Continuous growth through winter correlates with increased resting metabolic rate but does not affect daily energy budgets due to torpor use

Abstract

Small mammals that are specialists in homeothermic thermoregulation reduce their self-maintenance costs of normothermy to survive the winter. By contrast, heterothermic ones that are considered generalists in thermoregulation can lower energy expenditure by entering torpor. It is well known that different species vary the use of their strategies to cope with harsh winters in temperate zones; however, little is still known about the intraspecific variation within populations and the associated external and internal factors. We hypothesized that yellow-necked mice Apodemus flavicollis decrease their resting metabolic rate (RMR) from autumn to winter, and then increase it during spring. However, since the alternative for seasonal reduction of RMR could be the development of heterothermy, we also considered the use of this strategy. We measured body mass (m _b), RMR, and body temperature (T _b) of mice during 2 consecutive years. In the 1st year, mice decreased whole animal RMR in winter, but did not do so in the 2nd year. All mice entered torpor during the 2nd winter, whereas only a few did so during the first one. Mice showed a continuous increase of m _b, which was steepest during the 2nd year. The relationship between RMR and m _b varied among seasons and years most likely due to different mouse development stages. The m _b gain at the individual level was correlated positively with RMR and heterothermy. This indicates that high metabolism in winter supports the growth of smaller animals, which use torpor as a compensatory mechanism. Isotope composition of mice hair suggests that in the 1st year they fed mainly on seeds, while in the 2nd, they likely consumed significant amounts of less digestible herbs. The study suggests that the use of specialist or generalist thermoregulatory strategies can differ with environmental variation and associated differences in developmental processes.

Keywords: growth rate; heterothermy; phenotypic flexibility; resting metabolic rate; torpor.

Figure 1.

Time course of body temperature (T_b) readings in two representative yellow-necked mice during 10 consecutive days of measurements (plots on left). Nine subsequent days of measurements were conducted at home cages during winter 2017 (upper plots) and 2018 (lower plots). Gray shading indicates 23.5 h period when mice were measured in respirometry chambers without access to food. In addition (plots on right), time course of T_b and metabolic rate (MR) readings (in red) of two mice during daily measurements in respirometry chambers in winter 2017 and 2018. Black-and-white boxes refer to the dark–light cycle.

Figure 2.

Changes of body mass in yellow-necked mice during 2 study years (dark gray: 2016/2017, light gray: 2017/2018). Consecutive measurements of the same individuals (dots) are connected with lines. Each boxplot shows the median (line inside), 25–75 percentile ranges (box edges), and non-outlier ranges (whiskers).

Figure 3.

Relationship between resting metabolic rate and body mass in yellow-necked mice during 2 years (dark gray: 2016/2017, light gray: 2017/2018) in 3 experimental sessions.

Figure 4.

Heterothermy indices in yellow-necked mice during 2 years (dark gray: 2016/2017, light gray: 2017/2018) in 2 experimental sessions. Consecutive measurements of the same individuals (dots) are connected with lines. Each boxplot shows the median (line inside), 25–75 percentile ranges (box edges), and non-outlier ranges (whiskers).

Figure 5.

Relationship between torpor occurrence when yellow-necked mice were kept in home cages with access to food ad libilitum and heteothermy indices when they were fasted daily at respirometry chambers in winter 2017 (dark gray) and 2018 (light gray). Torpor occurrence was defined as episodes when body temperature decreased below 32°C. Logistic regression curve indicates that HI in fasted mice was a significant predictor for torpor occurrence when mice were kept in home cages with non-limited access to food (z = 2.53, P = 0.011). Shaded area refers to 95% CIs.

Figure 6.

Stable carbon (δ¹³C) and nitrogen ((δ¹⁵N)) isotope values of the rodent hair (circles) collected at the study site during autumn of 2016 (dark gray) and 2017 (light gray), with 100 ellipses (lines) sampled based on posterior distributions of data from both years.

Figure 7.

Relationship between residual resting metabolic rate (RMR) and residual growth rate in yellow-necked mice during 2 years (dark gray: 2016/2017, light gray: 2017/2018). RMR was obtained from linear relationship: RMRmb, residual growth rate was obtained from mixed effects model adjusted for variation related to sex and heterothermy use (see “Material and Methods” section for details).

Figure 8.

Relationship between heterothermy and residual growth rate in yellow-necked mice during 2 years (dark gray: 2016/2017, light gray: 2017/2018). Residual growth rate was obtained from mixed effects model adjusted for variation related to sex and residual resting metabolic rate (see “Material and Methods” section for details).