Anole Classics: Ray Huey (1974) on the Cost of Behavioral Thermoregulation (or, What’s the Deal with Thermoconformity?)

A male Anolis cristatellus from Puerto Rico. Photo by Dave Steinberg.

It is somewhat intuitive to assume that the body temperatures of “cold-blooded” animals like anoles must closely match ambient temperatures. For example, lizards from cold climates should be active at colder body temperatures than those from warm climates, and body temperature should change throughout the day in concert with air temperature. As Martha Muñoz has discussed, Cowles and Bogert laid this expectation to rest in 1944. They demonstrated that lizards can behaviorally thermoregulate, altering the effective thermal environment that they experience to remain within a “preferred” temperature range while active.

The potential benefits of behavioral thermoregulation are pretty obvious. Seek out a little sunlight on a cold day and you can go from freezing your hemi-penes off to enjoying a fulfilling day of doing whatever a lizard might find fulfilling. So for many years after Cowles and Bogert, observing patterns consistent with behavioral thermoregulation became the expectation.

However, pesky examples of lizards apparently not thermoregulating kept cropping up, including data collected on Cuban and Puerto Rican anoles by Rudolfo Ruibal and Stanley Rand. This lead folks to wonder: If thermoregulation is so beneficial, why doesn’t everyone do it? What’s the deal with thermoconformity?

Ray Huey provided a potential answer to this question in 1974. Building on ideas put forth by Rudolfo Ruibal, Michael Soulé, and Sam McGinnis, Ray posited that along with benefits, behavioral thermoregulation must also incur costs. For example, shuttling between shade and sun has an energetic cost, and the movement required may increase your chances of being picked off by a predator. Within this conceptual framework, whether or not you behaviorally thermoregulate should depend on whether or not the benefit outweighs the cost.

Ray tested this hypothesis by studying two different populations of the Puerto Rican Anolis cristatellus, a common trunk-ground species. One population lived in a relatively open park, and the other in a more shaded forest. Ray measured three things: 1) lizard body temperatures 2) air temperatures where the lizards perched, and 3) the distance to the nearest basking site if a lizard was in the shade. This last measurement was meant to serve as a correlate of the energetic cost of behaviorally thermoregulating in each habitat.

Percentage of lizards basking in the open park versus the more shaded forest from Huey 1974.

Ray found that the lizards in the shaded forest were thermoconformers, with body temperatures closely matching air temperatures. In contrast, the lizards in the open park were thermoregulating: their body temperatures were warmer than air temperature for much of the day. Importantly, Ray found that lizards in the shaded forest would have to travel relatively large distances to find sunlight (about 8 meters on average) and most would have to move to a different tree to do so. The lizards in the open park had short transit distances to sunlight (about 1 meter on average) and very few would have to move to a new tree. Thus, thermoconformity and thermoregulation occurred in different populations of the same species and correlated with the apparent cost of thermoregulation. The cost/benefit theory of behavioral thermoregulation has been a cornerstone of thermal biology ever since, with important implications for ecology, evolutionary biology, and conservation. But that is a story for another post.

Incidentally, Ray remembers the moment he had the idea that costs might be important. In his own words: “I was sitting on the top of a chair in the basement of the Bio Labs, staring at anole data, and wondering what was going on – with a Stones album playing in the background.  The rhythm was hypnotic, and then the idea that one needed to consider costs, not just benefits, came like a flash.  I don’t think I ever acknowledged Mick & Keith, but certainly should have.”

If there is a moral to this story, it is obviously this: listen to the Rolling Stones and you will greatly increase your chances of developing transformative ideas in your field. You might call it “The Principle of Sympathy for the Devil”.

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Alex Gunderson

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