Article in Focus: High temperature, oxygen, and performance: Insights from reptiles and amphibians

Post written by Dr. Eric Gangloff

Elgaria multicarinata, the Southern Alligator Lizard. Photo: E. Gangloff & R. Telemeco

While graduate students at Iowa State University, Rory and I participated in many discussion groups and conferred about new and exciting ideas in eco-physiology. From these conversations naturally flowed research collaborations. At one point we became intensely interested in the oxygen- and capacity-limited thermal tolerance (OCLTT) hypothesis, as put forth by Hans-Otto Pörtner and colleagues, about which there has been much lively debate. We realized that this hypothesis was relatively unexplored in reptiles, our taxa of preference, and set out to design experiments to test this hypothesis. We also became excited about some of the new possibilities to gain high-throughput physiological data. Rory had recently conducted an experiment with alligator lizards (Elgaria coerulea and E. multicarinata), designed to test for variation in response to thermal stress in these two closely-related species. With samples of skeletal muscle from this experiment, we utilized a metabolomics approach to identify differences in metabolites between heat-stressed and non-stressed animals and between species (Telemeco et al. J Anim Ecol 2017). Concurrently, we tested the hormonal and metabolic response to garter snakes (Thamnophis elegans) exposed to extreme but sub-lethal temperatures (Gangloff et al. J Exp Biol 2016). To our surprise, the results of both experiments provided rather robust results refuting the importance of the OCLTT mechanism in setting thermal tolerance limits in these species. So what then? We continued our discussions and collaborations, both on classroom whiteboards and over beers, and decided to challenge ourselves with a review/commentary paper.

Ideas flowing. Photo: E. Gangloff & R. Telemeco

After graduating, Rory took a post-doc position at the University of Washington where he conducted further work in this area. This included one study with lizard (Sceloporus tristichus) eggs, providing support for oxygen capacity playing an important role setting tolerance limits in lizard embryos (Smith et al. Biol Lett 2015). With this result and some other studies published around the same time, our ideas began to germinate. By combining current theoretical work on thermal tolerance limits in fishes with decades of great physiological studies in reptiles and amphibians, we could propose an integrative framework to predict when and how different mechanisms would set thermal tolerance limits. The broad ideas were there, we had lots of papers to read, so then…we just needed to figure out how to make time to put it all together. Last winter, we were able to arrange for Rory to give a departmental seminar at Iowa State University – where I was working as a post-doc – which allowed us to spend a week working on this manuscript. We hunkered down for the most part in a basement room with a couple computers and a whiteboard, hashing out ideas. It proved to be enormously productive (and fun!). We set a timetable to complete a full draft of the manuscript within a couple months. We were able to do this just as I began a new post-doc position at the Station d’Ecologie Théorique et Expérimentale du CNRS in Moulis, France. Here, I am studying how oxygen limitation interacts with temperature regime to limit high-altitude colonization in the lizard Podarcis muralis (read more about this work in the project’s blog). Perfect!

After several rounds of re-naming, we are now very pleased to present the Hierarchical Mechanisms of Thermal Limits (HMTL) hypothesis with our paper: “High temperature, oxygen, and performance: Insights from reptiles and amphibians.” With this commentary, we seek to integrate ideas about how either subcellular components or organ systems first suffer under exposure to high temperatures and thus set thermal limits in ectotherms. Furthermore, we hope to merge the well-established thermal performance curve paradigm with these ideas of the proximal mechanisms setting thermal limits. As we outline in the paper, this framework combines a variety of observations in reptiles and amphibians and points to exciting new directions and untested questions. For example, what is the factor that signals animals to reduce their preferred temperature in hypoxia? Is the lethal thermal limit always lower when it is determined by oxygen capacity rather than subcellular components? Does maximum aerobic capacity underlie whole-organism thermal optima? Will species that invade high-elevation habitats suffer reduced performance as oxygen availability decreases? While reptiles and amphibians provide a great diversity of ecological and ontogenetic contexts in which to test these ideas, we think they are broadly applicable to many ectothermic taxa. As Rory begins his new position as assistant professor at California State University, Fresno, and I continue my post-doc work here, we are excited to begin empirical studies that further test and develop these ideas.

We are most thankful to our families for support and patience while we spent long hours debating these ideas in the basement of Bessey Hall at Iowa State University. We are also grateful to M. Angilletta, B. Bodensteiner, and J. VandenBrooks for comments on earlier drafts of the manuscript, and for the support of A. Bronikowski, T. Schwartz, and A. Toth.

R.S.T. received support from Auburn University and California State University, Fresno. E.J.G. was supported by the U.S. National Science Foundation (IOS-1558071 to A. Bronikowski), the “Laboratoire d’Excellence (LABEX)” TULIP (ANR-10-LABX-41), and the European Union’s Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie grant agreement No 752299.

Author: Isaac Ligocki

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