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Experimental Research to Obtain a Better Understanding of the Epidemiology, Transmission and Dispersal of Amphibian Chytrid Fungus in Australian Ecosystems”

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Experimental Research to Obtain a Better Understanding of the Epidemiology, Transmission and Dispersal of Amphibian Chytrid Fungus in Australian Ecosystems” FINAL REPORT TO DEPARTMENT OF THE ENVIRONMENT AND HERITAGE ON RFT 42/2004 “Experimental research to obtain a better understanding of the epidemiology, transmission and dispersal of amphibian chytrid fungus in Australian ecosystems” Adult of the rediscovered armoured mist frog Litoria lorica (left) and Litoria nannotis (right) Lee F. Skerratt1, Andrea D. Phillott1, Scott D. Cashins1,2, Rebecca Webb1, Robert Puschendorf2, Bryan Windmiller3, Rebecca James1, Alison Robbins3, Lee Berger1, Jamie Voyles1, Rick Speare1, Ross A. Alford2, Keith McDonald4, Diana Mendez1, Jeremy VanDerWal2, and Stephen Garland1 1 School of Public Health and Tropical Medicine, James Cook University, Townsville, Qld 4811, Australia 2 School of Marine and Tropical Biology, James Cook University, Townsville, Qld 4811, Australia 3 65 Arrowhead Road, Concord, MA 01742, USA 4 Queensland Parks and Wildlife Service, PO Box 975, Atherton, Qld 4883 1 TABLE OF CONTENTS Zoospore survival times in leaf detritus collected from stream environments.....................................14 Methods................................................................................................................................................14 Results ..................................................................................................................................................15 Discussion ............................................................................................................................................15 Epidemiology of Batrachochytrium dendrobatidis in Rainforest Stream Tadpoles..........................108 Introduction ........................................................................................................................................108 Effects of Infection with Batrachochytrium dendrobatidis on Tadpoles...........................................144 Introduction ........................................................................................................................................144 Discussion ..........................................................................................................................................213 EXECUTIVE SUMMARY This is the final report for this tender due 31 March 2009. The original tender was three years duration but this was extended to four years early on in the tender once it became clear that it would take some time to get all projects within the tender up and running. This tender is linked to tender 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.” Both tenders were undertaken concurrently by the Amphibian Disease Ecology Group at James Cook University. The objectives of the tender are listed below with the major findings. Detailed results follow this executive summary. Objective 1. Does B. dendrobatidis exist as a free-living organism in suitable habitats, particularly natural water bodies and moist substrates? If so, can we identify and describe these free-living organisms and their biology/ecology? Final Report to Department of the Environment and Heritage on RFT 42/2004 2 Batrachochytrium dendrobatidis exists as a free living organism given that it releases aquatic zoopores into the environment. Our results suggest that motility and possibly survival of these zoospores are decreased in higher nutrient environments due to competition with more robust microflora. In addition, encystment of zoopores and subsequent growth and reproduction of zoosporangia also appears to be decreased in higher nutrient environments and can be explained by an inability to compete with other microflora. We therefore propose that B. dendrobatidis is more likely to survive and grow as a saprobe in low nutrient environments. We did detect B. dendrobatidis DNA in water, on rocks, leaves and in sand within the stream at very low levels suggesting that B. dendrobatidis is widespread and mostly likely surviving as zoospores and possibly small colonies of zoosporangia within biofilms in low nutrient environments. We showed that B. dendrobatidis is able to readily disperse within water bodies. We also showed that B. dendrobatidis has the ability to adapt to low nutrient environments to maximize its fitness. The management implications of this are that whilst B. dendrobatidis exists within the environment and water and water body substrates are potential fomites for spread, the environment is not a major site for growth and reproduction of B. dendrobatidis. It is therefore likely that B. dendrobatidis can be readily controlled within amphibian populations by controlling infection within amphibian hosts. It is also likely that transmission of B. dendrobatidis is affected by the environment and may be less likely within high nutrient water bodies or other environments that affect the survival of zoospores such as saline or polluted water bodies. In disturbed habitats, modification of water bodies to reduce survival of zoospores may be a viable management option. Potentially infectious water or substrates from water bodies should be treated to kill B. dendrobatidis prior to their movement to prevent spread. Objective 2. What environmental characteristics (eg. pH, pO2, ion content, nitrate, organic content) of natural water bodies (both permanent and ephemeral) and climate (eg. temperature, rainfall) favour the biology of B. dendrobatidis? Objective 2.1: We will determine whether any of the above environmental or climatic variables are correlated with either intensity and prevalence of infection in frogs and tadpoles or environmental levels of B. dendrobatidis. Objective 2.2: Perform a case control study to determine risk factors for survival of L. aurea in NSW water bodies with a focus on heavy metal pollution and salinity. Objective 2:3: Determine if there are differences in the growth rate of B. dendrobatidis in vitro using water from these sites. Objective 2.4: If heavy metals or salinity appear to have a negative effect on B. dendrobatidis, perform experimental infections to evaluate the effect on the natural history of chytridiomycosis. The effects of organic content of natural water bodies are explored above under objective 1. Further work on effects of water quality on the epidemiology of chytridiomycosis in the green and golden bell frog Litoria aurea has been undertaken by scientists at Newcastle University, Michael Mahony, John Clulow and a PhD Candidate Michelle Stockwell. Their results suggest that higher levels of sodium in water may protect this species from Bd and prevent population extirpation. The results of this work are included in Appendix 1 and will be published by Michelle Stockwell (PhD thesis, in preparation). Some similar collaborative work on the epidemiology of chytridiomycosis in the southern bell frog Litoria raniformis has been undertaken with scientists Ray and Cherie Draper from Victoria. It is hoped that this work will be published in the scientific literature by the end of 2011. Final Report to Department of the Environment and Heritage on RFT 42/2004 3 We explored the effects of climate, confirming the negative affects of relatively high temperatures on chytridiomycosis such as when minimum temperatures are above an ambient air temperature of 20°C (see also Objective 4 for experimental work showing higher temperatures (32 versus 23°C) increased survival of metamorphs with chytridiomycosis). We also found potential negative effects of high rainfall and high humidity and low humidity. Climate interacts with habitat and life history of species so that the effects of climate can vary. The data collected for this Objective have not been fully analysed but the potential limiting affects of extreme climatic conditions on chytridiomycosis even if they only occur seasonally have been well demonstrated in lowland rainforest populations of frogs. This understanding led to the rediscovery of the armoured mist frog, Litoria lorica, during this project in dry sclerophyll forest that is outside the former known distribution of the species in high altitude rainforest. The high altitude dry sclerophyll forest on the western edge of the Wet Tropics is regarded as suboptimal for chytridiomycosis due to its generally unfavourable climate (hotter and drier) for at least part of the year. The management implications of this work are that species highly susceptible to chytridiomycosis may persist in areas that are climatically unsuitable for chytridiomycosis for at least part of the year. Similarly, unsuitable water bodies for chytridiomycosis may be a refuge for species highly susceptible to chytridiomycosis. Protection of these areas are a priority for management as some may occur outside of current reserves and is currently being addressed for L. lorica. Objective 3. What is the minimum density of chytrid zoospores in natural water bodies required to infect species of native amphibians? B. dendrobatidis occurs at low density wihin rainforest streams (as shown in Objective 1) and yet transmission occurs readily (as shown in Objective 7). Transmission is likely to occur at densities of zoospores below our current ability to readily detect them. Therefore, until methods to filter large volumes of water and concentrate zoospores to enable detection are developed we will be unable to answer this Objective. Objective 4. Does the density of chytrid zoospores in natural water bodies correlate with intensity of
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