ; Brenes R; Connelly S; Colon-Gaud JC; Hunte-Brown M; Huryn AD; Montgomery C; Peterson S, 2006. The effects of amphibian population declines on the structure and function of Neotropical stream ecosystems. Frontiers in Ecology and the Environment, 4(1):27-34.

Wollenberg KC; Jenkins RKB; Randrianavelona R; Ralisata M; Rampilamanana R; Ramanandraibe A; Ravoahangimalala OR; Vences M, 2010. Raising awareness of amphibian chytridiomycosis will not alienate ecotourists visiting Madagascar. EcoHealth, 7(2):248-251. http://www.springerlink.com/content/av16541053109107/

Wongtavatchai J; McLean JG; Ramos F; Arnold D, 2009. Chloramphenicol. World Health Organization. [WHO Food Additives Series: 53.] http://www.inchem.org/documents/jecfa/jecmono/v53je03

Wood LR; Griffiths RA; Schley L, 2009. Amphibian chytridiomycosis in Luxembourg. Bulletin de la Société des naturalistes luxembourgeois, 110:109-114.

Woodhams DC; Alford RA, 2005. Ecology of chytridiomycosis in rainforest stream frog assemblages of tropical Queensland. Conservation Biology, 19(5):1449-1459. http://www.blackwell-synergy.com/servlet/useragent?func=showIssues&code=cbi

Woodhams DC; Alford RA; Marantelli G, 2008. Emerging disease of amphibians cured by elevated body temperature. Diseases of Aquatic Organisms, 55(1):65-67.

Woodhams DC; Ardipradja K; Alford RA; Marantelli G; Reinert LK; Rollins-Smith LA, 2007. Resistance to chytridiomycosis varies among amphibian species and is correlated with skin peptide defenses. Animal Conservation, 10(4):409-417. http://www.blackwell-synergy.com/doi/pdf/10.1111/j.1469-1795.2007.00130.x

Woodhams DC; Kilburn VL; Reinert LK; Voyles J; Medina D; Ibáñez R; Hyatt AD; Boyle DG; Pask JD; Green DM; Rollins-Smith LA, 2008. Chytridiomycosis and amphibian population declines continue to spread eastward in Panama. EcoHealth, 5(3):268-274. http://www.springerlink.com/content/u6l4775128852478/?p=49bbc10b47854c998770743b9d60a9ea&pi=5

Woodhams DC; Rollins-Smith LA; Alford RA; Simon MA; Harris RN, 2007. Innate immune defenses of amphibian skin: antimicrobial peptides and more. Animal Conservation, 10:425-428.

Woodhams DC; Voyles J; Lips KR; Carey C; Rollins-Smith LA, 2006. Predicted disease susceptibility in a Panamanian amphibian assemblage based on skin peptide defenses. Journal of Wildlife Diseases, 42(2):207-218. http://www.wildlifedisease.org

Yang HyoJin; Baek HaeJun; Speare R; Webb R; Park SunKyung; Kim TaeHo; Lasater KC; Shin SangPhil; Son SangHo; Park JaeHak; Min MiSook; Kim YoungJun; Na KiJeong; Lee Hang; Park SeChang, 2009. First detection of the amphibian chytrid fungus Batrachochytrium dendrobatidis in free-ranging populations of amphibians on mainland Asia: survey in South Korea. Diseases of Aquatic Organisms, 86(1):9-13. http://www.int-res.com/abstracts/dao/v86/n1/p9-13/

Zeng ZhaoHui; Bai ShiZhuo; Zhu YunQi; Wang XiaoLong, 2011. Genetic differentiation of the pathogen of Batrachochytrium dendrobatidis in toads. Journal of Economic Animal, 15(3):160-163. http://jdxb.jlau.edu.cn

Links to Websites

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WebsiteURLComment
AmphibiaWebhttp://amphibiaweb.org/
Bd-Mapshttp://www.spatialepidemiology.net/bd/
OIE Aquatic Animal Health Codehttp://www.oie.int/fileadmin/Home/eng/Health_standards/aahc/2010/en_sommaire.htmThe aim of the Aquatic Animal Health Code is to assure the sanitary safety of international trade in aquatic animals (fish, molluscs and crustaceans) and their products.
Pet Industry Joint Advisory Council Bd-Free 'Phibs Campaignhttp://www.pijac.org/projects/project.asp?p=26

Organizations

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World: OIE (World Organisation for Animal Health), 12, rue de Prony, 75017 Paris, France, http://www.oie.int/

USA: EcoHealth Alliance, 460 West 34th Street, 17th Floor, New York NY 10001-2320, www.ecohealthalliance.org

USA: PARC - Partners in Amphibian and Reptile Conservation, www.parcplace.org

Contributors

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25/05/10 Original text by:

Lisa Schloegel, EcoHealth Alliance 460 West 34th Street, 17th floor, New York, NY 10001, USA

Peter Daszak, Wildlife Trust, USA

Distribution Maps

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