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Survey Protocol for Detecting Chytridiomycosis in All Australian Frog Populations

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Survey Protocol for Detecting Chytridiomycosis in All Australian Frog Populations Vol. 80: 85–94, 2008 DISEASES OF AQUATIC ORGANISMS Published July 7 doi: 10.3354/dao01923 Dis Aquat Org OPENPEN ACCESSCCESS Survey protocol for detecting chytridiomycosis in all Australian frog populations Lee F. Skerratt1,*, Lee Berger1, Harry B. Hines2, Keith R. McDonald3, Diana Mendez1, Richard Speare1 1Amphibian Disease Ecology Group, School of Public Health, Tropical Medicine and Rehabilitation Sciences, James Cook University, Townsville, Queensland 4811, Australia 2Queensland Parks and Wildlife Service, PO Box 64, Bellbowrie, Queensland 4070, Australia 3Amphibian Disease Ecology Group, Queensland Parks and Wildlife Service, PO Box 975, Atherton, Queensland 4883, Australia ABSTRACT: Spread of the amphibian chytrid fungus Batrachochytrium dendrobatidis (Bd) has caused the decline and extinction of frogs, but the distribution of Bd is not completely known. This information is crucial to implementing appropriate quarantine strategies, preparing for outbreaks of chytridiomycosis due to introduction of Bd, and for directing conservation actions towards affected species. This survey protocol provides a simple and standard method for sampling all frog popula- tions in Australia to maximise the chances of detecting Bd. In order to structure and prioritise the pro- tocol, areas are divided by bioregion and frog species are allocated depending on the water bodies they utilize into 3 groups representing different levels of risk of exposure to Bd. Sixty individuals per population need to be tested to achieve 95% certainty of detecting 1 positive frog, based on the min- imum apparent prevalence of ≥5% in infected Australian frog populations and using a quantitative real-time TaqMan PCR test. The appropriate season to sample varies among bioregions and will ide- ally incorporate temperatures favourable for chytridiomycosis (e.g. maximum air temperatures gen- erally <27°C). Opportunistic collection and testing of sick frogs and tadpoles with abnormal mouth- parts should also be done to increase the probability of detecting Bd. The survey priorities in order are (1) threatened species that may have been exposed to Bd, (2) bioregions surrounding infected bioregions/ecological groups, and (3) species of frogs of unknown infection status in infected biore- gions. Within these priority groups, sampling should first target ecological groups and species likely to be exposed to Bd, such as those associated with permanent water, and areas within bioregions that have high risk for Bd as indicated by climatic modelling. This protocol can be adapted for use in other countries and a standard protocol will enable comparison among amphibian populations globally. KEY WORDS: Batrachochytrium dendrobatidis · Mapping · Chytrid fungus · Disease · Decline · Amphibian Resale or republication not permitted without written consent of the publisher INTRODUCTION decline and extinction of frogs in other countries, but the distribution of Bd globally is not completely known The amphibian disease chytridiomycosis, caused by (Skerratt et al. 2007, Olson & Ronnenberg 2008, Berger the fungus Batrachochytrium dendrobatidis (Bd), et al. in press). It occurs in all continents except Antarc- invaded Australia, probably in the 1970s (Berger et al. tica, in a wide range of habitats and climates (Speare & 1999). Infection with the amphibian chytrid fungus, Berger 2007). resulting in chytridiomycosis, is a ‘Key Threatening National mapping protocols to identify country-wide Process’ for Australian frogs (Australian Government distributions of chytridiomycosis have not been pub- Department of the Environment and Heritage lished. The background document to the Australian [AGDEH] 2006). This fungus has also caused the Government Threat Abatement Plan for chytridiomy- *Email: [email protected] © Inter-Research 2008 · www.int-res.com 86 Dis Aquat Org 80: 85–94, 2008 cosis discusses the issues involved (AGDEH 2006). Sci- the distribution of Bd, taking the guesswork out of entists have done studies on the prevalence of chytrid- management decisions on quarantine and manage- iomycosis in populations at particular sites, but there ment of frogs that have been translocated and helping have been no systematic studies at a state/province or to direct conservation actions towards populations that national scale. Weldon et al. (2004), in their histological are most likely to be affected by chytridiomycosis. This study of museum specimens extending back to the data will also improve the accuracy of a model of the 19th century, demonstrated that chytridiomycosis is biogeographic requirements for Bd and help identify widespread in southern Africa. Ouellet et al. (2005) naïve populations that would be at risk if Bd was intro- performed a similar study on museum specimens from duced. 25 countries but with the major focus on Canadian The aim of this survey protocol is to provide a simple amphibians. However, both studies were opportunistic and standard method for sampling all wild frog popu- and not designed as systematic national surveys. Gar- lations in Australia for infection with Bd. It also pro- ner et al. (2005) used PCR to map Bd in 13 European vides priorities for surveillance and justification for countries and reported results only as prevalence by extrapolation of results to minimise the number of pop- country. ulations that need to be surveyed. To systematically Patchy data on the distribution of Bd in Australia survey all frog populations throughout Australia is a exists from opportunistic collection of sick or dead major task logistically, due to the large land area, the frogs (Berger et al. 2004) and surveys of healthy frogs diversity of environments and the large number of from restricted locations including examination of amphibian species. Therefore, there is a need to sim- archived specimens (McDonald et al. 2005, Speare et plify and prioritise the task by splitting the continent al. 2005, Kriger et al. 2007). The fungus has been found into areas and allocating species of frogs into groups on 46 species from 3 families (Hylidae, Myobatrachi- that reflect the risk of exposure to Bd. This will result in dae and Bufonidae) in Australia (AGDEH 2006). It has more manageable units (both area- and species-wise) also been reported in 1 individual of Cophixalus orna- to survey initially and enable prioritisation of units to tus (belonging to the family Microhylidae) (Kriger & survey. The number of areas and species that need to Hero 2006). However, this result needs to be inter- be surveyed could be reduced if results from compar- preted with caution, as 557 microhylids, including C. able areas and species were extrapolated. For ex- ornatus, from the areas surrounding the positive ample, if species that are susceptible and likely to be record have tested negative for Bd by either quantita- exposed to Bd are negative then it is likely that other tive real-time PCR (qPCR) or histology (K. Hausel- species in the same area are also negative. We discuss berger & D. Mendez et al. unpubl. data). Chytridiomy- these issues and how to prioritise the work, the number cosis is known to occur in eastern Australia from of frogs that need to be sampled, the time of year to Tasmania north to Cooktown (occurring mainly on or sample, the life-stage to sample, the sampling strategy between the Great Dividing Range and the coast), to employ, the logistics of sampling, and which diag- around Adelaide in South Australia, and in southwest nostic test should be used. We designed the survey Western Australia (Berger et al. 2004, Speare et al. protocol so that it could be used by professional and 2005). Bd has been found in most areas in Australia amateur herpetologists and volunteers working with where it is predicted to occur based on modelling the conservation agencies and other institutions. This pro- climatic variables that described the known distribu- tocol could be adapted for surveying amphibian popu- tion of Bd in Australia in 2003 (Retallick 2003). Al- lations in other countries. As the World Organisation though this model may reflect some collection biases, for Animal Health moves towards implementation of recent surveys have detected Bd in areas where the disease protocols for the international movement of model predicted a high likelihood of occurrence, such amphibians (OIE 2006), a standard technique that as Tasmania, and have failed to detect it in hot or dry can be used to assess the chytridiomycosis-status of areas where it is unlikely to occur, such as the North- countries and demonstrate adequate surveillance will ern Territory, Cape York Peninsula, inland arid areas become essential. of Queensland, and northwest Western Australia (Speare et al. 2005). Ron (2005) produced a model that is valuable in predicting climatic suitability for Bd at a MATERIALS AND METHODS larger spatial scale. The known biology of Bd suggests that high temperatures and lack of permanent water Key aspects to consider when surveying. Priorities: bodies are likely to limit its distribution (Johnson et al. The task of surveying all Australian frog populations is 2003, Berger et al. 2004, Piotrowski et al. 2004, Kriger large. For many frog species, information on the extent & Hero 2007a, Kriger et al. 2007). More detailed map- of their distribution patterns is unknown. Therefore, ping is important as it will identify the exact limits of this survey protocol aims to take into account the feasi- Skerratt et al.: Survey protocol for chytridiomycosis in Australia 87 bility of such an undertaking. Surveys for
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