Flexible energy-saving strategies in female temperate-zone bats

Abstract

Torpor is characterized by an extreme reduction in metabolism and a common energy-saving strategy of heterothermic animals. Torpor is often associated with cold temperatures, but in the last decades, more diverse and flexible forms of torpor have been described. For example, tropical bat species maintain a low metabolism and heart rate at high ambient and body temperatures. We investigated whether bats (Nyctalus noctula) from the cooler temperate European regions also show this form of torpor with metabolic inhibition at high body temperatures, and whether this would be as pronounced in reproductive as in non-reproductive bats. We simultaneously measured metabolic rate, heart rate, and skin temperature in non-reproductive and pregnant females at a range of ambient temperatures. We found that they can decouple metabolic rate and heart rate from body temperature: they maintained an extremely low metabolism and heart rate when exposed to ambient temperatures changing from 0 to 32.5 °C, irrespective of reproductive status. When we simulated natural temperature conditions, all non-reproductive bats used torpor throughout the experiment. Pregnant bats used variable strategies from torpor, to maintaining normothermy, or a combination of both. Even a short torpor bout during the day saved up to 33% of the bats' total energy expenditure. Especially at higher temperatures, heart rate was a much better predictor of metabolic rate than skin temperature. We suggest that the capability to flexibly save energy across a range of ambient temperatures within and between reproductive states may be an important ability of these bats and possibly other temperate-zone heterotherms.

Keywords: Heart rate; Metabolism; Nyctalus noctula; Reproduction; Thermoregulation; Torpor.

Fig. 1

Irrespective of reproductive status (green = non-reproductive, yellow = reproductive), N. noctula remained torpid when exposed to rising T_a. a $\dot{V}{\text{O}}_2$ increased slightly but remained low across all T_a (non-reproductive: n = 19, n_Observations = 491; reproductive: n = 9, n_Observations = 193). Grey dashed line indicates the BMR of N. noctula = 1.47 mL O₂ g⁻¹ h⁻¹ (reported in Geiser 2004). b f_H increased slightly but remained low across a wide range of T_a (non-reproductive: n = 19, n_Observations = 484; reproductive: n = 9, n_Observations = 164). c T_skin increased with rising T_a when torpid bats thermoconformed (non-reproductive: n = 12, n_Observations = 256; reproductive: n = 9, n_Observations = 182). Shaded green and yellow areas indicate the 95% CI

Fig. 2

Different torpor use strategies in non-reproductive and reproductive female N. noctula in the 12-h experiment. a Representative figure of a non-reproductive bat using the “only torpid” strategy. Upper panel: $\dot{V}{\text{O}}_2$ (black dashed line) and f_H (pink solid line) were lowered after a short arousal at the beginning of the experiment. Lower panel: the bat thermoconformed T_skin (light-blue solid line) to T_a (dark-blue dashed line). b Representative figure of a reproductive bat using the “only resting” strategy. Upper panel: $\dot{V}{\text{O}}_2$ (black dashed line) and f_H (pink solid line) were very variable. Lower panel: the bat thermoregulated and T_skin (light-blue solid line) was constantly higher than T_a (dark-blue dashed line)

Fig. 3

Predictions for $\dot{V}{\text{O}}_2$ from the T_skin model and the f_H model and the measured $\dot{V}{\text{O}}_2$ for one representative bat in the 6-h experiment with rising T_a. a Predictions for $\dot{V}{\text{O}}_2$ from the f_H model (pink dashed line) were similar to the measured $\dot{V}{\text{O}}_2$ (black solid line). Predictions for $\dot{V}{\text{O}}_2$ from the T_skin model (light-blue dotted line) overpredicted $\dot{V}{\text{O}}_2$ when T_a was raised above 20 °C. b T_a (dark-blue solid line) was raised every hour and was > 20 °C after 09:00