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...
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.
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.
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 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.
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.
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).
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.
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).
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.
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.
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.
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The 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 Campaign
