Infection increases vulnerability to climate change via effects on host thermal tolerance

Unprecedented global climate change and increasing rates of infectious disease emergence are occurring simultaneously. Infection with emerging pathogens may alter the thermal thresholds of hosts. However, the effects of fungal infection on host thermal limits have not been examined. Moreover, the influence of infections on the heat tolerance of hosts has rarely been investigated within the context of realistic thermal acclimation regimes and potential anthropogenic climate change. We tested for effects of fungal infection on host thermal tolerance in a model system: frogs infected with the chytrid Batrachochytrium dendrobatidis. Infection reduced the critical thermal maxima (CTmax) of hosts by up to ~4 °C. Acclimation to realistic daily heat pulses enhanced thermal tolerance among infected individuals, but the magnitude of the parasitism effect usually exceeded the magnitude of the acclimation effect. In ectotherms, behaviors that elevate body temperature may decrease parasite performance or increase immune function, thereby reducing infection risk or the intensity of existing infections. However, increased heat sensitivity from infections may discourage these protective behaviors, even at temperatures below critical maxima, tipping the balance in favor of the parasite. We conclude that infectious disease could lead to increased uncertainty in estimates of species’ vulnerability to climate change

A project that designs and trials a pilot survey to map the distribution of chyridomycosis (caused by the amphibian chytrid fungus) in Australian frogs

[Extract] The aim of this tender was to design and trial a pilot survey to map the distribution of chytridiomycosis in Australian frogs. The project has 5 components: Scope Items 1 and 3 being desk top synthesis and evaluation activities, Scope Item 2 being a data gathering and proof of concept activity, Scope Item 4 being a field and laboratory based project testing the protocol developed in Scope Item 3, and Scope Item 5 assessing and evaluating the previous outputs and providing recommendations that need to be addressed to allow a national survey for chytridiomycosis to proceed in an effective manner. Diagnostic Tests: An analysis of published and unpublished literature identified that chytridiomycosis could be diagnosed by at least 11 tests, that can be collapsed into 5 categories; culture, microscopical examination of unstained epidermis, histology, capture ELISA and PCR. Although each diagnostic test has detection of the amphibian chytrid fungus, Batrachochytrium dendrobatidis (Bd), as its final outcome and could on superficial assessment appear to be competing with each other, we discovered that this was true only in part. The tests have different functions and complement, rather than exclude, one another. For example, examination of fresh tissue is an essential test when culture of B.dendrobatidis from infected skin is being attempted in the laboratory. Histology is the diagnostic test of choice for retrospective surveys of archived specimens, and the sensitivity of diagnosis is increased by immunohistochemistry using polyclonal antibodies. For the proposed mapping survey, real-time PCR is the recommended diagnostic technique owing to its increased sensitivity and non-invasiveness

Red hot frogs:Identifying the Australian frogs most at risk of extinction

More than a third of the world’s amphibian species are listed as Threatened or Extinct, with a recent assessment identifying 45 Australian frogs (18.4% of the currently recognised species) as ‘Threatened’ based on IUCN criteria. We applied structured expert elicitation to 26 frogs assessed as Critically Endangered and Endangered to estimate their probability of extinction by 2040. We also investigated whether participant experience (measured as a self-assigned categorical score, i.e. ‘expert’ or ‘non-expert’) influenced the estimates. Collation and analysis of participant opinion indicated that eight species are at high risk (>50% chance) of becoming extinct by 2040, with the disease chytridiomycosis identified as the primary threat. A further five species are at moderate–high risk (30–50% chance), primarily due to climate change. Fourteen of the 26 frog species are endemic to Queensland, with many species restricted to small geographic ranges that are susceptible to stochastic events (e.g. a severe heatwave or a large bushfire). Experts were more likely to rate extinction probability higher for poorly known species (those with <10 experts), while non-experts were more likely to rate extinction probability higher for better-known species. However, scores converged following discussion, indicating that there was greater consensus in the estimates of extinction probability. Increased resourcing and management intervention are urgently needed to avert future extinctions of Australia’s frogs. Key priorities include developing and supporting captive management and establishing or extending in-situ population refuges to alleviate the impacts of disease and climate change

Emerging disease of amphibians cured by elevated body temperature

The emerging infectious disease chytridiomycosis is thought to have contributed to many of the recent alarming declines in amphibian populations. Mortalities associated with these declines have often occurred during cooler seasons and at high elevations, suggesting that environmental temperature may be an important factor in disease emergence. We found that thermal environment affects the progress of the disease, and that housing frogs Litoria chloris at an environmental temperature of 37°C for less than 16 h can clear them of the chytrid pathogen Batrachochytrium dendrobatidis. Our experiment demonstrated that elevated body temperatures similar to those experienced in behavioral fever and during normal thermoregulation can clear frogs of chytrid infection; therefore, variation in thermoregulatory opportunities and behaviors are likely to contribute to the differences in disease incidence observed among host species, populations, and regions. Although further refinement of the technique is needed to encompass various host species, appropriately applied thermal manipulations of amphibians and their enclosures may prove to be a safe and effective way of eliminating the fungal pathogen from captive amphibian populations and preventing accidental spread of the pathogen when animals are translocated or released from captivity

Distribution of the amphibian chytrid Batrachochytrium dendrobatidis and keratin during tadpole development

A large outbreak of chytridiomycosis occurred in captive metamorphs of Mixophyes fasciolatus that died between 9 and 25 days post metamorphosis. The mortality rate in infected tubs was 100% and more than 500 frogs died. Examination of the husbandry records suggested that tadpoles had been infected before two weeks of age. However, a sample of tadpoles separated before hatching remained uninfected. We studied the changes in distribution of keratin and sporangia of Batrachochytrium dendrobatidis in tadpoles during development, by examination of histology sections stained with Ayoub-Shklar stain. Keratin occurred only on the mouthparts during most of tadpole life, and appeared on the feet shortly before metamorphosis. At metamorphosis the keratinized mouthparts are shed before keratin forms on the skin of the body. B. dendrobatidis only occurred on keratinized, stratified epidermis and followed the changes in distribution. There is a rapid redistribution of B. dendrobatidis at metamorphosis leading to fatal infection in M. fasciolatus. These findings are useful considerations when translocating tadpoles as well as for diagnosis and treatment

Virulence of the amphibian chytrid fungus Batrachochytrium dendrobatidis varies with the strain

Although mortality in 3 groups of 15 green tree frogs Litoria caerulea exposed to 3 isolates of Batrachochytrium dendrobatidis was 100%, time to death varied with isolate, highlighting the importance of strain and/or passage history in pathogenicity studies and possibly in the epidemiology of chytridiomycosis. A standard naming scheme for isolates of B. dendrobatidis is proposed

Low humidity is a failed treatment option for chytridiomycosis in the critically endangered southern corroboree frog

Context: One of the major drivers of the current worldwide amphibian decline and extinction crisis is the spread of the amphibian chytrid fungus, Batrachochytrium dendrobatidis (Bd). Captive assurance colonies may be the only lifeline for some species. Current antifungal chemotherapies can be effective for clearing infection but may have detrimental side effects. The only non-chemotherapeutic treatment that has been clinically tested is heat, which is impractical for cold-adapted species. The fungus does not survive desiccation, and therefore a plausible alternative non-chemotherapeutic treatment would be a low-humidity regimen.\ud \ud Aims: We tested the efficacy of a low-humidity treatment regimen for treating Bd-infected animals of the critically endangered species Pseudophryne corroboree. This species has high tolerance of dry environments, and is thus an ideal candidate for this treatment trial.\ud \ud Methods: Forty frogs were exposed to 1 × 106 zoospores. At three weeks after exposure access to water was reduced to once daily for 10 days for 20 animals. Ten of these animals were also rinsed daily with the aim of removing zoospores.\ud \ud Key results: The drying regimen neither increased survival nor decreased infection load, and treatment may have hastened mortality. All infected frogs died between 21 and 80 days after exposure, except one untreated frog.\ud \ud Conclusions: Our results suggest that a drying regimen is not a viable treatment for chytridiomycosis. Infection may decrease the host's ability to cope with water stress.\ud \ud Implications: The failed drying treatment in P. corroboree suggests that drying is not an appropriate treatment for chytridiomycosis and treatment efforts should be focussed on chemotherapies for cold-adapted species. P. corroboree is a critically endangered species for which chytridiomycosis is the primary cause of decline, yet few experiments have been carried out on this species with regards to chytridiomycosis. All experimental information about this species and disease will benefit the management and protection of the species

Optimal release strategies for cost-effective reintroductions

1. Ex situ programmes for endangered species commonly focus on two main objectives: insurance against immediate risk of extinction and reintroduction. Releases influence the size of captive and wild populations and may present managers with a trade-off between the two objectives. This can be further complicated when considering the costs of the captive population and the possible release of different life stages. 2. We approached this decision problem by combining population models and decision-analytic methods, using the reintroduction programme for the southern corroboree frog Pseudophryne corroboree in Australia as an example. We identified the optimal release rates of eggs and subadults which maximized the size of the captive and reintroduced populations while meeting constraints. We explored two scenarios: a long-term programme for a stable age-distributed captive population and a short-term programme with non-stable age distribution and limited budget. We accounted for uncertainty in the estimated vital rates and demographic stochasticity. 3. Assuming a stable age distribution, large proportions of individuals could be released without decreasing the captive population below its initial size. The optimal strategy was sensitive to the post-release survival of both life stages, but subadult releases were generally most cost-effective, producing a large wild population and requiring a cheaper captive population. Egg releases were optimal for high expected juvenile survival, whereas mixed releases of both life stages were never optimal. 4. In the short-term realistic scenario, subadult releases also produced the largest wild population, but they required a large increase in the size and cost of the captive population that exceeded the available budget. Egg releases were cheaper but yielded smaller numbers in the wild, whereas joint releases of both life stages provided more wild individuals, meeting budget constraints without depleting the captive population. 5. Synthesis and applications. Optimal release strategies for endangered species reflect the trade-offs between insurance and reintroduction objectives and depend on the vital rates of the released individuals. Although focusing on a single life stage may have practical advantages, mixed strategies can maximize cost-effectiveness by combining the relative advantages of releasing early and late life stages

Presence of the amphibian chytrid fungus Batrachochytrium dendrobatidis in threatened corroboree frog populations in the Australian Alps

Since the early 1980s, the southern corroboree frog Pseudophryne corroboree and northern corroboree frog P. pengilleyi have been in a state of decline from their sub-alpine and high montane bog environments on the southern tablelands of New South Wales, Australia. To date, there has been no adequate explanation as to what is causing the decline of these species. We investigated the possibility that a pathogen associated with other recent frog declines in Australia, the amphibian chytrid fungus Batrachochytrium dendrobatidis, may have been implicated in the decline of the corroboree frogs. We used histology of toe material and real-time PCR of skin swabs to investigate the presence and infection rates with B. dendrobatidis in historic and extant populations of both corroboree frog species. Using histology, we did not detect any B. dendrobatidis infections in corroboree frog populations prior to their decline. However, using the same technique, high rates of infection were observed in populations of both species after the onset of substantial population declines. The real-time PCR screening of skin swabs identified high overall infection rates in extant populations of P. corroboree (between 44 and 59%), while significantly lower rates of infection were observed in low-altitude P. pengilleyi populations (14%). These results suggest that the initial and continued decline of the corroboree frogs may well be attributed to the emergence of B. dendrobatidis in populations of these species