A Changing Climate – The Birth of Biophysical Ecology and Modern Reptile Thermobiology

Anolis armouri basking on a rock.

Our era of human-mediated climate change has brought startling new realities that we must face – ocean acidification, desertification, and receding ice caps, among others. For those of us who study lizards, one message is pervasive and clear – many species are being pushed to their thermal limit, and it is likely that many lizards, especially those that prefer cooler temperatures, won’t be able to take the heat. But, how do we know this? One of the main methods used to determine how reptiles will respond to climate change is to compare their preferred temperature (i.e., where lizards would like to keep their body temperature, given the option) to a random sampling of the thermal environment.

From a lizard’s eye view, though, the thermal environment is more complex than just air temperature. Lizards have volume, shape, and color, all of which affect their core temperature. Essentially, the operative temperature (Te) describes a lizard’s thermal environment as the sum total of many different interactions, such as radiation and convection, among others. Because it describes how temperature is shaped by everything except behavior and physiology, the operative temperature essentially describes how a perfect thermoconformer instantaneously perceives the environment. As such, it has been used as the null hypothesis for behavioral thermoregulation – if we can describe the thermal environment by recording Te, then we can use field-measured body temperature to determine the degree to which animals are thermoregulating. Here on the Anole Annals I’ve considered how devices have evolved to capture the operative temperature. The earliest prototype was a water-filled beer can, and we now have copper models painted to match the organism’s reflectance and HOBO devices.

Copper models of Anolis cybotes in the making.

But just where did these devices come from? I’ve been in Terre Haute, Indiana working with Dr. George Bakken at Indiana State University for the past two weeks making copper models of Anolis cybotes for my field research in the Dominican Republic. Dr. Bakken, along with Dr. David Gates, operationalized the term “operative temperature” for the ecological community in a seminal 1975 paper. I sat down with Dr. Bakken for an interview to learn how the intellectual climate promoted this and other important foundational works for biophysical ecology and reptilian thermobiology.

The field of modern biophysical ecology sprung from a movement in the late 1960s and early 1970s led by David Gates, now a Professor Emeritus at the University of Michigan. Although he was a physicist by trade, Dr. Gates’ father was a plant ecologist, and so he kept up with the biological literature. He noticed that many studies in plant transpiration were getting uninterpretable results. Because of his background in physics he knew that this was likely due to the single-factor experiments that were being conducted, wherein transpiration was measured in response to change in a single variable, such as air temperature. To Gates this came as no surprise, as he knew the energy budget of plants involved multiple components, including radiation, convection, and transpiration.

It was clear that incorporating some physical modeling into ecology and physiology would prove useful and beneficial. To this end, Gates secured a five-year Ford Foundation grant aimed at unifying physical concepts in biological systems, with special emphasis on transport physics, heat, energetics, and microclimate in plants and animals. Gates, then Director of the Missouri Botanical Garden, assembled a diverse group of scientists to engage in this project. Among the biologists were some familiar names in reptile ecology, such as Jim Spotila, who has since founded the Leatherback Trust, Warren Porter, and Dick Tracy. Bakken was one of the lead physicists in the group, along with David Gates and Paul Lommen.

“The goal was to get a group of biologists and physicists and lock them in an office trailer behind the herbarium, and see if we could get some physics into biology,” Bakken says. Their approach to ecology was to use the principles of chemistry, physics, and mathematics to mechanistically understand how organisms interact with their environment.

Perspectives of Biophysical Ecology (1975) was a text of the symposium proceedings summarizing the major findings of the consortium.

The project was very successful, and the papers and book that resulted from this symposium laid the foundation for modern biophysical ecology. However, the goals of the symposium were not just to jump start the field of biophysical ecology, but hopefully to help it grow. The idea was to encourage new scientists to integrate physics and biology to address big questions in ecology. “Just (the physicists and biologists) talking to each other doesn’t quite do it. We need people who can do both. At first I tried to go for physics-level precision, but it was impossible in the field,” Bakken explains. Yes, many of us who study anoles in nature know exactly how messy field ecology can be. In fact, we have a term for it – the principle of unsympathetic magic – coined by anolologist Ernest E. Williams. “My goal was to simplify it to make it practical for the biologist,” he says.

A goal of this symposium was to generate mathematical models that could be used to understand how organisms interact with their environment. Among the seminal studies that emerged from this consortium were models for predicting the body temperatures and thermal ecology of large dinsosaurs, heat-energy budgets in alligators, a definitive treatise on thermal equilibria by Porter and Gates, and a re-assessment of Newton’s law of cooling, where it was shown that heat transfer between the organism and its environment is not linear, which had until then been the prevailing wisdom in physiological ecology.

The symposium helped expand this text, Biophysical Ecology, by David Gates (1980). An earlier version is "Energy Exchanges in the Biosphere" by Gates (1965).

One of the most relevant papers to those of us who study thermal ecology in anoles is Bakken and Gates (1975). This paper proposes a theoretical model of heat transfer between an organism and its environment that simultaneously combines multiple parameters to derive the steady-state temperature (Te). The authors operationalize Te for field biologists by describing methods of measurement and, most importantly, provide a detailed appendix on how to make copper animal casts for Te thermometers. Until then instruments used to measure micrometeorological parameters could not get to the spatial scale animals experienced. Moreover, they were expensive and so only a point or two could be measured. The purpose of the models was to obtain a parameter at the appropriate scale, measure multiple points, minimize excessive calculations, and reduce instrument costs. Finally, Bakken and Gates describe Te as a dynamic interplay between the organism and its environment, wherein the temperature of one is dependent on the other. “Thus we have the interesting situation in which the supposed property of the animal is determined in part by the environment… and the temperature of the environment is determined by the properties of the animal.”

This paper provided the theoretical background and methodological logistics for modern thermal ecology. Research using copper lizard models has proven quite fruitful in anoles. Paul Hertz and Ray Huey have been using copper models to map the thermal environment for anoles in Puerto Rico for several decades. Hertz (1992) examined thermal niche partitioning in sympatric populations of the trunk-ground anoles, A. cristatellus and A. cooki. He found that mean A. cristatellus body temperatures were a few degrees below mean Te, while those of A. cooki were a few degrees above it, showing that these two species, though sympatric, exploit the microclimate in different ways. In a long-term study of A. gundlachi, a forest dwelling trunk-ground, and A. cristatellus, a species found in open habitat, Huey, Hertz and others have found that a slightly warmer environment will push A. gundlachi beyond its preferred temperature range and that this species may be experiencing thermal stress.

Several important concepts emerged from the Biophysical Ecology consortium. Organisms interact with the environment in complex ways. Measuring the operative temperature, presumably with an appropriate model, can provide insight into how organisms perceive the environment in the absence of behavior and physiology. These data can allow us to create testable hypotheses about ecological interactions, behavioral thermoregulation, and responses to global climate change, among many others. For these reasons, and many more, the Biophysical Ecology consortium helped advance Anolis biology. Stay tuned for pictures and descriptions of how to build copper Anolis models.

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Martha Muñoz

Martha is a postdoctoral researcher in Sheila Patek's laboratory at Duke University. She received her Ph.D. at Harvard University, where she studyied the evolutionary ecology and thermal physiology of anoles, focusing on the cybotoid anoles from the Dominican Republic. Martha serves as Conference Editor for the Anole Annals.
Website: www.marthamunoz.weebly.com

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