Turtles on a Budget: The Cost of Temperature in a Warming World

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Thermal Environments as a Resource

One of the defining traits of the reptiles we study here at The Orianne Society is that they are ectothermic. Ectothermic animals cannot internally maintain stable body temperatures, so they must rely on their surroundings to thermoregulate. As such, features of their habitat not only provide food, protection, and nesting conditions, but also thermal opportunities. Unimpeded access to the sun offers the chance for individuals to warm up after a cold night while also providing access to UV light that aids in growth. Shady areas provide thermal refugia when individuals are at risk of overheating, though come with less-than-ideal thermal conditions for growth. Therefore, thermal environments are just another resource (Tracy & Christian, 1986) for ectothermic individuals to balance as they navigate their lives and make choices that optimize survival.

Ornate Box Turtles are characterized by the yellow, radiating stripes on their shells.

The Costs of Getting Hot

While many understand the importance of thermoregulation in reptiles for maintaining a body temperature, it is easy to overlook the energetic implications of thermoregulatory behaviors in conservation efforts. Beyond determining whether an individual is hot or cold, temperature also determines the amount of energy that individual is burning through. Organisms have limited energy to divide among basic maintenance, growth, reproduction, and other biological processes. Energy spent on one process isn’t available for another. For reptiles, higher temperatures typically result in increased energy use, meaning an individual sitting in full sun expends more baseline energy than an individual sitting in full shade. As ambient temperatures are projected to increase due to climate change, ectothermic animals may be required to devote more energy to baseline maintenance and less energy to growth or reproduction, ultimately affecting population persistence. The energetic costs of rising temperatures may become even greater in landscapes where individuals have limited access to thermal refugia, highlighting the importance of maintaining easy access to cooler conditions across the landscape. A few years ago, my interest in the energetic costs of thermoregulation was piqued and it became my master’s degree. However, my study animal was not the Spotted Turtles or Eastern Indigo Snakes of the Southeast, but rather a small species of box turtle that lives a couple hundred miles to the west.

An Ornate Box Turtle taking advantage of the shade.

Ornate Box Turtles in Illinois

I completed my master’s at the University of Illinois Urbana-Champaign studying Ornate Box Turtles. Unlike other species of box turtles that prefer forested areas, Ornate Box Turtles are a prairie species. Historically, they ranged throughout the Great Plains in open grasslands and sandhill prairies. Agricultural development has destroyed and fragmented habitat and increased the chances for road mortalities, making the Ornate Box Turtle a Threatened species in Illinois. For box turtles, declining habitat quality can also alter the range of temperatures available for thermoregulation. For my master’s, I was interested in investigating the thermal environments available to turtles, how they were thermoregulating within those confines, and the energetic costs associated with their thermoregulatory behaviors.

A prairie habitat typical of Ornate Box Turtles.

Thermoregulatory Behaviors of Ornate Box Turtles

To determine the thermal environments available to turtles, I had to create and employ the use of operative models affixed with temperature loggers. Operative models mimic the thermal qualities of an organism to approximate what temperature it would achieve if it were sitting in the same spot as the operative model. By placing operative models in various spots throughout the landscape, I could estimate the range of temperatures turtles could theoretically achieve.

Operative models used to estimate temperatures available to turtles.

To see what temperatures turtles were actually achieving, I simply affixed temperature loggers to the turtles. By comparing turtle temperatures to average operative model temperatures, I could estimate thermoregulatory effort. Turtles close to average model temperatures were likely conforming to their thermal environment, while turtles warmer or cooler than models were potentially seeking out different thermal conditions.

Ornate Box Turtle with radio transmitter and temperature logger.

I then investigated how factors such as time of day, season, weather, and location influenced thermoregulatory effort. I found that my study landscapes were thermally homogeneous, with the coolest and warmest models often within 4-8℃ of each other. I also found that Ornate Box Turtles most often achieved temperatures closest to average operative model temperatures, indicating conformity to their thermal environment (known as thermoconformity). Despite the typical pattern of thermoconformity, it was clear turtles occasionally buffered against extremes. The most evident drivers of thermoregulatory effort were time, UV irradiance, and ambient temperature. In general, as conditions became hotter, turtles sought cooler conditions relative to the operative models. Interestingly, raw temperature data indicated that turtles from at least one site showed evidence of burrowing to escape the hottest parts of the day.

Turtles start to seek cooler conditions relative to operative models towards midday, when temperatures are hottest. Temperature difference refers to the difference between average operative model temperature and turtle temperature. Positive numbers indicate turtles are warmer than models, negative numbers indicate turtles are cooler.
Turtles seek cooler conditions as UV irradiance increases.
As the average ambient temperature increases, turtles seek cooler conditions.
Temperature data for one day at one study site. The top of the gray ribbon represents the warmest operative model, the bottom represents the coolest. The line represents average model temperature. The points represent average turtle temperatures. From roughly 12:00-16:00, turtles were nearly 10℃ stably cooler than the coolest model, suggesting burrowing.

How Much Does it Cost to be a Turtle?

To estimate energy use from turtles’ field temperatures, they had to come into the lab for a quick two-week vacation. Unfortunately, turtles couldn’t take part in one of the better parts of a vacation: checking out the food scene. Digestion requires energy, and I was interested in measuring their resting metabolic rates. Resting metabolic rates reflect the baseline energy it costs to simply exist as a turtle before accounting for any other biological processes. Metabolic rates can be measured in two ways: the amount of oxygen consumed (VO2 in ml/hr) or the amount of carbon dioxide produced (VCO2 in ml/hr). My equipment was sophisticated enough to record both. Turtles were fasted for 9 days, and gas exchange was recorded at 15℃, 20℃, 25℃, and 30℃.

Turtles were placed in airtight chambers to record gas exchange and measure metabolic rates.

 I found that resting metabolic rates increased with turtle mass and temperature, consistent with well-established relationships in reptilian physiology. Knowing the degree to which temperature and mass elevated energy use, I was able to calculate baseline seasonal energy use using turtles’ field temperatures. I found that turtles use remarkably little energy to simply exist (61-147 kilocalories per season). I went one step further and applied projected ambient temperature increases under low- and high-emissions scenarios for 2050, estimating that baseline energy expenditure could increase by an average of 9.2% and 14.6%, respectively.

Turtles expend more energy as they grow in mass.
Turtles expend more energy at warmer temperatures.

Keeping Cool in a Warming World

My estimates of seasonal energy use are shockingly small but make sense for a largely sedentary species (Converse et al., 2002) that often exhibits thermoconformity. Thermoconformity may help conserve energy compared to more precise thermoregulation, which can require individuals to constantly shuttle between environments to maintain preferred temperatures. Thermoconformity may also be advantageous in the face of climate change as thermoconforming individuals are already better equipped to function within a larger range of temperatures. However, that advantage becomes moot if climate change shifts the range of temperatures landscapes have to offer toward hotter conditions and eliminates access to thermal refugia. Without access to cooler conditions, Ornate Box Turtles may be forced to spend more time inactive in burrows to conserve energy. This makes maintaining diverse thermal conditions an important consideration when managing habitat for ectothermic species. Providing food, nesting sites, and vegetation structure may not be enough if individuals cannot also access the temperatures needed for regulating energetic costs. As our climate continues to change, protecting thermal environments as a resource may become increasingly important to give species like the Ornate Box Turtle the flexibility they need to adapt.

A male Ornate Box Turtle.
A juvenile Ornate Box Turtle (a rare find).

References

Converse, S.J., Iverson, J.B., & Savidge, J.A. (2002). Activity, reproduction, and overwintering behavior of ornate box turtles (Terrapene ornata ornata) in the Nebraska sandhills. The American Midland Naturalist, 148(2), 416-422.

Tracy, R.C. & Christian, K.A. (1986). Ecological relations among space, time, and thermal niche axes. Ecology, 67(3), 609-615.

All photos by Andrea Colton.