One of the most universal threats to biodiversity is the global alteration of environmental thermal regimes (Mooney et al. 2009; Traill et al. 2010). Predictive models are often used to assess the degree to which alterations in environmental temperatures will impact different groups and such models are often constructed from taxon-specific biophysical and physiological parameters (Kearney and Porter 2004, 2009; Kearney et al. 2008; Gunderson and Leal 2012). Inherent in these models are estimates of the thermal sensitivity of critical physiological processes that determine the performance of individuals and ultimately their fitness (Huey and Berrigan 2001; Angilletta 2009). Among the most relevant physiological processes that can influence the performance of ectotherms is the thermal sensitivity of metabolism, or the rate at which energy flows through an organism at different body temperatures (Huey and Stevenson 1979).

Although the majority of variation in standard metabolism of ectotherms can be accounted for by environmental temperature, individual effects such as body size, sex, and reproductive status may also exert strong influences (Bennett and Dawson 1976; Andrews and Pough 1985). We aimed to test the hypothesis that both environmental and individual factors can explain observed variation in metabolism in a terrestrial emydid, the Eastern Box Turtle (Terrapene carolina). Specifically, we tested the predictions that box turtle metabolism is influenced by differences in temperature, body mass, and sex.

Box turtles are a good group to address these predictions as they vary a great deal in body temperature when active in the field (do Amaral et al. 2002; Penick et al. 2002; Currylow et al. 2012), and can vary in body mass from ∼ 10 to > 500 g over a lifetime (Dodd 2001). Additionally, T. carolina is geographically widespread throughout much of the eastern United States in a range of habitat types with seasonally variable climates and thermal regimes. Yet surprising little is known about energy use in box turtles or the relative importance of thermal and individual influences on whole-animal metabolism. Previous studies of Terrapene metabolism are somewhat limited in their ability to make predictions about patterns of energy use because they are either restricted to a single test temperature, use a narrow range of body sizes, or report data in a format (such as mass-specific units) that cannot be used to model the allometric effects of body size on metabolism (Ultsch 2013).

MATERIALS AND METHODS

RESULTS

We measured metabolism in 59 box turtles, including 23 adult males, 31 adult females, and 5 juveniles (not able to be sexed). Mass ranged from 106 to 510 g (323.6 ± 12.08 g SE). In the full GLM, which included the effects of sex, body mass, and temperature, there was no significant difference between sexes in SMR (F_1,51 = 3.19, p  = 0.08; juveniles not included in analysis of sex). However, there were significant effects of both body mass (F_1,57 = 16.46, p = 0.0002) and temperature (F_1,57 = 360.52, p < 0.0001) on SMR (all turtles included; Fig. 1). The interaction between body mass and temperature was also significant (F_1,57 = 14.13, p < 0.0004), even though regression lines for these groups crossed well below the range of body masses considered here. Together, body mass, temperature, and their interaction accounted for 88% of the measured variation in box turtle SMR. The linear predictive equation for SMR (ml · O₂ · hr⁻¹) when considering both body mass and body temperature was −16.360 + 0.015 × mass + 0.761 × temperature + (temperature − 25) × [(mass − 323.559) × 0.0016].

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Because the significant interaction between body mass and body temperature (Fig. 1) potentially obfuscates the statistical interpretation of the linear model (and the covariate; Vanderburgh et al. 1998; Engqvist 2005), we log transformed the data and present allometric equations as a power function of the form SMR = aM^b, where a is the scaling coefficient (intercept), M is body mass, and b is an exponent (slope of the regression line). Transformed to standard allometric equations, SMR was 0.202M^0.49 at 20°C and 0.311M^0.61 at 30°C and there was a significant effect of both body mass (F_1,57 = 15.15, p = 0.0002) and temperature (F_1,57 = 616.90, p < 0.0001) on SMR (Fig. 1).

There was significant among-individual variation in SMR and a positive relationship between residual SMR at 20°C and residual SMR at 30°C (r = 0.59, F_1,57 = 30.59, p < 0.001; Fig. 2). The Q₁₀ of SMR between 20°C and 30°C was 3.04.

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DISCUSSION

As expected, body temperature and body mass were both significant predictors of SMR in Eastern Box Turtles. The predictive equation presented in our study considers both body mass and body temperature, but differs somewhat from recent reviews summarizing interspecific expectations for turtle energy use (Ultsch 2013). At the mean body mass observed in our study (323.6 g), Eastern Box Turtles are expected to have an SMR of 3.72 and 11.34 ml · O₂ · hr⁻¹ at 20°C and 30°C, respectively. The interspecific allometric equations of Ultsch (2013, fig. 1) would predict box turtles to have SMRs of 8.41 and 14.13 ml · O₂ · hr⁻¹ at 20°C and 30°C, respectively, which are 126% and 25% higher estimates than expected from our intraspecific equation. These differences highlight the need to apply species-specific empirical data when modeling expected rates of energy use.

Turtles used in this study varied in body mass by nearly a factor of 5 (106–510 g), but our metabolic measurements were limited to large juveniles and adults. Including or excluding neonates and juveniles from allometric analyses can alter the predicted rates of metabolism for an ontogenetic series of individuals, sometimes substantially (Nagy 2000). Juveniles tend to have higher rates of metabolism than expectations from the mass scaling of older animals (Beaupre and Zaidan 2001; Gienger et al. 2012), which may be partially explained by the energy demands accompanying rapid growth and tissue synthesis (Thompson and Withers 1998).

There was significant individual variation in SMR of box turtles, and individuals with high residual SMR at one temperature tended to have high residual SMR at the other (Fig. 2). Among-individual variation in phenotype provides the raw material for natural selection to act (Endler 1986) and because relative SMR was individually conserved across temperatures, SMR in box turtles should be subject to selection as well (Marais and Chown 2003; Nespolo et al. 2003).

The calculated Q₁₀ of SMR (3.04) for Eastern Box Turtles falls within the range of Q₁₀s reported for other chelonians tested at both 20°C and 30°C (summarized by Litzgus and Hopkins 2003). Reported mean Q₁₀ values for other turtles include 1.60 for the closely related Terrapene ornata (Gatten 1974), 2.87 for Trachemys scripta (Gatten 1974), and 5.10 for the highly aquatic Kinosternon subrubrum (Litzgus and Hopkins 2003). The variability in the thermal sensitivity of metabolism (as indexed by Q₁₀) seems to be high among chelonians and could be one factor that will, in part, determine species' vulnerability to future climate change (Stillman 2003; Somero 2010).

If the predictions of current climate models are correct, then many ectotherms will likely become increasingly vulnerable to extinction as a result of global climate change. Increased habitat temperatures may lead to alterations in individual foraging opportunities, energy budgets, and ultimately growth (Deutsch et al. 2008; Sinervo et al. 2010). Recent articles suggest that these changes may be already occurring (Caruso et al. 2014; Ohlberger 2013). Therefore, data describing the individual influences and thermal sensitivity of metabolism, such as those presented here for box turtles, will be essential to predicting species-specific responses.

An important factor not considered herein is the capacity for box turtles to acclimate metabolically to gradual changes in temperature. Slow changes in environmental thermal regimes, such as those that are experienced across seasons, or changes occurring over time with climate change, may also influence patterns of metabolism. In other studies that have aimed to specifically address thermal acclimation effects, it is clear that turtles have the capacity to compensate physiologically for changing environmental temperatures (Gatten 1978; Wood et al. 1978; Hochscheid et al. 2004). The data presented here (measured under acute temperature change) should provide a starting point for other investigations aimed at determining how box turtles might acclimate to changing thermal landscapes.