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Heat tolerance of reptile embryos in a changing world: Physiological mechanisms and ecological effects


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dc.contributor.advisorWarner, Daniel
dc.contributor.authorHall, Joshua Matthew
dc.date.accessioned2020-07-09T13:53:37Z
dc.date.available2020-07-09T13:53:37Z
dc.date.issued2020-07-09
dc.identifier.urihttp://hdl.handle.net/10415/7268
dc.description.abstractAspects of global change (e.g. climate change, urbanization) create stressful thermal environments that threaten biodiversity. Oviparous, non-avian reptiles have received considerable attention because eggs are left to incubate under prevailing conditions, leaving developing embryos vulnerable to increases in temperature. Though many studies assess embryo responses to long-term (i.e. chronic) incubation temperatures, few assess responses to acute exposures which are more relevant for many species and may become more common due to global change. Because warming temperatures cause increases in both mean and variance of nest temperatures, it is crucial to consider embryo responses to both chronic and acute heat stress. Currently, there are no standard metrics or terminology for determining heat stress of embryos. This impedes comparisons across studies and species and hinders our ability to predict how species will respond to warming temperatures. In Chapter 1, I compare various methods that have been used to assess embryonic heat tolerance in reptiles and provide new terminology and metrics for quantifying embryo responses to both chronic and acute heat stress. I apply these recommendations to data from the literature to assess chronic heat tolerance in 16 squamates, 16 turtles, 5 crocodilians, and the tuatara and acute heat tolerance for 9 squamates and 1 turtle. My results indicate there is relatively large variation in chronic and acute heat tolerance across species, and I outline directions for future research, calling for more studies that assess embryo responses to acute thermal stress and identify mechanisms that determine heat tolerance. In Chapters 2, 3 and 4, I make progress toward both these goals. In Chapter 2, to better understand the effects of acute thermal stress on development, I subjected brown anole (Anolis sagrei) eggs to heat shocks, thermal ramps, and extreme diurnal fluctuations to determine the lethal temperature of embryos, measure the thermal sensitivity of embryo heart rate and metabolism, and quantify the effects of sub-lethal but stressful temperatures on development and hatchling phenotypes and survival. Most embryos died at heat shocks of 45 or 46 °C, which is ~12 °C warmer than the highest constant temperatures suitable for successful development (i.e. chronic heat stress). Heart rate and O2 consumption increased with temperature; however, as embryos approached the lethal temperature, heart rate and CO2 production continued rising while O2 consumption plateaued. These data indicate a mismatch between oxygen supply and demand at high temperatures. Exposure to extreme, diurnal fluctuations depressed embryo developmental rates and heart rates, and resulted in hatchlings with smaller body size, reduced growth rates, and lower survival in the laboratory. Thus, even brief exposure to extreme temperatures can have important effects on embryo development, and Chapter 2 highlights the role of both immediate and cumulative effects of high temperatures on egg survival. In Chapter 3, I consider how increased nest temperatures due to urbanization (i.e. the urban heat island effect) influence embryo development. In reptiles, relatively warm incubation temperatures increase developmental rate and often enhance fitness-relevant phenotypes, but extremely high temperatures cause death. Human-altered habitats (i.e., cities) potentially create unusually warm nest conditions that differ from adjacent natural areas in both mean and extreme temperatures. Such variation may exert selection pressures on embryos. To address this, I measured soil temperatures in places where the Puerto Rican crested anole lizard (A. cristatellus) nests in both city and forest habitats. I bred anoles in the laboratory and subjected their eggs to 5 incubation treatments that mimicked temperature regimes from the field, three of which included brief exposure to extremely high temperatures (i.e. thermal spikes) measured in the city. I monitored growth and survival of hatchlings in the laboratory for three months and found that warmer, city temperatures increase developmental rate, but brief, thermal spikes reduce survival. Hatchling growth and survival were unaffected by incubation treatment. Thus, the urban landscape can potentially create selection pressures that influence organisms at early life stages. Finally, studies that examine thermal tolerance of embryos rarely assess the potential for tolerance to change with ontogeny or how effects differ among sympatric species, and often utilize unrealistic temperature treatments. In Chapter 4, I used thermal fluctuations from nests within the urban-heat island to determine how thermal tolerance of embryos changes across development and differs between two sympatric lizards (A. sagrei and A. cristatellus). I applied fluctuations that varied in frequency and magnitude at different times during development and measured effects on embryo physiology, egg survival, and hatchling morphology, growth, and survival. Thermal tolerance differed between the species by ~ 2 °C: embryos of A. sagrei, a lizard that prefers warmer, open-canopy microhabitats, were more robust to thermal stress than embryos of A. cristatellus, which prefers cooler, closed-canopy microhabitats. Moreover, thermal tolerance changed through development; however, the nature of this change differed between the species. For A. cristatellus, thermal tolerance was greatest mid-development. For A. sagrei the relationship was not statistically clear. The greatest effects of thermal stress were on embryo and hatchling survival and embryo physiology. Hatchling morphology and growth were less affected. Collectively, the chapters of this dissertation demonstrate that inter-specific responses and the timing of stochastic thermal events with respect to development have important effects on egg survival. Thus, research that integrates responses to both acute and chronic thermal stress using ecologically-meaningful thermal treatments and examines interspecific responses will be critical to make robust predictions of the impacts of global change on wildlife.en_US
dc.subjectBiological Sciencesen_US
dc.titleHeat tolerance of reptile embryos in a changing world: Physiological mechanisms and ecological effectsen_US
dc.typePhD Dissertationen_US
dc.embargo.statusNOT_EMBARGOEDen_US
dc.contributor.committeeGuyer, Craig
dc.contributor.committeeWada, Haruka
dc.contributor.committeeLangkilde, Tracy
dc.contributor.committeeStoeckel, James
dc.creator.orcid0000-0002-5587-3402en_US

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