Many organisms have adapted successfully to long-term temperature fluctuations, but when temperatures shift quickly, these same organisms often rely instead on behavioral responses as a means of acclimation. For aquatic ectotherms, conduction and convection with the surrounding water are the primary means by which they manipulate their body temperature (Reynolds and Casterlin, 1979). They are capable of moving through their environment to select areas in the water with the most optimal temperature (Hutchison and Dupré, 1992). However, temperature fluctuations tend to be rather minimal in aquatic environments because of water's high specific heat, thereby limiting the range of temperatures these organisms can realistically access (Hillman et al., 2009). This limitation in aquatic thermal range is important given that body temperatures for aquatic ectotherms rarely differ from the surrounding water by more than 2°C (Spotila et al., 1992). Understanding the temperatures that individuals select at different times in life can help illuminate their thermal needs at a particular age or developmental stage as well as how those needs may be impacted by rapidly shifting global temperatures. Improved knowledge of temperature selection shifts throughout ontogeny can also increase the accuracy and utility of species distribution models, as survivability can vary with body size (Riddell et al., 2018; Gouveia et al., 2019).

Temperature preference is of particular interest to species with complex life histories, such as amphibians and aquatic insects. Temperature preference for some anuran species can shift as tadpoles progress through development, with individuals in later developmental stages showing preference for warmer temperatures than those at earlier stages (Floyd, 1984; Dupré and Petranka, 1985). For example, both Rana (Lithobates) catesbeiana and Rhinella marina tadpoles exhibit a preference for higher temperatures at later developmental stages (Hutchison and Hill, 1978; Floyd, 1984; Dupré et al., 1986). Pseudacris triseriata tadpoles do not show distinct temperature preferences earlier in development, but from stage 36 onward, they show a preference for warmer temperatures (Dupré and Petranka, 1985). However, there are some species of anurans—for example, Rana boylii—that exhibit no difference in temperature selection at the various life-history stages (Catenazzi and Kupferberg, 2013).

Larval amphibians, in general, balance growth and metamorphosis, depending on a variety of environmental conditions, by using the release of particular hormones to stimulate and inhibit responses (Wilbur and Collins, 1973; Werner, 1986; Hillman et al., 2009). In addition, Rana arvalis tadpoles exposed to increased temperatures demonstrated shorter larval periods and larger masses at metamorphosis (Richter-Boix et al., 2015), providing evidence that temperature can interact with other drivers, such as hormones, to alter the rate of growth, metamorphosis, or both. In tadpoles, selection of lower temperatures typically leads to a slower rate of development (Smith-Gill and Berven, 1979), likely the result of decreased metabolism, whereas selection of higher temperatures has been shown to increase growth and developmental rate (Hutchison and Hill, 1978; Wu et al., 2007). The ability for tadpoles to influence their developmental rate is critical for survival, especially to escape stressors, such as predation and pond drying (Wilbur, 1997). In addition, swimming performance increases with temperature in Limnodynastes peronii tadpoles (Niehaus et al., 2011), so the selection for higher temperatures could also maximize the ability of tadpoles to escape predation with improved locomotor performance.

Here, we address the temperature preference of tadpoles of a broadly distributed anuran species, Hyla chrysoscelis (Cope, 1880) (Cope's Gray Treefrog). We hypothesized that temperature preference would increase for H. chrysoscelis tadpoles at larger body sizes to maximize the rate of metamorphosis and emergence as metamorphs, a trend similar to that seen in other North American anurans (Hutchison and Hill, 1978; Floyd, 1984; Dupré and Petranka, 1985; Dupré et al., 1986).

Materials and Methods

Results

The body length of tadpoles was 12.2 ± 2.1 mm (range, 7–15 mm). Tadpoles had average temperature selections ranging from 12.9 to 30.0°C. Our model explained 13.05% of the variance, and we found a significant, positive relationship (F_1,62= 9.454, P = 0.0031, β = 1.0606 ± 0.3449 [mean ± SE]) between body length and mean temperature preference (Fig. 1).

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Discussion

Temperature plays an integral role in anuran life cycles, wherein it can influence both metabolic (Wu et al., 2007) and developmental (Smith-Gill and Berven, 1979; Goldstein et al., 2017) rates, which contribute to the maturation of tadpoles into adults. Our study demonstrates that preferred temperature increases as body size increases in H. chrysoscelis tadpoles. This pattern is similar to that found in several other anuran tadpoles (Hutchison and Hill, 1978; Floyd, 1984; Dupré and Petranka, 1985; Dupré et al., 1986).

There are two main hypotheses to explain the positive relationship between tadpole body size and temperature preference: (1) escape from environmental pressures and (2) escape from ecological pressures. Seeking out warmer temperatures later in development could be an attempt to increase the rate of development, as tadpoles at later stages of development are in a more vulnerable state (Dupré and Petranka, 1985). From an environmental perspective, this vulnerability is often the result of environmental factors, such as pond drying (Wellborn et al., 1996; Wilbur, 1997), that will lead to mortality if tadpoles cannot escape the deteriorating environment in time. Selecting warmer temperatures generally increases the rate at which development proceeds, thus enabling tadpoles to emerge from their aquatic habitats to avoid desiccation (Newman, 1992).

In an ecological sense, increased temperatures can also enable tadpoles to escape ecological pressures, such as predation and competition. Selection of warmer temperatures may decrease the threat of predation by either increasing locomotion of the tadpoles (Niehaus et al., 2011) or by enabling them to metamorphose and leave the pond sooner (Wilbur, 1997). Dupré and Petranka (1985) discuss that the correlation between thermal preference and body size of tadpoles might also spatially segregate size classes and minimize competition and cannibalism in aquatic habitats, although cannibalism is not known in H. chrysoscelis. Differences in thermal preference may even contribute to interspecific niche partitioning, allowing multiple species to coexist in a given habitat by exploiting different temperature regimes.

Although our study demonstrates a relationship between preferred temperature and body size in H. chrysoscelis tadpoles, it is narrow in scale as it focuses on a single population in the southern third of its North American range. The tadpoles used in our study were from an artificial wetland and retention pond, which might not mimic a natural thermal regime. Temperature preferences may vary among anuran populations due to local thermal adaptations (Drakulić et al., 2017). Therefore, our results might represent a local thermal adaptation to artificial habitats that might differ if compared with thermal preferences of tadpoles from natural habitats. Because of its cosmopolitan distribution in North America, temperature preference of H. chrysoscelis could vary considerably among populations depending on local climates, and future studies should investigate temperature preference of H. chrysoscelis at a larger scale.