Seasonal variation of behavioural thermoregulation in a fossorial salamander (Ambystoma maculatum)

Abstract

Temperature seasonality plays a pivotal role in shaping the thermal biology of ectotherms. However, we still have a limited understanding of how ectotherms maintain thermal balance in the face of varying temperatures, especially in fossorial species. Due to thermal buffering underground, thermal ecology theory predicts relaxed selection pressure over thermoregulation in fossorial ectotherms. As a result, fossorial ectotherms typically show low thermoregulatory precision and low evidence of thermotactic behaviours in laboratory thermal gradients. Here, we evaluated how temperature selection (T _sel) and associated behaviours differed between seasons in a fossorial amphibian, the spotted salamander (Ambystoma maculatum). By comparing thermoregulatory parameters between the active and overwintering seasons, we show that A. maculatum engages in active behavioural thermoregulation despite being fossorial. In both seasons, T _sel was consistently offset higher than acclimatization temperatures. Thermoregulation differed between seasons, with salamanders having higher T _sel and showing greater evidence of thermophilic behaviours in the active compared with the overwintering season. Additionally, our work lends support to experimental assumptions commonly made but seldom tested in thermal biology studies. Ultimately, our study demonstrates that the combination of careful behavioural and thermal biology measurements is a necessary step to better understand the mechanisms that underlie body temperature control in amphibians.

Keywords: amphibian; body temperature; ectotherm; fossorial; seasonality; thermal biology.

Figure 1.

(a) Thermal image of the annular thermal gradient used in this study depicting the temperature range used in the overwintering season. The oval shapes denote two individuals of Ambystoma maculatum. The one on the lower left has a surface body temperature slightly higher than that of the floor of the thermal gradient. By contrast, the one on the lower right has a surface body temperature in equilibrium with that of the thermal gradient floor. (b) Thermal image of a female A. maculatum in the annular thermal gradient. Note the different temperature (°C) range bars between panels (a) and (b). In both panels, darker colours indicate lower temperatures and lighter colours indicate higher temperatures.

Figure 2.

Temporal variation in the selected body temperature (T_sel) of Ambystoma maculatum throughout 8 h during the active and overwintering seasons. In both panels, the grey dashed lines represent the acclimatization temperatures in the active (14°C) and overwintering (2°C) seasons. Boxes denote the among-individual 25th and 75th bounds of T_sel at a given hour. The horizonal line in each box indicates the median T_sel, and the black line connecting each median T_sel showcases the hourly change in this parameter. Temperatures selected by each individual salamander are shown as semi-transparent dots. The violin plots show the kernel density probability of T_sel data at different hours of experimentation.

Figure 3.

Kernel density estimations of median selected temperature (T_sel) highlighting the negatively skewed and platykurtic nature of T_sel in Ambystoma maculatum. In both panels, the grey lines depict the T_sel distribution of each individual, whereas the colour-coded lines show the mean T_sel distribution considering all individuals tested within a season (N = 50 each season). Values above 0.5 on the y-axis pertain to salamanders that remained mostly stationary during the experiments.

Figure 4.

Relationship between skewness and median selected temperatures (T_sel) for Ambystoma maculatum. The solid black lines and coloured fills indicate the line of best fit and the corresponding 95% confidence interval, respectively. The grey dashed line indicates the zero. Dots represent individual A. maculatum (N = 50 per season). The inset shows a female A. maculatum.