Thermal thresholds in the amphibian disease chytridiomycosis

Greenspan, Sasha Eden (2017) Thermal thresholds in the amphibian disease chytridiomycosis. PhD thesis, James Cook University.

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Recent emergences of fungal diseases have caused catastrophic global losses of biodiversity and temperature strongly influences many host-fungus associations. Ectothermic host body temperatures fluctuate diurnally, seasonally, and annually, but our understanding of the effects of host temperature variability on disease development remains incomplete. My thesis focuses on the effects of host temperature variation on interactions between frog hosts and the widely distributed fungal parasite Batrachochytrium dendrobatidis (Bd), which causes the disease chytridiomycosis. I first designed and validated a set of economical, fluctuating-temperature chambers (Chapter 2) that forms the core research infrastructure for four laboratory experiments (Chapters 3–6). Chapter 3 compares frog immune responses after temperature shifts (increases and decreases). Cold-acclimated frogs treated with a dose of Bd and a temperature increase had active immune systems before and after treatment. In contrast, hot-acclimated frogs treated with a dose of Bd and a temperature decrease had active immune systems only after treatment and had higher Bd burdens than the cold-acclimated frogs. My results suggest that cold acclimation may prime the immune system for some challenges of infection and help to explain the observation that susceptibility to Bd tends to be lower after temperature increases than after temperature decreases. In Chapter 4, I demonstrate that heavy Bd infections increased the heat sensitivity of frog hosts. 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. My results suggest that increased heat sensitivity from infections may at times discourage these protective behaviors, tipping the balance in favor of the parasite. Chapters 5–6 center on effects of diurnal temperature variability on Bd growth and the course of Bd infections. In the Australian Wet Tropics species Litoria serrata, daily body temperatures may regularly exceed the thermal optimum of the fungus, so I focus on effects of these 'heat spikes.' In Chapter 5, I exposed Bd cultures and Bd-infected frogs to thermal regimes representing population medians of body temperatures and of daily heat spikes experienced by L. serrata. Compared to cool constant-temperature control treatments, Bd grew more slowly in the heat spike treatments and frogs that experienced heat spikes developed Bd infections more slowly, were less likely to exceed lethal infection intensities, and were more likely to clear infections. In Chapter 6, I examined the field body temperature regimes of individual L. serrata and exposed Bd cultures to heat spike treatments representing individual frogs. My data revealed evidence that L. serrata appear to thermoregulate. In uplands in summer and in lowlands in winter, most frogs regularly elevated their body temperatures above the thermal optimum range for Bd. In contrast, frogs appeared unable to reach such elevated temperatures in uplands in winter. These results are consistent with the previous finding that prevalence of Bd in the Wet Tropics tends to be highest in winter at elevations above 400 m, but for the first time, I linked population-level seasonal and elevational patterns in infection prevalence to host body temperature at the scale of the individual frog. In addition, growth of Bd cultures was highly responsive to temperature regimes reproducing the fluctuating body temperatures of individual frogs. Overall, this thesis highlights the direct effects of temperature variability on the course and outcome of Bd infections and underscores the importance of individual body temperatures and thermoregulatory behaviors, in addition to population averages, in predicting climate-dependent chytridiomycosis dynamics. Understanding the effects of temperature variability on host-pathogen interactions will remain critical as we continue to confront the realities of the effects of anthropogenic climate change on biodiversity.

Item ID: 53032
Item Type: Thesis (PhD)
Keywords: amphibian, applied ecology, Batrachochytrium dendrobatidis, body condition, calling effort, chytridiomycosis, disease, disease ecology, frog calling, immunity, incubator, leukocytes, life-history trade-offs, mate attraction, microbial ecology, replication, sublethal effects, temperature variability, thermal acclimation, thermal biology, vocalization
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Publications arising from this thesis are available from the Related URLs field. The publications are:

Chapter 2: Greenspan, Sasha E., Morris, Wayne, Warburton, Russell, Edwards, Lexie, Duffy, Richard, Pike, David, Schwarzkopf, Lin, and Alford, Ross A. (2016) Low-cost fluctuating-temperature chamber for experimental ecology. Methods in Ecology and Evolution, 7. pp. 1567-1574.

Chapter 3: Greenspan, Sasha E., Bower, Deborah S., Webb, Rebecca J., Berger, Lee, Rudd, Donna, Schwarzkopf, Lin, and Alford, Ross A. (2017) White blood cell profiles in amphibians help to explain disease susceptibility following temperature shifts. Developmental and Comparative Immunology, 77. pp. 280-286.

Chapter 4: Greenspan, Sasha E., Bower, Deborah S., Roznik, Elizabeth A., Pike, David A., Marantelli, Gerry, Alford, Ross A., Schwarzkopf, Lin, and Scheffers, Brett R. (2017) Infection increases vulnerability to climate change via effects on host thermal tolerance. Scientific Reports, 7.

Chapter 5: Greenspan, Sasha E., Bower, Deborah S., Webb, Rebecca J., Roznik, Elizabeth A., Stevenson, Lisa A., Berger, Lee, Marantelli, Gerry, Pike, David A., Schwarzkopf, Lin, and Alford, Ross A. (2017) Realistic heat pulses protect frogs from disease under simulated rainforest frog thermal regimes. Functional Ecology, 31. pp. 2274-2286.

Appendix: Greenspan, Sasha E., Roznik, Elizabeth A., Schwarzkopf, Lin, Alford, Ross A., and Pike, David A. (2016) Robust calling performance in frogs infected by a deadly fungal pathogen. Ecology and Evolution, 6 (16). pp. 5964-5972.

Date Deposited: 03 Apr 2018 23:04
FoR Codes: 06 BIOLOGICAL SCIENCES > 0605 Microbiology > 060502 Infectious Agents @ 34%
06 BIOLOGICAL SCIENCES > 0608 Zoology > 060806 Animal Physiological Ecology @ 33%
05 ENVIRONMENTAL SCIENCES > 0501 Ecological Applications > 050101 Ecological Impacts of Climate Change @ 33%
SEO Codes: 96 ENVIRONMENT > 9603 Climate and Climate Change > 960305 Ecosystem Adaptation to Climate Change @ 34%
96 ENVIRONMENT > 9604 Control of Pests, Diseases and Exotic Species > 960499 Control of Pests, Diseases and Exotic Species not elsewhere classified @ 33%
96 ENVIRONMENT > 9608 Flora, Fauna and Biodiversity > 960899 Flora, Fauna and Biodiversity of Environments not elsewhere classified @ 33%
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