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

The call for tenders RFT43/2004 designated 6 objectives to be addressed. In the proposal we submitted in response to RFT43/2004, 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.

[1]  S. Williams,et al.  Ecological traits of declining amphibians in upland areas of eastern Australia , 2005 .

[2]  A. Huryn,et al.  The effects of amphibian population declines on the structure and function of Neotropical stream ecosystems , 2006 .

[3]  Ian Joint,et al.  Specificity in the settlement -- modifying response of bacterial biofilms towards zoospores of the marine alga Enteromorpha. , 2003, Environmental microbiology.

[4]  G. Palade,et al.  CELL JUNCTIONS IN AMPHIBIAN SKIN , 1965, The Journal of cell biology.

[5]  R. Ruibal,et al.  Skin Structure and Wiping Behavior of Phyllomedusine Frogs , 1976 .

[6]  P. Ewald Evolution of virulence , 2004, Infectious Disease Clinics of North America.

[7]  M. Fisher Potential interactions between amphibian immunity, infectious disease and climate change , 2007 .

[8]  L. Larsen,et al.  Structure of the toad epidermis during the moulting cycle , 1973, Zeitschrift für Zellforschung und Mikroskopische Anatomie.

[9]  S. Richards The tadpole of the Australian frog Litoria nyakalensis (Anura, Hylidae), and a key to the torrent tadpoles of northern Queensland , 1992 .

[10]  P. Morin Predation, Competition, and the Composition of Larval Anuran Guilds , 1983 .

[11]  R. Speare,et al.  Distribution of Batrachochytrium dendrobatidis and pathology in the skin of green tree frogs Litoria caerulea with severe chytridiomycosis. , 2005, Diseases of aquatic organisms.

[12]  E. Brodie,et al.  Laboratory Behavior of Ascaphus Truei Tadpoles , 1972 .

[13]  K. Gosner,et al.  A simplified table for staging anuran embryos and larvae with notes on identification , 1960 .

[14]  M. Mahony The decline of the Green and Golden Bell Frog Litoria aurea viewed in the context of declines and disappearances of other Australian frogs , 1996 .

[15]  Peter M. Letcher,et al.  A molecular phylogeny of the flagellated fungi (Chytridiomycota) and description of a new phylum (Blastocladiomycota). , 2006, Mycologia.

[16]  M. Fisher,et al.  The emerging amphibian pathogen Batrachochytrium dendrobatidis globally infects introduced populations of the North American bullfrog, Rana catesbeiana , 2006, Biology Letters.

[17]  A. Fagotti,et al.  Ecology: The proximate cause of frog declines? , 2007, Nature.

[18]  P. Eterovick,et al.  DISTRIBUTION OF TADPOLES WITHIN AND AMONG BRAZILIAN STREAMS: THE INFLUENCE OF PREDATORS, HABITAT SIZE AND HETEROGENEITY , 2006 .

[19]  P. Ewald Evolution of Infectious Disease , 1993 .

[20]  J. Rowley Why does Chytridiomycosis drive some frog populations to extinction and not others?: the effects of interspecific variation in host behaviour , 2006 .

[21]  S. Williams,et al.  Rainforest frogs of the Australian Wet Tropics: guild classification and the ecological similarity of declining species , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[22]  C. Briggs,et al.  Effect of Temperature on Host Response to Batrachochytrium dendrobatidis Infection in the Mountain Yellow-legged Frog (Rana muscosa) , 2008, Journal of wildlife diseases.

[23]  A. Evans Causation and Disease: The Henle-Koch Postulates Revisited 1 , 1976, The Yale journal of biology and medicine.

[24]  John D. Reeve,et al.  Ecological Traits Predicting Amphibian Population Declines in Central America , 2003 .

[25]  R. Inger,et al.  Organization of a community of tadpoles in rain forest streams in Borneo , 1986, Journal of Tropical Ecology.

[26]  C. Briggs,et al.  INVESTIGATING THE POPULATION‐LEVEL EFFECTS OF CHYTRIDIOMYCOSIS: AN EMERGING INFECTIOUS DISEASE OF AMPHIBIANS , 2005 .

[27]  T. Day PARASITE TRANSMISSION MODES AND THE EVOLUTION OF VIRULENCE , 2001, Evolution; international journal of organic evolution.

[28]  P. Eterovick,et al.  Factors influencing spatial and temporal structure of frog assemblages at ponds in southeastern Brazil , 2006 .

[29]  R. Alford,et al.  Lack of Evidence for Epidemic Disease as an Agent in the Catastrophic Decline of Australian Rain Forest Frogs , 1997 .

[30]  J. Czopek Quantitative studies on the morphology of respiratory surfaces in amphibians. , 1965, Acta anatomica.

[31]  S. Richards Influence of flow regime on habitat selection by tadpoles in an Australian rainforest stream , 2002 .

[32]  K. Lips,et al.  Decline and extirpation of an endangered Panamanian stream frog population (Craugastor punctariolus) due to an outbreak of chytridiomycosis , 2008 .

[33]  J. Koella,et al.  Shared Control of Epidemiological Traits in a Coevolutionary Model of Host‐Parasite Interactions , 2003, The American Naturalist.

[34]  R. May,et al.  Population biology of infectious diseases: Part II , 1979, Nature.

[35]  A. Hyatt,et al.  Rapid quantitative detection of chytridiomycosis (Batrachochytrium dendrobatidis) in amphibian samples using real-time Taqman PCR assay. , 2004, Diseases of aquatic organisms.

[36]  D. Wake,et al.  Amphibian Declines: Judging Stability, Persistence, and Susceptibility of Populations to Local and Global Extinctions , 1994 .

[37]  D. Benos,et al.  Surface potentials and sodium entry in frog skin epithelium. , 1981, The Journal of physiology.

[38]  R. Lingeman,et al.  Estimating the impact of fungal parasites on phytoplankton populations , 1992 .

[39]  K. R. Clarke,et al.  The attachment of Enteromorpha zoospores to a bacterial biofilm assemblage , 2000 .

[40]  D. Hankin,et al.  A habitat-based design for sampling and monitoring stream amphibians with an illustration from Redwood National Park , 1997 .

[41]  B. T. Clarke,et al.  THE NATURAL HISTORY OF AMPHIBIAN SKIN SECRETIONS, THEIR NORMAL FUNCTIONING AND POTENTIAL MEDICAL APPLICATIONS , 1997, Biological reviews of the Cambridge Philosophical Society.

[42]  R. Balaban,et al.  On the mechanism of the amiloride-sodium entry site interaction in anuran skin epithelia , 1979, The Journal of general physiology.

[43]  J. Longcore,et al.  BATRACHOCHYTRIUM DENDROBATIDIS GEN. ET SP. NOV., A CHYTRID PATHOGENIC TO AMPHIBIANS , 1999 .

[44]  K. Richards,et al.  A non-lethal technique for detecting the chytrid fungus Batrachochytrium dendrobatidis on tadpoles. , 2006, Diseases of aquatic organisms.

[45]  B. Ibelings,et al.  Parasitic chytrids: their effects on phytoplankton communities and food-web dynamics , 2007, Hydrobiologia.

[46]  W. Heyer Studies in larval amphibian habitat partitioning , 1976 .

[47]  Edward H. Miller,et al.  Comparative Biochemistry and Physiology, Part A , 2009 .

[48]  R. Speare,et al.  Endemic Infection of the Amphibian Chytrid Fungus in a Frog Community Post-Decline , 2004, PLoS biology.

[49]  L. Larsen,et al.  Structure of the toad epidermis during the moulting cycle , 1973, Cell and Tissue Research.

[50]  J. Morton,et al.  SURVEILLANCE FOR BATRACHOCHYTRIUM DENDROBATIDIS USING MIXOPHYES (ANURA: MYOBATRACHIDAE) LARVAE , 2007, Journal of wildlife diseases.

[51]  G. Fellers,et al.  Disappearance of the cascades frog Rana cascadae at the southern end of its range, California, USA , 1993 .

[52]  P. Ewald,et al.  Host-Parasite Relations, Vectors, and the Evolution of Disease Severity , 1983 .

[53]  R. Harris,et al.  Amphibian Pathogen Batrachochytrium dendrobatidis Is Inhibited by the Cutaneous Bacteria of Amphibian Species , 2006, EcoHealth.

[54]  Lars Råberg,et al.  Disentangling Genetic Variation for Resistance and Tolerance to Infectious Diseases in Animals , 2007, Science.

[55]  S. Savkovic,et al.  Intestinal epithelial responses to enteric pathogens: effects on the tight junction barrier, ion transport, and inflammation , 2003, Gut.

[56]  D. Brown,et al.  The amphibian epidermis: distribution of mitochondria-rich cells and the effect of oxytocin. , 1981, Journal of cell science.

[57]  D. Ebert Experimental evolution of parasites. , 1998, Science.

[58]  Marti J. Anderson,et al.  Spatial and temporal heterogeneity of the bacterial communities in stream epilithic biofilms. , 2008, FEMS microbiology ecology.

[59]  Dieter Ebert,et al.  Challenging the trade-off model for the evolution of virulence: is virulence management feasible? , 2003, Trends in microbiology.

[60]  J. Voyles Virulence and pathogenesis of chytridiomycosis: a lethal disease of amphibians , 2009 .

[61]  R. F. Ewer The Effects of Posterior Pituitary Extracts on Water Balance in Bufo Carens and Xenopus Laevis, together with some General Considerations of Anuran Water Economy , 1952 .

[62]  R. Alford,et al.  Behaviour of Australian rainforest stream frogs may affect the transmission of chytridiomycosis. , 2007, Diseases of aquatic organisms.

[63]  K. Beard,et al.  Infection of an invasive frog Eleutherodactylus coqui by the chytrid fungus Batrachochytrium dendrobatidis in Hawaii , 2005 .

[64]  P. Daszak,et al.  Cryo-archiving of Batrachochytrium dendrobatidis and other chytridiomycetes. , 2003, Diseases of aquatic organisms.

[65]  P. Daszak,et al.  Presence of an emerging pathogen of amphibians in introduced bullfrogs Rana catesbeiana in Venezuela , 2004 .

[66]  R. Speare,et al.  Additional disinfectants effective against the amphibian chytrid fungus Batrachochytrium dendrobatidis. , 2007, Diseases of aquatic organisms.

[67]  L. M. Castanho,et al.  Moulting behavior in leaf-frogs of the genus phyllomedusa (Anura : hylidae) , 2001 .

[68]  G. Bradley,et al.  Chytridiomycosis in Native Arizona Frogs , 2002, Journal of wildlife diseases.

[69]  D E Green,et al.  Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[70]  R. Alford,et al.  Emerging infectious disease and the loss of biodiversity in a Neotropical amphibian community. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[71]  P. Dixon,et al.  Ecology: Global amphibian population declines , 2001, Nature.

[72]  U. Klein,et al.  The key role of the H+ V-ATPase in acid-base balance and Na+ transport processes in frog skin. , 1997, The Journal of experimental biology.

[73]  C. Shiff,et al.  Frequency of Moulting in Anura , 1953, Nature.

[74]  L. J. Douglas,et al.  Blood group glycolipids as epithelial cell receptors for Candida albicans , 1996, Infection and immunity.

[75]  R. Ricklefs,et al.  Community Diversity: Relative Roles of Local and Regional Processes , 1987, Science.

[76]  J. Piotrowski,et al.  Physiology of Batrachochytrium dendrobatidis, a chytrid pathogen of amphibians. , 2004, Mycologia.

[77]  D. Sigee Freshwater Microbiology: Biodiversity and Dynamic Interactions of Microorganisms in the Aquatic Environment , 2005 .

[78]  Michael K. Young,et al.  A hierarchical approach to classifying stream habitat features , 1993 .

[79]  C. Frith,et al.  Seasonality of litter invertebrate populations in an Australian upland tropical rain forest. , 1990 .

[80]  N. Cooper,et al.  Predicting susceptibility to future declines in the world's frogs , 2008 .

[81]  M. Fisher,et al.  Persistence of the emerging pathogen Batrachochytrium dendrobatidis outside the amphibian host greatly increases the probability of host extinction , 2008, Proceedings of the Royal Society B: Biological Sciences.

[82]  C. Williams,et al.  Effect of season and temperature on mortality in amphibians due to chytridiomycosis. , 2004, Australian veterinary journal.

[83]  A. Dobson Population Dynamics of Pathogens with Multiple Host Species , 2004, The American Naturalist.

[84]  P. Ewald,et al.  Transmission modes and the evolution of virulence , 1991, Human nature.

[85]  J. Travis,et al.  The Role of Abiotic Factors in Community Organization , 1991, The American Naturalist.

[86]  A. Hyatt,et al.  Production of polyclonal antibodies to Batrachochytrium dendrobatidis and their use in an immunoperoxidase test for chytridiomycosis in amphibians. , 2002, Diseases of aquatic organisms.

[87]  J. Bosch,et al.  Chytrid fungus infection related to unusual mortalities of Salamandra salamandra and Bufo bufo in the Peñalara Natural Park, Spain , 2006, Oryx.

[88]  R. Alford,et al.  Structure and dynamics of a rainforest frog (Litoria genimaculata) population in northern Queensland , 2005 .

[89]  M. Brehm,et al.  HOST PARASITE INTERACTIONS BETWEEN FRESHWATER PHYTOPLANKTON AND CHYTRID FUNGI (CHYTRIDIOMYCOTA) 1 , 2004 .

[90]  William W. Woessner,et al.  Evaluation of an Inexpensive Small-Diameter Temperature Logger for Documenting Ground Water-River Interactions , 2005 .

[91]  C. L. Richards ECOLOGICAL AND EVOLUTIONARY IMPLICATIONS FOR THE CONSERVATION OF PANAMANIAN GOLDEN FROGS. , 2008 .

[92]  R. Alford,et al.  Ecology of Chytridiomycosis in Rainforest Stream Frog Assemblages of Tropical Queensland , 2005 .

[93]  S. Ron Predicting the Distribution of the Amphibian Pathogen Batrachochytrium dendrobatidis in the New World 1 , 2005 .

[94]  J. Eischeid,et al.  Climate Variability in Regions of Amphibian Declines , 2001 .

[95]  Ross A. Alford,et al.  Global Amphibian Declines: A Problem in Applied Ecology , 1999 .

[96]  S. Kupferberg THE ROLE OF LARVAL DIET IN ANURAN METAMORPHOSIS , 1997 .

[97]  L. Rollins‐Smith Metamorphosis and the amphibian immune system , 1998, Immunological reviews.

[98]  C. Carey,et al.  Possible interrelations among environmental toxicants, amphibian development, and decline of amphibian populations. , 1995, Environmental health perspectives.

[99]  R. Alford,et al.  Habitat Partitioning among Size Classes of Larval Southern Leopard Frogs, Rana utricularia , 1982 .

[100]  J. Brunner,et al.  Pathogenicity and Transmission of Chytridiomycosis in Tiger Salamanders (Ambystoma tigrinum) , 2003, Copeia.

[101]  P. Budtz Epidermal Tissue Homeostasis , 1985, Cell and tissue kinetics.

[102]  R. Speare,et al.  Electrolyte depletion and osmotic imbalance in amphibians with chytridiomycosis. , 2007, Diseases of aquatic organisms.

[103]  T. Zohary,et al.  Interactions between the bloom-forming dinoflagellate Peridinium gatunense and the chytrid fungus Phlyctochytrium sp. , 2007, Hydrobiologia.

[104]  D. Sacks,et al.  Metacyclogenesis is a major determinant of Leishmania promastigote virulence and attenuation , 1987, Infection and immunity.

[105]  P. Daszak,et al.  Emerging infectious diseases of wildlife--threats to biodiversity and human health. , 2000, Science.

[106]  P. Daszak,et al.  Infectious disease and amphibian population declines , 2003 .

[107]  Kay S. Bradfield,et al.  Ecology: Global warming and amphibian losses , 2007, Nature.

[108]  M. Fisher,et al.  Environmental detection of Batrachochytrium dendrobatidis in a temperate climate. , 2007, Diseases of aquatic organisms.

[109]  P. Daszak,et al.  The Decline of the Sharp-Snouted Day Frog (Taudactylus acutirostris): The First Documented Case of Extinction by Infection in a Free-Ranging Wildlife Species? , 2006, EcoHealth.

[110]  K. Lips,et al.  Batrachochytrium dendrobatidis infection patterns among Panamanian amphibian species, habitats and elevations during epizootic and enzootic stages. , 2008, Diseases of aquatic organisms.

[111]  E. Middleton,et al.  Amphibian Declines and Environmental Change: Use of Remote‐Sensing Data to Identify Environmental Correlates , 2001 .

[112]  Benjamin M. Bolker,et al.  Mechanisms of disease‐induced extinction , 2004 .

[113]  L. Berger Diseases in Australian frogs , 2001 .

[114]  G. Castillo,et al.  Response of frog and toad skin to norepinephrine. , 1997, Comparative biochemistry and physiology. Part A, Physiology.

[115]  C. Carey,et al.  Hypothesis Concerning the Causes of the Disappearance of Boreal Toads from the Mountains of Colorado , 1993 .

[116]  R. J. Stevenson,et al.  Algal ecology: freshwater benthic ecosystems , 1996 .

[117]  C. Frith,et al.  Seasonality of insect abundance in an Australian upland tropical rainforest , 1985 .

[118]  R. Speare,et al.  Origin of the Amphibian Chytrid Fungus , 2004, Emerging infectious diseases.

[119]  M. Fisher,et al.  Emergence of amphibian chytridiomycosis in Britain , 2005, Veterinary Record.

[120]  R. Alford,et al.  Emerging disease of amphibians cured by elevated body temperature. , 2003, Diseases of aquatic organisms.

[121]  K. Choe,et al.  A putative H+-K+-ATPase in the Atlantic stingray, Dasyatis sabina: primary sequence and expression in gills. , 2004, American journal of physiology. Regulatory, integrative and comparative physiology.

[122]  M. Barinaga Where have all the froggies gone? , 1990, Science.

[123]  A. Cann,et al.  Reversion to neurovirulence of the live-attenuated Sabin type 3 oral poliovirus vaccine. , 1984, Nucleic acids research.

[124]  J. Carver,et al.  Host defence antibacterial peptides from skin secretions of Australian amphibians. The relationship between structure and activity , 1999 .

[125]  J. Hero,et al.  Large‐scale seasonal variation in the prevalence and severity of chytridiomycosis , 2006 .

[126]  Richard Speare,et al.  Spread of Chytridiomycosis Has Caused the Rapid Global Decline and Extinction of Frogs , 2007, EcoHealth.

[127]  D. E. Scott The Effect of Larval Density on Adult Demographic Traits in Ambystoma Opacum , 1994 .

[128]  T. Dietz,et al.  Chloride transport across isolated skin of Rana pipiens. , 1975, The American journal of physiology.

[129]  M. Voytek,et al.  Quantitative PCR detection of Batrachochytrium dendrobatidis DNA from sediments and water. , 2007, Diseases of aquatic organisms.

[130]  David W. Hosmer,et al.  Applied Logistic Regression , 1991 .

[131]  A. Gitelman,et al.  Carryover aquatic effects on survival of metamorphic frogs during pond emigration. , 2006, Ecological applications : a publication of the Ecological Society of America.

[132]  I. Mikaelian,et al.  Clinical diagnosis and treatment of epidermal chytridiomycosis in African clawed frogs (Xenopus tropicalis). , 2002, Comparative medicine.

[133]  M. Fisher,et al.  The relationship between the emergence of Batrachochytrium dendrobatidis, the international trade in amphibians and introduced amphibian species , 2007 .

[134]  P. Hosseini,et al.  Seasonality and the dynamics of infectious diseases. , 2006, Ecology letters.

[135]  P. Budtz Epidermal Tissue Homeostasis. , 1988 .

[136]  R. Alford,et al.  Experimental Exposures of Boreal Toads (Bufo boreas) to a Pathogenic Chytrid Fungus (Batrachochytrium dendrobatidis) , 2006, EcoHealth.

[137]  M. Fuller,et al.  Cutaneous Chytridiomycosis in Poison Dart Frogs (Dendrobates spp.) and White's Tree Frogs (Litoria Caerulea) , 1999, Journal of veterinary diagnostic investigation : official publication of the American Association of Veterinary Laboratory Diagnosticians, Inc.

[138]  L. Mantel,et al.  Osmotic and ionic regulation , 1983 .

[139]  Arturo Casadevall,et al.  Host-Pathogen Interactions: Redefining the Basic Concepts of Virulence and Pathogenicity , 1999, Infection and Immunity.

[140]  F. Gleason,et al.  Diagnostic assays and sampling protocols for the detection of Batrachochytrium dendrobatidis. , 2007, Diseases of aquatic organisms.

[141]  R. May,et al.  Regulation and Stability of Host-Parasite Population Interactions: I. Regulatory Processes , 1978 .

[142]  S. Burgin,et al.  A rapid technique to detect chytrid infection in adult frogs , 2003 .

[143]  D. Berg,et al.  Virulence Genes in Helicobacter pylori Strains from West Bengal Residents with Overt H. pylori-Associated Disease and Healthy Volunteers , 2002, Journal of Clinical Microbiology.

[144]  R. Speare,et al.  Fungicidal effects of chemical disinfectants, UV light, desiccation and heat on the amphibian chytrid Batrachochytrium dendrobatidis. , 2003, Diseases of aquatic organisms.

[145]  W. Heyer,et al.  Tadpoles, Predation and Pond Habitats in the Tropics , 1975 .

[146]  J. Koella,et al.  Concurrent Evolution of Resistance and Tolerance to Pathogens , 2004, The American Naturalist.

[147]  M. L. Crump Opportunistic Cannibalism by Amphibian Larvae in Temporary Aquatic Environments , 1983, The American Naturalist.

[148]  Res Altwegg,et al.  PATTERNS OF NATURAL SELECTION ON SIZE AT METAMORPHOSIS IN WATER FROGS , 2003, Evolution; international journal of organic evolution.

[149]  J. Stajich,et al.  Proteomic and phenotypic profiling of the amphibian pathogen Batrachochytrium dendrobatidis shows that genotype is linked to virulence , 2009, Molecular ecology.

[150]  H. Holfeld Fungal infections of the phytoplankton: seasonality, minimal host density, and specificity in a mesotrophic lake. , 1998 .

[151]  P. Daszak,et al.  Experimental evidence that the bullfrog (Rana catesbeiana) is a potential carrier of chytridiomycosis, an emerging fungal disease of amphibians , 2004 .