Chytridiomycosis due to the amphibian chytrid fungus

1. Name and description of the threatening process

Name

'Chytridiomycosis due to the amphibian chytrid fungus'

The nominated name does not represent a process. The threat described is the impact due to amphibians being infected with chytrid fungus resulting in the disease chytridiomycosis. TSSC therefore recommend the threatening process be re-named:

'Infection of amphibians with chytrid fungus resulting in chytridiomycosis'

Description

The following description is based on that provided in the nomination:

Chytridiomycosis is an infectious disease affecting amphibians worldwide. The disease has been recorded in four regions of Australia- east coast, southwest Western Australia, Adelaide and central Kimberley. Chytridiomycosis is caused by the amphibian chytrid fungus, Batrachochytrium dendrobatidis. This is a highly virulent fungal pathogen of amphibians capable at the minimum of causing sporadic deaths in some populations, and 100% mortality in other populations. Surviving individuals are believed to be carriers. The inoculating dose is low, 100 zoospores able to cause clinical chytridiomycosis within 4 weeks. Some species appear highly susceptible to developing the disease, progressing to death, while other species appear less susceptible to disease manifestations.

Many attributes of the fungus and the disease in the wild are unknown, including reasons for death of hosts, survival of the fungus in the absence of amphibian populations, methods of transmission and spread, and place/s and time of origin. There is no known treatment once the fungus is contracted. It appears fungus zoospores are contracted through contact with water when released from infected frogs. Interaction between the fungus and environmental factors, such as temperature and stress, do vary the impact of the disease. The disease was first identified in 1998.

It is not currently known whether the fungus is exotic or native to Australia, and experts differ in their opinion on the likelihood of the fungus being a novel pathogen. This uncertainty is based on: limited sampling previous to the first detections; limited sampling in areas without noticeable frog declines; the unknown relationship of chytrid strains worldwide; and the possibility that other factors have triggered expression of the disease.

In Australia, Panama and NZ the fungus is thought to have 'appeared' suddenly and expanded its range. However, the initial prospective and retrospective searching has concentrated on areas with amphibian declines, and without similar searching in areas without amphibian declines, a sampling bias is possible. It is also possible that the fungus could have been present at low levels or low intensity in infected frogs, before the declines occurred. Thorough testing is difficult due to the earliest declines occurring 20 years prior to the disease and fungus being discovered, and the limited number of testable museum specimens from many areas. However, as the intensity of retrospective searching has increased, there is increasing evidence of sudden arrival and expansion. In addition, preliminary studies in Australia and the USA to date support the conclusion that fungus isolates belong to a single closely-related population, in favour of the hypothesis that the fungus is a newly emerged, exotic agent.

The alternate possibility is that the fungus is a natural infective agent, which has recently emerged as an infectious disease due to: 1) increased virulence; 2) increased prevalence in the environment; or 3) reduced resistance to infection in host populations. All these possibilities could potentially be caused by other factors, such as environmental changes or as yet undetected co-infections. Interactions between the host, the environment and the fungus are known to be important. This is demonstrated by the most severe declines being recorded in upland amphibian populations (both in Australia and Panama). The exact nature of this interaction is uncertain. The nomination asserts that in host populations of poikilotherms exposed to virulent pathogens, increases in stressful environmental conditions (such as lower temperatures) often result in increases in morbidity and mortality.

It has been suggested that if an environmental factor is critical, that factor should be the threatening process, rather than the disease. It can also be argued that all diseases represent the outcome of a complex nexus of interactions between pathogen, host and environment, and that, regardless of the impact of a disease being mediated by environmental conditions, the disease remains the proximate cause of morbidity and death.

The TSSC believes that, as the disease itself is the proximate cause of any impact on amphibian species, the threatening process to be assessed against the criteria for listing should be 'Infection of amphibians with chytrid fungus resulting in chytridiomycosis'.

2. How judged by TSSC in relation to the Environment Protection and Biodiversity Conservation Act 1999 criteria

Section 188(4) of the Environment Protection and Biodiversity Conservation Act 1999 states:

A threatening process is eligible to be treated as a key threatening process if:

1. it could cause a native species or an ecological community to become eligible for listing in any category, other than conservation dependent; or
2. it could cause a listed threatened species or a listed threatened ecological community to become eligible to be listed in another category representing a higher degree of endangerment; or
3. it adversely affects 2 or more listed threatened species (other than conservation dependent species) or 2 or more listed threatened ecological communities.

The Action Plan for Australian Frogs was completed in April 1997, before discovery of the disease. It states that dramatic declines in some Australian frog species have been reported since the 1980s, and, although some declines can be associated with changes to habitat, pollution and predation, for most species (24 of the 27 included) the cause of decline is unknown. Disease was speculated as a possible cause of decline in 10 species.

Many of the experts consulted by the TSSC commented that the process meets all criteria and is eligible for listing. Relevant general comments (not related to specific criteria) include:

• it is likely the fungus has been a proximal cause of decline and disappearance in a number of species, and many unusual and restricted species are at threat;
• evidence to date suggests the fungus is the proximate cause of death in recently declined species;
• although the nomination contains a number of inferences/extrapolations not yet supported by rigorous testing, there is overwhelming circumstantial evidence it is a key threatening process;
• there is considerable evidence, overwhelming circumstantial evidence, and increasing acceptance in the scientific community that the disease is responsible for amphibian declines;
• the disease is a key factor in extinction or decline of many frog species in the past 2-3 decades;
• the disease is a major threat to Australian amphibians;
• it is highly probable that frog mortality, under optimum conditions of pathogenic impact, might reach near absolute levels (i.e. chance of survival close to zero);
• whether native or introduced, the disease poses a serious threat to amphibians, with the potential to decimate susceptible populations and species; and
• the disease has had a dramatic effect on frog populations in many parts of Australia, and has the potential to cause major population declines and extinctions if not checked.

Contrasting comments include that the process is not eligible as cause and effect is not demonstrated, unless as association between death and declines and the presence of the fungus is adequate.

A. Could the threatening process cause a native species or an ecological community to become eligible for listing in any category, other than conservation dependant?

The nomination does not provide a list of species, which could become eligible for listing due to the process, asserting that:

• as the fungus appears capable of infecting any amphibians, and causing death of individuals of most species, and population declines and loss of populations in some species, it has the potential to cause many species to change status;
• some species appear more likely to die once infected, due to innate characteristics of the species and/or environmental factors;
• predicting which species are liable to severe impacts is difficult - reports indicate stream associated species in high elevations appear most susceptible, however, the disease also occurs in arid zone amphibians and across a wide range of other habitats; and
• species most likely to become listed due to the process are those in currently chytrid-free zones, particularly those at risk from expansion from current zones: Tasmania, Cape York Peninsula and the Gulf Country in Queensland, northwest Western Australia, the Northern Territory and central Australia.

Many experts state there is considerable evidence and/or circumstantial evidence that the disease has caused significant declines in amphibian populations, including Endangered species once regarded as common/secure. A further issue raised is that, regardless of whether the pathogen is new to Australia or has been triggered by environmental factors, the full impact of infections may not be seen in widespread, abundant species for several decades after the fungus has become endemic in these populations.

The fungus is proven as a cause of morbidity and death in a number of Australian frogs. This has been demonstrated in three WA species: Litoria moorei, Limnodynastes dorsalis and Heleioporus eyrei.However, although deaths may occur, not all species are impacted at the population level:

• for some southwest WA species there is no data showing significant declines despite the disease being actively expressed for at least 15 years - Geocrinia vitellina has maintained its status (Vulnerable) over that time, and L. moorei is still widespread;
• the population of L. genimaculata at Big Tableland suffered a sudden decline at the same time Taudactylus acutirostris disappeared (see below), however, the L. genimaculata recovered close to former numbers after 2.5 years, though occasional individuals are found ill or dying from the disease.

The nomination includes 30 currently unlisted species known to have infected populations. Updated information indicates there is now evidence of infection (museum and field data) for a further 6 species. Of these species the nomination only provides information on status for Adelotus brevis. In addition, three are currently included in State/Territory threatened species lists (all in Qld): L. pearsoniana; L. genimaculata; and Lechriodus fletcheri.

Adelotus brevis has had declines over much of its range, particularly upland populations, and the 'Nandewar and New England Tablelands Bioregions population' was recently listed as Endangered in NSW. The species as a whole is not currently listed as threatened in the two States where it occurs (NSW and Qld). The listed population is likely to be reduced to a critical level, if it is not already extinct. The listing determination mentions chytrid as a potential cause of decline, but also includes clearing, habitat modification and predation by introduced fish as possible threats.

L. pearsoniana occurs in south-eastern Qld and northern NSW. The fungus has been recorded in this species in NSW and Qld. In NSW it is not listed and there are no reports of declines. In Qld it is listed as Endangered, with declines recorded in the late 1970s through to the early 1990s. The Draft National recovery plan for mid-east Australian stream-dependant frogs 2000-2005 states that while recent studies have found the species to be reasonably widespread with recovery at some sites, at other sites where seemingly suitable habitat exists they are at low densities.

L. genimaculata only occurs in Qld and is listed there as Rare. As described above one population in which deaths due to the disease were recorded recovered close to former numbers, even though occasional individuals are still found ill or dying from the disease. There is currently no information on the degree of impact of the disease in other populations of this species.

Lechriodus fletcheri occurs in northern NSW and south-eastern Qld, with the greater part of the range in NSW. It is listed as Rare in Qld, and the disease has been recorded in this species at a Qld site. There is no information on the impact of the disease in populations of this species.

Given the potential for chytridiomycosis outbreaks to result in sudden decline and/or extinction of populations, many unlisted species which have already undergone some declines, or occur in a restricted number of small populations, could become eligible for listing due to this process - examples include Adelotus brevis and Litoria pearsoniana.

In addition to species not currently listed, the nomination asserts the process has already resulted in seven species being listed as Endangered, by causing sudden population declines:Taudactylus acutirostris, Litoria nyakalensis, L. lorica, L. nannotis, L. rheocola, Nyctimystes dayi and Mixophyes fleayi. It also includes a species which has undergone local extinctions and is now listed as Endangered- L. spenceri; and states that by implication the disease is the likely cause of population declines that led to listing of Rheobatrachus silus, R. vitellinus, and T. diurnus as Extinct, T. eungellensis and T. rheophilus as Endangered,and L. aurea as Vulnerable.

Of these 14 species:

• eight have now been recorded with the amphibian chytrid;
• there are currently no reports of the fungus in L. nyakalensis, L. lorica, or T. rheophilus; and
• the remaining three (R. silus, R. vitellinus, and T. diurnus) are currently listed as 'Extinct', and although they may have been eliminated by the disease, they disappeared prior to knowledge of the disease, and there are too few museum specimens to determine if the disease was the cause.

Further information on whether the disease could have caused listing of the 8 species recorded with chytrid fungus follows.

T. acutirostris changed status from not listed to Endangered in 1992, then to Extinct in 1999. It occurred over a relatively small area in the upland Wet Tropics, with abundant populations at all locations before 1990, when the first populations disappeared. Populations to the north then progressively disappeared, and the final population at Big Tableland declined abruptly. The disease was found in wild frogs, captive adults and captive metamorphs. Some of the last individuals were taken into captivity and died of the disease, and the fungus was found on dead animals in the wild during the decline. However, this does not prove the disease caused extinction of this species.

L nannotis, L. rheocola and N. dayi all also occurred in the Wet Tropics in relatively small ranges, and had sudden declines recorded in the early 1990s, following the same pattern as T. acutirostris, ie. extinction of all upland populations and persistence of lowland populations on the same watercourses. In the lowlands sporadic deaths occur, but populations appear stable. The disease has been recorded in these species. Whether chytridiomycosis was the cause of the population declines leading to listing is not known, but it is the most likely cause of these local population extinctions.

L. spenceri, which occurs in Victoria and NSW, showed a similar decline pattern to T. acutirostris. The disease was a cause of death in autopsied frogs, and in a retrospective survey of toe clips the fungus first appeared in March 1996 - the last date the frogs were seen in high numbers. In lowland populations the disease was present, but the population did not decline.

The disease has also been recorded in the following listed species, however whether it was the cause of the population declines leading to listing is unknown:

• L. aurea - occurs in NSW and Victoria, listed as Endangered in NSW, fungus found in individuals from 3 sites.
• T. eungellensis - restricted to undisturbed rainforest in Eungella National Park in mid-eastern Qld, underwent a rapid range contraction in the mid-1980s, fungus recorded in specimens from Eungella National Park.
• M. fleayi occurs in SE Qld and NE NSW, and declines were recorded in Qld from the late 1970s, and the species has disappeared from some sites in Qld and possibly NSW. Very low numbers in many well surveyed sites suggest that declines may also have occurred in sites for which there is little data. The fungus has been recorded in the individuals from NSW and Qld sites.

Although there is no conclusive proof that the disease caused listing of any species, there is significant circumstantial evidence that the disease may have caused the listing of (at least) Taudactylus acutirostris, L. nannotis,L. rheocola, N. dayi and L. spenceri as Endangered.

Conclusion: Based on the information provided and summarised above TSSC considers that the threatening process:

• could have caused the listing of Taudactylus acutirostris, Litoria nannotis,L. rheocola, N. dayi and L. spenceri as Endangered; and
• has the potential to cause a number of other native amphibian species to become eligible for listing as threatened, including Adelotus brevis and Litoria pearsoniana.

The threatening process could cause a number of native amphibian species to become eligible for listing as threatened, and is therefore eligible under this criterion.

B. Could the threatening process cause a listed threatened species or a listed threatened ecological community to become eligible to be listed in another category representing a higher degree of endangerment?

The nomination includes a list of threatened species known to have infected populations:

• Geocrinia vitellina Vulnerable
• Heleioporus australiacus Vulnerable
• Litoria aurea Vulnerable
• Litoria raniformis Vulnerable
• Pseudophryne pengilleyi Vulnerable
• Litoria nannotis Endangered
• Litoria rheocola Endangered
• Litoria spenceriEndangered
• Mixophyes fleayi Endangered
• Mixophyes iteratus Endangered
• Nyctimystes dayiEndangered
• Pseudophryne corroboree Endangered
• Taudactylus eungellensisEndangered
• Taudactylus acutirostris Extinct

This represents 48% of the listed frog species, whilst only 15% of non-listed native frog species have been found infected. This may be due to search effort, however, the nominator believes it suggests a relationship between disease occurrence and population vulnerability. Characteristics of threatened species that could make them more vulnerable to greater impacts are low fecundity and remnant populations. Remnant populations could be made extinct by arrival of the disease in previously chytrid free areas, or by environmental stressors upsetting the balance between chytrid and the frog host where the disease is already present.

The nomination states that all intensively studied populations in which the fungus has been found show some pathological effect ie. some deaths. Four species response patterns are described:

1. extinction;
2. extinction of local populations and survival of the species;
3. population decline and recovery; and
4. sporadic deaths. The first two responses would lead to change of status of a listed species to a more threatened level.

Most of the existing national Recovery Plans for threatened frog species were written before the disease was discovered and recognised as a potential cause of declines. Those plans written after discovery of the disease (including 1 draft plan), cover 4 Extinct, 9 Endangered and 2 unlisted species. They list the disease as a potential threat, and recommend investigation of its occurrence and the likelihood it has caused declines, including retrospective sampling of museum specimens prior to declines and field sampling of surviving frog species.

As described in criterion A, for some southwest WA species there is no data showing significant declines, despite the disease being actively expressed for at least 15 years eg. Geocrinia vitellina, which has maintained its status of Vulnerable over that time. In addition, although the disease has been found in many of the listed species which previously underwent unexplained declines, the disease has not been proven to be the cause of the declines.

For the majority of listed species in which chytridiomycosis has been recorded, the extent of impact on current populations is unknown. However, the disease is the most likely proximate cause of T. acutirostris changing status from Endangered to Extinct; and several examples of the disease being the most likely cause of local population extinctions are known. These include the upland wet tropics species L. nannotis, L. rheocola and N. dayi (allEndangered). The disease has the potential to cause further declines in these species, thus causing them to become eligible for listing in a category representing a higher degree of endangerment.

Conclusion: Based on the information provided and summarised above TSSC considers that the threatening process:

• most likely caused Taudactylus acutirostris to change status from Endangered to Extinct; and
• has the potential to cause a number of other listed threatened amphibian species to become eligible for listing as more threatened, including Litoria nannotis, L. rheocola and Nyctimystes dayi.

The threatening process could cause listed threatened native amphibian species to become eligible for listing in another category representing a higher degree of endangerment, and is therefore eligible under this criterion.

C. Does the threatening process adversely affect 2 or more listed threatened species (other than conservation dependent species) or 2 or more listed threatened ecological communities?

All four species response patterns described in the nomination (extinction; extinction of local populations and survival of the species; population decline and recovery; and sporadic deaths) would constitute adverse impacts on listed threatened species, especially for those listed as Endangered or Critically Endangered.

The nomination includes the following impacts to listed threatened amphibians:

• T. acutirostris populations appear to have suddenly declined as a result of an epidemic;
• three threatened species in Qld (L. nannotis, L. rheocola and N. dayi) had upland populations killed by the disease; and
• it is a known cause of death to several other threatened species (L. aurea, L. spenceri, M. fleayi, P. corroboree, P. pengilleyi, T. eungellensis).

As discussed under criterion A, whether the disease was directly responsible for the extinction of T. acutirostris is not proven. However, it is known to have caused the death of a number of specimens when few individuals remained, which constitutes a significant adverse effect on this listed species.

Conclusion: Based on the information provided and summarised above TSSC considers that the threatening process:

• adversely affected T. acutirostris when it was listed as Endangered; and
• currently adversely affects at least 9 listed threatened species, including: Litoria aurea (Vulnerable); and L. nannotis, L. rheocola, L. spenceri, Mixophyes fleayi, Nyctimystes dayi, Pseudophryne corroboree, P. pengilleyi, and Taudactylus eungellensis (Endangered).

and is therefore eligible under this criterion.

CONCLUSION - The threatening process meets s188(4)(a), s188(4)(b) and s188(4)(c) of the EPBC Act. The threatening process could cause native amphibian species to become listed as threatened, could cause listed threatened species to become listed in another category representing a high degree of endangerment, and adversely affects at least 5 listed threatened amphibian species.

3. Threat Abatement Plan

The nomination does not contain specific information on a threat abatement plan. Information in the nomination relevant to threat abatement includes:

• accidental and deliberate movement of amphibians between and within countries could spread the disease;
• the exact transmission method is unknown, but actions could be taken to minimise spread to uninfected areas eg. the 1999 ban on importation or transfer of amphibians into the NT;
• if environmental factors are related to mortality rate, reducing physical and chemical stressors becomes a major tool in decreasing the impact on populations where the fungus is present.

Expert opinion on the potential for threat abatement differs. Arguments against the feasibility of reducing the threat are based on the lack of knowledge of the disease and treatment options, that the disease is already widespread, and that existing controls on movement of amphibians have not prevented dispersal of the fungus. However, the majority of experts state that, although there are gaps in knowledge, many actions could be implemented to reduce the threat posed, and that a threat abatement plan could: include research to aid and refine threat abatement activities; and build on and integrate with existing regulations, policies and activities.

Actions already underway to restrict spread include: a ban on import of amphibians to the Northern Territory (NT Parks and Wildlife Commission); many frog researchers implementing protocols to reduce the risk of spreading the fungus between frog populations (eg. disinfecting equipment, handling in disposable bags); and some government agencies imposing similar conditions on research permits involving frogs (Qld PWS, NSW NPWS). A number of experts also comment that, given the potential impact of this pathogen we must do whatever is feasible to mitigate its impact.

Recent developments which experts believe indicate threat abatement may be possible include:

• development of hygiene protocols for use during amphibian research and management in both field and laboratory;
• chytrid has been found to be highly susceptible to dehydration, which may help in developing quarantine procedures for captive frogs, and in effective quarantine of frogs in the field; and
• early trials show infected individuals may be treated with fungicides, so procedures for appropriate treatment could be developed, especially for the protection and maintenance of highly threatened amphibian species within institutions responsible for captive breeding.

A number of experts refer to the recommendations of the workshop 'Developing management Strategies to Control Amphibian Diseases: Decreasing the risks due to communicable diseases', held in January 2001. The aim of the workshop was to develop a set of recommendations, for government, non-government and individuals, which are liable to reduce risks of disease to amphibian populations, are feasible and cost effective. The result was 110 recommendations under the headings International, National, Regional and Community Role. The first step in developing a threat abatement plan would be to review these recommendations and incorporate those suitable relevant actions which are not already being implemented.

Experts identified that a threat abatement plan should have as its aims/priorities to:

• reduce further spread and ensure chytrid-free populations remain so;
• manage the disease in populations where the fungus is known to occur;
• prevent exposure of populations to new strains;
• prioritise and investigate the incidence, impact and possible management responses;
• provide a link between a number of recovery plans;
• initiate captive husbandry for highly susceptible species, to ensure at least captive persistence;
• re-stock threatened populations; and
• develop a cure.

Two experts suggest that without knowing the origin of the disease, a threat abatement plan must include priority actions appropriate under each scenario. If the disease is native, it poses greatest threat to 'susceptible' populations, thus the priority should be investigating environmental factors affecting virulence/prevalence, and intrinsic factors rendering frogs susceptible. If the disease is exotic, it poses greatest threat to 'naive' populations, thus the priority should be to protect these from exposure to the fungus.

Specific activities recommended by experts for inclusion in a threat abatement plan have been summarised under three broad headings below.

Legislation/Regulation:

• extend and reinforce existing quarantine and handling protocols into a national protocol, potentially modelled on the 'Hygiene Protocol for the Control of Disease in Frogs' prepared and implemented by NPWS.
• control human movement and release of amphibians between areas, perhaps through local legislation. Implications for the pet trade, food market, provision of experimental animals to scientists, and transportation of plants, would need to be considered, and a procedure for not returning frogs to their point of origin would be required.
• identification of the disease within Australia and by the Office International des Epizooties would ensure 'stock' moved is certified disease free and make public the location of infected countries and regions.
• phase out amphibian importation from overseas (would also prevent other disease spread).
• improve management and packing of bananas at points of origin and destination.

Education/Information:

• educate the community about basic disease management and the risks of transport of potentially infected animals and materials.
• educate the community to ensure support for, and compliance with, existing legislation and regulations, targeting groups at higher risk of spreading the fungus eg. pet trade and scientists.
• encourage habitat rehabilitation specifically to facilitate frog breeding and dispersal (both in rural and urban contexts).

Research/Management:

• facilitate essential research eg. disease ecology, physiology, transmission, origins, factors influencing prevalence and virulence, presence pre-1970, incidence in native populations, and whether there are populations which have not been exposed that require protection.
• develop treatment and prevention protocols, and test at field monitoring sites.
• investigate whether it is possible to remove chytrid from infected sites.
• develop simple effective diagnostic tests for field, habitat and laboratories, and establish tests in accredited regional laboratories, for consistent detection and identification.
• establish baseline data on the distribution and abundance of various widely distributed taxa, and monitor selected areas on a long term basis.
• captive breed research animals instead of importation, and endangered species in areas where the disease is common, to increase numbers and thus increase chances of survival.

Each suggested activity would require consideration as to its feasibility, potential value and cost for inclusion.

Conclusion - A Threat Abatement Plan is considered to be a feasible, effective and efficient way to abate the process.

4. Recommendations

TSSC recommends that:

1. The list referred to in section 183 of the EPBC Act be amended by including in the list as a key threatening process: 'Infection of amphibians with chytrid fungus resulting in chytridiomycosis'; and
2. A threat abatement plan is considered a feasible, efficient, and effective way to abate the process.