Investigating disease ecology, pathogenesis and population persistence of frogs threatened by chytridiomycosis to improve management outcomes

Brannelly, Laura A. (2016) Investigating disease ecology, pathogenesis and population persistence of frogs threatened by chytridiomycosis to improve management outcomes. PhD thesis, James Cook University.

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Amphibians are currently experiencing the greatest decline in biodiversity of all vertebrate taxa globally. While there are many reasons for declines, recently disease has been identified as the primary cause of catastrophic population crashes. One disease in particular, chytridiomycosis, caused by the fungal pathogen Batrachochytrium dendrobatidis, Bd, is considered the worst pathogen to cause biodiversity loss. Declines of amphibians due to Bd infection began in the 1970s, and since then, numerous species have gone from being widespread and at high density to contracted populations near extinction. Much effort and research has been aimed at reversing these population declines but the disease is widespread with high prevalence and impacts. The purpose of this thesis is to explore how Bd infection affects declining amphibian species in Australia, with a focus on pathogenesis of the disease, mechanisms of population persistence and how understanding disease ecology can inform management techniques.

There were five major components of this project. Aim 1: to explore the disease ecology of a threatened and declining species and trial reintroduction as a management technique. Aim 2: to investigate the effect of disease on reproduction. Aim 3: to investigate underexplored mechanisms of pathogenesis of disease in susceptible species, specifically lymphocyte depletion and apoptosis. Aim 4: to investigate population differences on susceptibility of infection in a susceptible and endangered species. Aim 5: to explore new potential treatment options for captive colonies. I focused my investigations on declining or endangered alpine species of Australia, using two species: Pseudophryne corroboree and Litoria verreauxii alpina. In each chapter I used one or both of these species to explore the aims.

For the first aim, I trialled an amphibian reintroduction and explored disease ecology in wild populations of L. v. alpina. Captive raised animals were released into sites that held current populations and sites from which the species had been extirpated. Reintroduced animals initially fared well after reintroduction suggesting that reintroduction could be used as a management technique. However, infection increased throughout the breeding season and recovery from infection was low, suggesting that all animals succumbed to disease at the end of the breeding season, whether reintroduced or extant. These results suggest that while the populations are persisting at certain sites, the populations are experiencing near population turnover each year and disease resistance is not evolving.

For the second aim, I investigated the effect of disease on reproduction, specifically gametogenesis. Surprisingly, both spermatogenesis and oogenesis increased in experimentally infected animals. Therefore, increased reproduction might be an important mechanism of population persistence, and might be more important than immunity in these species. However, although increased reproduction and high recruitment may be effective in enabling population persistence in the short term, it appears a precarious strategy as it relies on annual success. These results also suggest that it is important to explore novel and understudied mechanisms of population persistence, which may impact management priorities.

Pathogenesis of Bd infection on understudied susceptible species was explored in Aim 4 by examining two potential aspects of the immune response in experimentally infected animals: hematopoietic tissue depletion and epidermal apoptosis. Quantifying hematopoietic tissue using histology showed leucocytes were depleted in infected animals, but this effect varied among species and tissue types examined (ie spleen, bone marrow and kidney). My results appear to confirm previous in vitro studies showing Bd releases immunosuppressive compounds. Assessing epidermal apoptosis using TUNEL assays and caspase activity revealed that apoptosis was suppressed early in infection, but then apoptosis increased reaching high levels at terminal stages of disease. These aspects of pathogenesis varied between individuals and species, suggesting that animals that can resist hematopoietic depletion and modulate epidermal apoptosis will be more likely to minimise infection risk and outcomes.

The fourth aim was to investigate population differences in susceptibility to Bd infection in remnant populations of a critically endangered species. I exposed P. corroboree sourced from four populations, and found that one population was more resistant, exhibiting decreased infection load and increased survivorship. This population can be utilised to identify mechanisms of resistance for incorporating into captive breeding programs.

The final aim was to explore new treatment options, because maintaining disease free colonies of amphibians is imperative to the conservation effort. I explored decreased humidity as a treatment and found it to be unsuccessful. I also trialled an intensive combination of electrolyte replacement and antifungal chemotherapy in an attempt to cure frogs with late stage disease, but only one frog recovered. But, there was an increased survival time, suggesting that there is potential to treat frogs with severe chytridiomycosis.

Research over the past decade on the impacts, outcomes and immune mechanisms of chytridiomycosis on amphibians has shown species vary widely. Although it is easier to use model species, it is important to study susceptible and declining amphibians to develop targeted and context specific conservation solutions. My research on pathogenesis has produced evidence for improved captive breeding and treatment. Field and laboratory studies on disease ecology, potential reservoir hosts and mechanisms of population persistence will inform management opportunities targeted at protecting these declining species. For example I have shown that supporting annual reproduction may be more feasible and effective than reducing mortality rates.

Item ID: 49467
Item Type: Thesis (PhD)
Keywords: amphibian decline, amphibian, apoptosis, batrachochytrium dendrobatidis, capture-mark-recapture, caspases, chytrid fungus, chytridiomycosis, conditional Arnason–Schwarz model, dry treatment, fitness, haematopoiesis, hematopoietic tissue, histology, infection, itraconazole, marking methods, non-chemotherapeutic treatment, oogenesis, passive integrative transponder tags, pathogenesis, Pseudophryne corroboree, reintroduction, reproduction, spermatogenesis, terminal investment, toe clip, treatment, TUNEL, visual implant elastomer tags, voriconazole, wildlife disease
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Publications arising from this thesis are available from the Related URLs field. The publications are:

Chapter 2: Brannelly, Laura A., Hunter, David A., Lenger, Daniel, Scheele, Ben C., Skerratt, Lee F., and Berger, Lee (2015) Dynamics of chytridiomycosis during the breeding season in an Australian alpine amphibian. PLoS ONE, 10 (12). pp. 1-15.

Chapter 2: Brannelly, L.A., Hunter, D.A., Skerratt, L.F., Scheele, B.C., Lenger, D., McFadden, M.S., Harlow, P.S., and Berger, L. (2016) Chytrid infection and post-release fitness in the reintroduction of an endangered alpine tree frog. Animal Conservation, 19 (2). pp. 153-162.

Chapter 2: Brannelly, Laura A., Berger, Lee, and Skerratt, Lee F. (2014) Comparison of three widely used marking techniques for adult anuran species Litoria verreauxii alpina. Herpetological Conservation and Biology, 9 (2). pp. 428-435.

Chapter 3: Brannelly, Laura A., Webb, Rebecca, Skerratt, Lee F., and Berger, Lee (2016) Amphibians with infectious disease increase their reproductive effort: evidence for the terminal investment hypothesis. Open Biology, 6.

Chapter 4: Brannelly, Laura A., Webb, Rebecca J., Skerratt, Lee F., and Berger, Lee (2016) Effects of chytridiomycosis on hematopoietic tissue in the spleen, kidney and bone marrow in three diverse amphibian species. Pathogens and Disease, 74 (7). pp. 1-10.

Chapter 5: Brannelly, Laura A., Roberts, Alexandra A., Skerratt, Lee F., and Berger, Lee (2017) Epidermal cell death in frogs with chytridiomycosis. PeerJ, 5. pp. 1-20.

Chapter 7: Brannelly, Laura A., Berger, Lee, Marantelli, Gerry, and Skerratt, Lee F. (2015) Low humidity is a failed treatment option for chytridiomycosis in the critically endangered southern corroboree frog. Wildlife Research, 42 (1). pp. 44-49.

Chapter 7: Brannelly, Laura A., Skerratt, Lee F., and Berger, Lee (2015) Treatment trial of clinically ill corroboree frogs with chytridiomycosis with two triazole antifungals and electrolyte therapy. Veterinary Research Communications, 39 (3). pp. 179-187.

Date Deposited: 05 Jul 2017 03:12
FoR Codes: 06 BIOLOGICAL SCIENCES > 0602 Ecology > 060207 Population Ecology @ 30%
06 BIOLOGICAL SCIENCES > 0605 Microbiology > 060502 Infectious Agents @ 40%
07 AGRICULTURAL AND VETERINARY SCIENCES > 0707 Veterinary Sciences > 070704 Veterinary Epidemiology @ 30%
SEO Codes: 86 MANUFACTURING > 8609 Veterinary Pharmaceutical Products > 860903 Veterinary Pharmaceutical Treatments (e.g. Antibiotics) @ 10%
92 HEALTH > 9204 Public Health (excl. Specific Population Health) > 920405 Environmental Health @ 60%
96 ENVIRONMENT > 9608 Flora, Fauna and Biodiversity > 960807 Fresh, Ground and Surface Water Flora, Fauna and Biodiversity @ 30%
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