Temporal niche switching and reduced nest attendance in response to heat dissipation limits in lactating common voles (Microtus arvalis)

Abstract

According to the heat dissipation limit theory, maximum metabolic turnover is limited by the capacity of the body to dissipate excess heat. Small mammals, including common voles (Microtus arvalis), face a heat dissipation limitation during lactation. Pup growth and milk production are reduced under higher ambient temperatures. Heat dissipation problems might in part be alleviated by modifying behavior, such as reducing nest attendance and being active at energetically optimal times of day. According to the circadian thermo-energetics hypothesis, animals can make use of daily ambient temperature fluctuations to alter their energetic expenditure. In this study we test whether heat challenged (housing at 30°C compared to 21°C) lactating common voles allocate their time differently among behaviors and whether their ultradian and circadian behavioral rhythmicity are altered.Behavior was scored every 13min from automated picture recordings, while general locomotor activity was measured by passive infrared detectors to assess ultradian and circadian organization. The effects of ambient temperature on the ultradian organization of behavior were assessed by determining the ultradian period length and the distribution of activity within the ultradian bout. Changes in circadian organization were assessed by the distribution of activity over the light and dark phase. As a complementary measure nest temperature recordings were used to quantify nest attendance distribution between day and night.Lactating dams at 30°C reduced the fraction of time spent on the nest while increasing the fraction of time resting without pups away from the nest. The ultradian period of locomotor activity was longer in voles housed at 30°C during pregnancy and lactation, but not after weaning when the pups were removed. No differences in the distribution of activity within the ultradian bout could be detected. The circadian organization was also modulated by ambient temperature. Lactating voles housed at 30°C became more day active and a loss of day–night differences in nest temperature suggests a shift of nest attendance towards the night.Reducing the time attending the nest can reduce the risk of hyperthermia, and may be the behavioral component resulting in lower milk production and hence reproductive output. Becoming more day active allows feeding and nursing of the pups during the rest phase to occur during the night at which lower ambient temperatures are expected in the field. In natural situations this strategy will increase heat dissipation and lactation capacity. Whether there are similar benefits associated with a longer ultradian period is currently unknown, but these are likely to result from decreased energy turnover at 30°C. In conclusion, our study shows that lactating common voles facing heat dissipation problems re-organize their behavior in a way that can maximize heat dissipation capabilities and thereby optimize lactation capacity.