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Experimental Research to Obtain a Better Understanding of the Pathogenesis of Chytridiomycosis, and the Susceptibility and Resis

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Experimental Research to Obtain a Better Understanding of the Pathogenesis of Chytridiomycosis, and the Susceptibility and Resis Final Report to Department of the Environment and Heritage on work completed for RFT 43/2004, “Experimental research to obtain a better understanding of the pathogenesis of chytridiomycosis, and the susceptibility and resistance of key amphibian species to chytridiomycosis in Australia.” 22 May 2010 Ross A. Alford, Lee F. Skerratt, Lee Berger, Richard Speare, Sara Bell, Nicole Kenyon, Jodi J.L. Rowley, Kim Hauselberger, Sam Young, Jamie Voyles, Robert Puschendorf, Scott Cashins, Rebecca Webb, Ruth Campbell, and Diana Mendez. James Cook University Amphibian Disease Ecology Group Executive Summary.......................................................................................................... 4 Introduction.................................................................................................................. 4 Objectives identified in RFT 43-04.............................................................................. 4 Results addressing Objectives 1, 2, 4, 5, and 6............................................................ 5 Results addressing Objective 3 .................................................................................. 10 Supporting research/technique development and testing......................................... 11 Summary and recommendations............................................................................... 11 Publications arising from work funded in whole or in part by Tender 43-04......... 13 Other publications by the JCU Amphibian Disease Ecology Group during the period of the tender and relevant to tender 43-04..................................................... 17 Conference presentations related to Tender 43-04 (incomplete listing).................. 19 Full report ....................................................................................................................... 23 Structure of the proposal and report......................................................................... 23 Reports on projects identified in Tender 43-04 .............................................................. 25 Project 1. Development of chytridiomycosis in thermal and humidity gradients... 25 Project 1.1. The effect of exposure to a fungal disease on anuran selection of microenvironments. A comparison of three Australian hylid frogs. ...................... 28 Project 1.2. Do frogs avoid water that contains Batrachochytrium dendrobatidis zoospores? .................................................................................................................. 49 Project 2. Microenvironmental profiling of frogs in the field and how microenvironmental history affects the development of chytridiomycosis.............. 63 Project 3. Determining the vulnerability and mechanisms of resistance to chytridiomycosis of microhylid frogs. ....................................................................... 67 Project 3.1 Resistance of the Australian Microhylidae to Batrachochytrium dendrobatidis in nature.............................................................................................. 69 Project 3.2 Anti-fungal skin peptides of microhylids .............................................. 85 Project 3.3 Experimental Infection of Cophixalus ornatus, an Australian direct developing frog, with Batrachochytrium dendrobatidis ...................................... 106 Project 4. Effects of water movement on infection and reinfection by the amphibian chytrid. ................................................................................................... 117 Project 4.1. Sodium hypochlorite denatures the DNA of the amphibian chytrid fungus Batrachochytrium dendrobatidis* .............................................................. 120 Project 4.2. Effect of Sample Collection Techniques on Sensitivity of a Real Time PCR Assay for Detecting the Amphibian Pathogen Batrachochytrium dendrobatidis............................................................................................................ 127 Project 4.3. Lethal Effect of Latex, Vinyl and Nitrile Gloves on Tadpoles .......... 137 Project 4.4 Tadpole Ecology: the context of interactions with B. dendrobatidis . 142 Project 4.5 Epidemiology of Batrachochytrium dendrobatidis in Rainforest Stream Tadpoles.................................................................................................................... 171 Project 5. Experimental studies on acquired immunity and the evolution of resistance.................................................................................................................. 217 Project 6. Determining the proximate causes of morbidity and mortality due to chytridiomycosis....................................................................................................... 218 Project 6.1 Review of virulence and pathogenesis as related to amphibian chytridiomycosis....................................................................................................... 219 Project 6.2 Life history adjustments of an amphibian pathogen: Differential growth of Batrachochytrium dendrobatidis............................................................ 233 Project 6.3. Differential growth and virulence of Batrachochytrium dendrobatidis........................................................................................................... 244 Project 6.4 Electrolyte depletion and osmotic imbalance in amphibians with chytridiomycosis....................................................................................................... 255 Project 6.5 Pathogenesis of amphibian chytridiomycosis: a pathological perfect storm? ....................................................................................................................... 263 Project 6.1-6.5 Bibliography and literature cited ................................................... 286 Project 6.6. Intensity of infection and sampling locality affect the distribution of Batrachochytrium dendrobatidis among body regions on green-eyed tree frogs (Litoria genimaculata)............................................................................................. 308 Project 7. Mechanisms of resistance to chytridiomycosis in recovered and recolonised populations. .......................................................................................... 329 Project 7.1 Have anuran skin peptide defences against an emerging amphibian pathogen responded to natural selection? .............................................................. 330 Project 7.2 Behaviour and microenvironment selection in recovered and recolonising populations.......................................................................................... 349 Project 7.2.1 Rediscovery of an Australian stream frog (Litoria lorica) and environmental refuges from chytridiomycosis........................................................ 351 Project 8. Epidemiology of chytridiomycosis ......................................................... 363 Project 9. Studies on Mixophyes balbus and L. aurea surviving in areas contaminated with heavy metals.............................................................................. 364 Executive Summary Introduction The call for tenders RFT43/2004 designated 6 objectives to be addressed. In the proposal we submitted in response to RFT 43/2004, we described 9 projects, each of which addressed some or all of these objectives. All of the projects were designed to share some resources with the projects we designed in our response to RFT 42/2004, and some were partially or wholly subsumed within the work to be carried out in that submission. Similarly, some of the 9 projects outlined in our proposal for RFT43/2004 addressed data needed in our response to RFT 42/2004. Both reports therefore refer to each other where appropriate. The tenders were called in 2004 and projects were initially designed to be completed within three years. Some projects were delayed by the need to recruit qualified staff and students, and funds were not expended as fast as initially anticipated, so the projects were extended for a fourth year. All are now complete, although some data collected remain to be written up. RFT 43/2004 identified six major objectives. Objectives 1, 2, 4, 5, and 6 are highly interrelated and were addressed by a series of linked projects. Objective 3 was addressed by a more clearly separate project. We will present Objectives 1, 2 ,4 5, and 6, and then summarise the findings dealing with those. We will then present Objective 3 and a summary Objectives identified in RFT 43-04 1. Build on our understanding of the pathogenesis of chytridiomycosis including the host and environmental factors that determine the ultimate outcome of infection, i.e., death, persistent infection with no obvious effect, and cure. 2. Investigate populations of frog species that have undergone widespread chytrid- associated decline to: i. identify the factors that maintain these populations, and ii. develop and assess management activities that can reproduce these factors in other populations, particularly threatened species. 3. Investigate the manifestation of chytridiomycosis by determining the physiological mechanisms associated with morbidity and mortality of affected frogs. 4. Determine whether populations that have recovered after chytrid-associated decline are susceptible to future severe effects from chytridiomycosis. 5. Determine the resistance of key frog species (how key frog species are determined must be clearly identified by the tenderer
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