Chytridiomycosis

International Common Names

• English: Bd disease

Local Common Names

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

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.

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).

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.

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).

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.

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).