Oxygen concentration affects upper thermal tolerance in a terrestrial vertebrate

Journal of Experimental Biology

Holden

Telemeco

et al. 2016

Extreme temperatures constrain organismal physiology and impose both acute and chronic effects. Additionally, temperature-induced hormone-mediated stress response pathways and energetic tradeoffs are important drivers of life-history variation. This study employs an integrative approach to quantify acute physiological responses to high temperatures in divergent life-history ecotypes of the western terrestrial garter snake (Thamnophis elegans). Using wild-caught animals, we measured oxygen consumption rate and physiological markers of hormonal stress response, energy availability and anaerobic respiration in blood plasma across five ecologically relevant temperatures (24, 28, 32, 35 and 38°C; 3 h exposure). Corticosterone, insulin and glucose concentrations all increased with temperature, but with different thermal response curves, suggesting that high temperatures differently affect energy-regulation pathways. Additionally, oxygen consumption rate increased without plateau and lactate concentration did not increase with temperature, challenging the recent hypothesis that oxygen limitation sets upper thermal tolerance limits. Finally, animals had similar physiological thermal responses to high-temperature exposure regardless of genetic background, suggesting that local adaptation has not resulted in fixed differences between ecotypes. Together, these results identify some of the mechanisms by which higher temperatures alter hormonal-mediated energy balance in reptiles and potential limits to the flexibility of this response.

Section: Discussionsupporting

confidence: 85%

Hormonal and metabolic responses to upper temperature extremes in divergent life-history ecotypes of a garter snake

Journal of Experimental Biology

Holden

Telemeco

et al. 2016

“…Under the OCLTT hypothesis, hypoxia is predicted to reduce thermal optima and tolerance limits (Smith et al 2015;Verberk et al 2016;DuBois et al 2017), and this prediction is somewhat supported in reptiles and amphibians. For example, CT MAX , preferred body temperature (PBT), panting temperature (T PANT ), and gaping temperature (T GAPE ) are reduced when diverse species are exposed to very-low oxygen environments (< 10 kPa; mostly lizards examined; Hicks and Wood 1985;Dupre et al 1986;Branco et al 1993;Cadena and Tattersall 2009;Shea et al 2016;DuBois et al 2017;Fig. 2) and when hematocrit is experimentally reduced (only PBT examined; Hicks and Wood 1985;Wood 1990).…”

Section: Organ-system Mechanismsmentioning

confidence: 99%

High Temperature, Oxygen, and Performance: Insights from Reptiles and Amphibians

Integrative and Comparative Biology

Telemeco

2018

106

Much recent theoretical and empirical work has sought to describe the physiological mechanisms underlying thermal tolerance in animals. Leading hypotheses can be broadly divided into two categories that primarily differ in organizational scale: 1) high temperature directly reduces the function of subcellular machinery, such as enzymes and cell membranes, or 2) high temperature disrupts system-level interactions, such as mismatches in the supply and demand of oxygen, prior to having any direct negative effect on the subcellular machinery. Nonetheless, a general framework describing the contexts under which either subcellular component or organ system failure limits organisms at high temperatures remains elusive. With this commentary, we leverage decades of research on the physiology of ectothermic tetrapods (amphibians and non-avian reptiles) to address these hypotheses. Available data suggest both mechanisms are important. Thus, we expand previous work and propose the Hierarchical Mechanisms of Thermal Limitation (HMTL) hypothesis, which explains how subcellular and organ system failures interact to limit performance and set tolerance limits at high temperatures. We further integrate this framework with the thermal performance curve paradigm commonly used to predict the effects of thermal environments on performance and fitness. The HMTL framework appears to successfully explain diverse observations in reptiles and amphibians and makes numerous predictions that remain untested. We hope that this framework spurs further research in diverse taxa and facilitates mechanistic forecasts of biological responses to climate change.

“…Given that neither V̇O 2 nor glucose concentration plateaued at high temperatures and that lactate concentration did not escalate with temperature, these snakes are not limited by oxygen acquisition or transport at temperatures near their thermal maximum. This result is in accordance with recent studies that refute the OCLTT hypothesis in free-living stages of terrestrial ectotherms He et al, 2013;McCue and Santos, 2013;; but see Shea et al, 2016). Our data do not address other possible mechanisms that may contribute to thermal tolerance limits, including protein denaturation, membrane fluidity, enzyme-substrate interactions, mitochondrial failure and failure of neural processes (reviewed in .…”

Section: Discussionsupporting

confidence: 87%

Ecology and evolution of physiological phenotypes in garter snakes (Thamnophis spp.)

First, my family: Becky, James, and Anna, whose immense support and patience made possible this adventure, and all our others. For my mom and dad, who tirelessly supported my pursuits even when they involved bringing home wild animals that sometimes escaped in the house. Mark, who has never held a snake but loves me anyway. Jason, whose passion for science and learning continues to inspire me. My Nina, who thinks that what I do is the greatest thing in the world. And Carol, Bill, Melissa, Matt, Bill, Shayna, Caleb, Ceci, Billy, and Ryan, whose love and support is remarkable. Thank you to Anne, a superlative scientist and incredible advisor. I am especially grateful for your patience and trusting support through this process. I've never had mentor for whom I've had more respect. My committee members, both current and past, have provided invaluable guidance: