Pathogens rarely cause extinctions of host species, and there are few examples of a pathogen changing species richness and diversity of an ecological community by causing local extinctions across a wide range of species. We report the link between the rapid appearance of a pathogenic chytrid fungus Batrachochytrium dendrobatidis in an amphibian community at El Cope, Panama, and subsequent mass mortality and loss of amphibian biodiversity across eight families of frogs and salamanders. We describe an outbreak of chytridiomycosis in Panama and argue that this infectious disease has played an important role in amphibian population declines. The high virulence and large number of potential hosts of this emerging infectious disease threaten global amphibian diversity.

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Emerging infectious disease and the loss of biodiversity in a Neotropical amphibian community

The global emergence and spread of the pathogenic, virulent, and highly transmissible fungus Batrachochytrium dendrobatidis, resulting in the disease chytridiomycosis, has caused the decline or extinction of up to about 200 species of frogs. Key postulates for this theory have been completely or partially fulfilled. In the absence of supportive evidence for alternative theories despite decades of research, it is important for the scientific community and conservation agencies to recognize and manage the threat of chytridiomycosis to remaining species of frogs, especially those that are naive to the pathogen. The impact of chytridiomycosis on frogs is the most spectacular loss of vertebrate biodiversity due to disease in recorded history.

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Spread of Chytridiomycosis Has Caused the Rapid Global Decline and Extinction of Frogs

Batrachochytrium dendrobatidis is a major pathogen of frogs worldwide, associated with declines in amphibian populations. Diagnosis of chytridiomycosis to date has largely relied upon histological and immunohistochemical examination of toe clips. This technique is invasive and insensitive particularly at early stages of infection when treatment may be possible. We have developed a real-time PCR Taqman assay that can accurately detect and quantify one zoospore in a diagnostic sample. This assay will assist the early detection of B. dendrobatidis in both captive and wild populations, with a high degree of sensitivity and specificity, thus facilitating treatment and protection of endangered populations, monitoring of pristine environments and preventing further global spread via amphibian trade.

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Rapid quantitative detection of chytridiomycosis (Batrachochytrium dendrobatidis) in amphibian samples using real-time Taqman PCR assay.

Batrachochytrium dendrobatidis is a fungus belonging to the Phylum Chytridiomycota, Class Chytridiomycetes, Order Chytridiales, and is the highly infectious aetiological agent responsible for a potentially fatal disease, chytridiomycosis, which is currently decimating many of the world's amphibian populations. The fungus infects 2 amphibian orders (Anura and Caudata), 14 families and at least 200 species and is responsible for at least 1 species extinction. Whilst the origin of the agent and routes of transmission are being debated, it has been recognised that successful management of the disease will require effective sampling regimes and detection assays. We have developed a range of unique sampling protocols together with diagnostic assays for the detection of B. dendrobatidis in both living and deceased tadpoles and adults. Here, we formally present our data and discuss them in respect to assay sensitivity, specificity, repeatability and reproducibility. We suggest that compliance with the recommended protocols will avoid the generation of spurious results, thereby providing the international scientific and regulatory community with a set of validated procedures which will assist in the successful management of chytridiomycosis in the future.

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Diagnostic assays and sampling protocols for the detection of Batrachochytrium dendrobatidis

Batrachochytrium dendrobatidis (Bd ) is a chytrid fungus that causes chytridiomycosis in amphibians. Only named in 1999, Bd is a proximate driver of declines in global amphibian biodiversity. The pathogen infects over 350 species of amphibians and is found on all continents except Antarctica. However, the processes that have led to the global distribution of Bd and the occurrence of chytridiomycosis remain unclear. This review explores the molecular, epidemiological, and ecological evidence that Bd evolved from an endemic ancestral lineage to achieve global prominence via anthropogenically mediated spread. We then consider the major host and pathogen factors that have led to the occurrence of chytridiomycosis in amphibian species, populations, and communities.

Global emergence of Batrachochytrium dendrobatidis and amphibian chytridiomycosis in space, time, and host.

The efficacy of a number of disinfection treatments was tested on in vitro cultures of the fungus Batrachochytrium dendrobatidis, the causative agent of chytridiomycosis in amphibians The aim was to evaluate the fungicidal effects of chemical disinfectants, sterilising ultraviolet (UV) light, heat and desiccation, using methods that were feasible for either disinfection in the field, in amphibian
husbandry or in the laboratory The chemical disinfectants tested were: sodium chloride, household bleach (active ingredient: sodium hypochlorite), potassium permanganate, formaldehyde solution, Path-XTM agricultural disinfectant (active ingredient: didecyl dimethyl ammonium chloride,
DDAC), quaternary ammonium compound 128 (DDAC), Dithane, Virkon, ethanol and benzalkonium chloride In 2 series of experiments using separate isolates of B dendrobatidis, the fungicidal effect was evaluated for various time periods and at a range of chemical concentrations The end point measured was death of 100% of zoospores and zoosporangia Nearly all chemical disinfectants resulted
in 100% mortality for at least one of the concentrations tested However, concentration and time of exposure was critical for most chemicals Exposure to 70% ethanol, 1 mg Virkon ml–1 or 1 mg benzalkonium chloride ml–1 resulted in death of all zoosporangia after 20 s The most effective products for field use were Path-XTM and the quaternary ammonium compound 128, which can be used at dilutions
containing low levels (eg 0012 or 0008%, respectively) of the active compound didecyl dimethyl ammonium chloride Bleach, containing the active ingredient sodium hypochlorite, was effective at concentrations of 1% sodium hypochlorite and above Cultures did not survive complete
drying, which occurred after <3 h at room temperature B dendrobatidis was sensitive to heating, and within 4 h at 37°C, 30 min at 47°C and 5 min at 60°C, 100% mortality occurred UV light (at 1000 mW m–2 with a wavelength of 254 nm) was ineffective at killing B dendrobatidis in culture

https://researchonline.jcu.edu.au/6203/1/6203_Johnson_et_al_2003.pdf

Fungicidal effects of chemical disinfectants, UV light, desiccation and heat on the amphibian chytrid, Batrachochytrium dendrobatidis

Amphibian chytridiomycosis is an emerging infectious disease of amphibians thought to be moved between countries by trade in infected amphibians. The causative fungus, Batrachochytrium dendrobatidis, produces aquatic, motile zoospores; infections have been achieved in experiments by exposing amphibians to water containing zoospores. However, the ability of this fungus to survive in the environment in the absence of an amphibian host is unknown. We show that B. dendrobatidis will survive in tap water and in deionized water for 3 and 4 weeks, respectively. In lake water, infectivity was observed for 7 weeks after introduction. The knowledge that water can remain infective for up to 7 weeks is important for the formulation of disease control and quarantine strategies for the management of water that has been in contact with amphibians.

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Survival of Batrachochytrium dendrobatidis in water: quarantine and disease control implications.

Life-history trade-offs allow many animals to maintain reproductive fitness across a range of climatic conditions. When used by parasites and pathogens, these strategies may influence patterns of disease in changing climates. The chytrid fungus, Batrachochytrium dendrobatidis, is linked to global declines of amphibian populations. Short-term growth in culture is maximal at 17°–25°C. This has been used in an argument that global warming, which increases the time that amphibians spend at these temperatures in cloud-covered montane environments, has led to extinctions. Here we show that the amphibian chytrid responds to decreasing temperatures with trade-offs that increase fecundity as maturation rate slows and increase infectivity as growth decreases. At 17°–25°C, infectious zoospores encyst (settle and develop a cell wall) and develop into the zoospore-producing stage (zoosporangium) faster, while at 7°–10°C, greater numbers of zoospores are produced per zoosporangium; these remain infectious for a longer period of time. We modeled the population growth of B. dendrobatidis through time at various temperatures using delayed differential equations and observational data for four parameters: developmental rate of thalli, fecundity, rate of zoospore encystment, and rate of zoospore survival. From the models, it is clear that life-history trade-offs allow B. dendrobatidis to maintain a relatively high long-term growth rate at low temperatures, so that it maintains high fitness across a range of temperatures. When a seven-day cold shock is simulated, the outcome is intermediate between the two constant temperature regimes, and in culture, a sudden drop in temperature induces zoospore release. These trade-offs can be ecologically important for a variety of organisms with complex life histories, including pathogenic microorganisms. The effect of temperature on amphibian mortality will depend on the interaction between fungal growth and host immune function and will be modified by host ecology, behavior, and life history. These results demonstrate that B. dendrobatidis populations can grow at high rates across a broad range of environmental temperatures and help to explain why it is so successful in cold montane environments.

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Life-history trade-offs influence disease in changing climates: strategies of an amphibian pathogen

Amphibian chytridiomycosis caused by Batrachochytrium dendrobatidis has spread at an alarming rate over large distances throughout sensitive frog populations in eastern Australia, Central America and New Zealand. Infected amphibians and contaminated water are implicated in translocation, but other vectors are unknown. Through in vitro studies we show that potential means of translocation may be moist soil and bird feathers. B. dendrobatidis survived for up to 3 mo in sterile, moist river sand with no other nutrients added. B. dendrobatidis attached to and grew on sterile feathers and were able to be transported by feathers to establish new cultures in media, surviving between 1 and 3 h of drying between transfers. If these in vitro results are valid in the natural environment, the findings raise the possibilities that B. dendrobatidis may be translocated by movement of moist river sand and that birds may carry the amphibian chytrid between frog habitats. However, further studies using sand and feathers containing normal microflora are essential.

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Megan L. Johnson

Papers

Fungicidal effects of chemical disinfectants, UV light, desiccation and heat on the amphibian chytrid, Batrachochytrium dendrobatidis

Survival of Batrachochytrium dendrobatidis in water: quarantine and disease control implications.

Life-history trade-offs influence disease in changing climates: strategies of an amphibian pathogen

Possible modes of dissemination of the amphibian chytrid Batrachochytrium dendrobatidis in the environment