Amphibian Chytridiomycosis and Emerging Infectious Diseases of Wildlife

Daszak, P.¹, Cunningham, A.A.² & Hyatt, A.D.³

¹Institute of Ecology, University of Georgia, Athens GA 30602, USA; ²Institute of Zoology, Zoological Society of London, Regent’s Park, London NW1 4RY, U.K.; ³Australian Animal Health Laboratory, CSIRO, Private Bag 24, Geelong, Victoria 3220, Australia.

This conference is dedicated to the diseases of amphibians and reptiles - diseases that have often been neglected and about which there is still much to learn. It is therefore fitting that we begin by focusing on amphibian chytridiomycosis, a panzootic emerging disease described in 1998 that has already achieved notoriety due to its association with the global phenomenon of amphibian population declines.

Over the past three decades, amphibian population declines have been reported in North, Central and South America, Europe, India and Australia¹. In most areas habitat loss is probably the major cause, although a range of other hypotheses have been proposed. A series of catastrophic declines in relatively undisturbed regions, however, has remained a mystery until recently. At these sites, notably in the montane rain forests of Australia and Central America, multiple species assemblages of amphibians have disappeared within a short time period and a number of global (species) extinctions are thought to have occurred. These include the extinction of the golden toad (Bufo periglenes) of Costa Rica and two species of gastric brooding frogs (Rheobatrachus) of Australia - species only discovered in the last half of the 20^th century. It is only within the past three years that detailed investigations have shed light on the underlying cause of many of these declines: a fungal disease of amphibians known as chytridiomycosis.

Amphibian chytridiomycosis was first described from carcasses collected by wildlife biologists at sites of mass mortality in the montane rain forests of Australia, Costa Rica and Panama^1,2. Initial diagnosis proved difficult - occasional abnormal epidermal sloughing and ulceration, or hemorrhage in the skin were the only gross lesions encountered and these were rare (Fig. 1). A range of standard parasitologic, bacteriologic, mycologic and virologic examinations revealed no significant known amphibian pathogens. However, skin smears and histologic sections contained large numbers of spherical to ovoid bodies resembling protozoan cysts (Fig. 2). Repeated findings of these parasites as more sick and dying frogs were investigated implied they were of significance. The flask-like morphology suggested a fungal infection, but poor preservation of carcasses hampered identification. Eventually, transmission electron microscopy of freshly fixed carcasses allowed a firm identification of the causative agent - a non-hyphal chytrid fungus (Phylum Chytridiomycota). This was supported by 18s rDNA sequence data. A simple transmission experiment confirmed this as the etiologic agent. Simultaneously, a group at the National Zoo, Washington identified chytridiomycosis as the cause of death in captive amphibians³. The agent was subsequently cultured, described as Batrachochytrium dendrobatidis and Koch’s postulates proven⁴.

Fig. 1. Carcass of an Australian amphibian (Myxophyes fasciolatus) that died from cutaneous chytridiomycosis. This individual died in a mass mortality event in a captive collection. No obvious gross lesions are visible and the animal showed no signs of emaciation.

Fig. 2. Toluidine blue-stained plastic section through the toe skin of an amphibian infected with chytridiomycosis (distal aspect on the right). Numerous vacuoles are visible within the keratinized cells of the epidermis. Some of these contain thin walls (septa) – a common characteristic of developing Batrachochytrium sporangia. Other cells contain fully-developed, flask-shaped sporangia.

We now know that chytridiomycosis has a wide host range including urodeles, aquatic amphibians such as Xenopus, terrestrial and semi-terrestrial frogs and toads^5,6. The disease is present in North America, causing mass mortalities and population declines in a range of ranid and bufonid species, notably Rana yavapaiensis, R. chiricahuensis, Bufo boreas and B. canorus. Analysis of museum specimens suggests it was also involved in die-offs of some North American ranids and bufonids in the 1970s and 1980s⁵. Chytridiomycosis has recently been reported in South America, Europe, New Zealand and Western Australia, often associated with marked population declines. In Western Australia, a large retrospective survey suggests introduction of the disease from an eastern focus⁶.

It is becoming increasingly clear that the presence of chytridiomycosis in an amphibian population may have a range of outcomes. For example, chytridiomycosis can be fatal to White’s tree frog, Litoria caerulea, but populations of this species appear to be stable. In contrast, montane rainforest Litoria species (e.g. L. nannotis) have undergone catastrophic declines. It appears that a combination of host factors (niche specialism, low fecundity) and pathogen factors (preferred cool developmental temperature) may predispose some montane species to an increased impact (Fig. 3). Other biological characteristics, such as the ability to survive outside the adult amphibian host as a saprobe or in larval mouthparts, suggest persistence, and may explain how this disease can cause local host extinctions⁵.

Fig. 3. A population pyramid to demonstrate the factors thought to heighten the impact of chytridiomycosis in amphibian populations. On the left hand side, host ecological constraints that predispose some populations to mass mortality and declines are listed. On the right hand side, characteristics of Batrachochytrium that are likely to enhance it’s ability to persist and cause declines are listed. The low preferred developmental temperature of Batrachochytrium may explain the severe declines within montane populations of amphibians. Note that the relative number of events is likely to decrease with increasing severity of impact, reflecting a large number of populations that are probably able to survive despite the presence of chytridiomycosis

Chytridiomycosis is one of a number of emerging infectious diseases (EIDs) that represent a significant threat to wildlife⁷. Diseases are termed emerging if they have recently increased in incidence or geographic range, recently moved into new host populations, recently been discovered or are caused by recently evolved pathogens. Using these criteria, a group of wildlife EIDs can be identified, including phocine distemper, a range of coral diseases, rabies in African wild dogs, elephant herpesvirus disease, BSE in zoo animals and many others. Most of the EIDs affecting humans are driven to emerge by changes in host-parasite ecology reflecting human demographic or biocultural changes, e.g. increased global travel leading to rapid dissemination of pathogens. This is mirrored closely for wildlife EIDs, the emergence of which is mostly driven similar anthropogenic factors, e.g. global transport of animals and their products leading to disease introduction (termed "pathogen pollution"). The implications of these wildlife EIDs are twofold: first, wildlife EIDs are a threat to biodiversity conservation due to their involvement in local and species extinctions; second, because we share pathogens, habitat and environmental changes with wildlife, we may be driving the emergence of zoonotic diseases that threaten human health⁷.

Amphibian chytridiomycosis fits the criteria of an emerging disease of wildlife: it is newly discovered, has recently expanded in geographic range and increased in incidence. As yet, the cause of its relatively synchronous appearance in Australia and the Americas is unknown. Two hypotheses have some supporting data: first, that the causative agent has been introduced either locally or globally from enzootic foci into naive populations (this may explain the catastrophic mortality, the wave-like spread of declines and its wide host range); second, that global warming has changed the behaviour of montane rainforest amphibians, resulting in increased transmission rates. Whatever the underlying cause, the significance of chytridiomycosis is clear. This is the first wildlife disease to emerge on a global scale that affects an entire class of vertebrates and is associated with mass mortalities, population declines and species extinctions. The repeated finding of this disease in wild populations and in captivity, and the recognition that it may have been responsible for previous die-offs, reminds us how much remains to be discovered within amphibian and reptile veterinary medicine.

References

1. Declines and Disappearances of Australian Frogs. Environment Australia. Available in free, downloadable format from: http://www.biodiversity.environment.gov.au/threaten/information/frogs/frogs.pdf

2. Berger, L. et al. (1998). Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. Proc. Natl. Acad. Sci., USA 95: 9031-9036.

3. Pessier A.P., Nichols D.K., Longcore J.E. & Fuller M.S (1999). Cutaneous chytridiomycosis in poison dart frogs (Dendrobates spp.) and White’s tree frogs (Litoria caerulea). J. Vet. Diagnost. Invest. 11: 194-199.

4. Longcore J.E., Pessier A.P. & Nichols D.K. (1999).Batrachochytrium dendrobatidis gen. et sp. nov., a chytrid pathogenic to amphibians Mycologia 91: 219-227.

5. Daszak P., Berger L., Cunningham A.A., Hyatt A.D., Green D.E. & Speare, R. (1999). Emerging infectious diseases and amphibian population declines. Emerg. Infect. Dis. 5: 735-748 http://www.cdc.gov/ncidod/eid/vol5no6/daszak.htm

6. Global chytridiomycosis distribution. Webpage on the amphibian diseases homepage (James Cook University, Australia). http://www.jcu.edu.au/school/phtm/PHTM/frogs/chyglob.htm

7. Daszak P., Cunningham A.A. & Hyatt A.D. (2000). Emerging infectious diseases of wildlife- threats to biodiversity and human health. Science 287: 443-449

Related links

1) Amphibian Diseases Homepage (Ed. Rick Speare, James Cook University, Australia).
http://www.jcu.edu.au/dept/PHTM/frogs/ampdis.htm

2) Declining Amphibian Populations Taskforce of the IUCN
http://www.open.ac.uk/OU/Academic/Biology/J_Baker/JBtxt.htm

3) US Government inter-agency Taskforce on Amphibian Declines and Deformities (TADD)
http://www.frogweb.gov/tadd/index.html

4) Declines and Disappearances of Australian Frogs. Book published by Environment Australia. Available in pdf format from:
http://www.biodiversity.environment.gov.au/threaten/information/frogs/frogs.pdf

5) Getting the Jump! on Amphibian Diseases. Conference held in Cairns, Australia, 26-30th August, 2000:
http://www.jcu.edu.au/school/phtm/PHTM/frogs/gjoad.htm

This Page Last Updated October 16, 2000

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