Metabolic rate in common shrews is unaffected by temperature, leading to lower energetic costs through seasonal size reduction

Abstract

Small endothermic mammals have high metabolisms, particularly at cold temperatures. In the light of this, some species have evolved a seemingly illogical strategy: they reduce the size of the brain and several organs to become even smaller in winter. To test how this morphological strategy affects energy consumption across seasonally shifting ambient temperatures, we measured oxygen consumption and behaviour in the three seasonal phenotypes of the common shrew ( Sorex araneus ), which differ in size by about 20%. Body mass was the main driver of oxygen consumption, not the reduction of metabolically expensive brain mass. Against our expectations, we found no change in relative oxygen consumption with low ambient temperature. Thus, smaller body size in winter resulted in significant absolute energy savings. This finding could only partly be explained by an increase of lower cost behaviours in the activity budgets. Our findings highlight that these shrews manage to avoid one of the most fundamental and intuitive rules of ecology, allowing them to subsist with lower resource availability and successfully survive the harsh conditions of winter.

Geographic patterns in seasonal changes of body mass, skull, and brain size of common shrews

“…It is striking that while the size of the brain and skull were largest in juveniles and only partially regrew after the winter decrease (Pucek, 1965) TA B L E 1 Results from linear models to test correlation between intensity of Dehnel's Phenomenon and geographic variables ambient temperatures, is by far the highest in the heavy adults and thus probably driven by mass (Schaeffer et al, 2020). Reproduction is the most important investment adult shrews face.…”

“…The decrease in mass from summer to winter then leads to large absolute energy savings, which are not yet physiologically understood but may at least partly be due to the reduction in size of energetically expensive organs. Thus, food requirements of the size-decreased subadult winter shrews are also lower than in the juvenile summer animals and especially in the adult individuals, whose mass doubles in the spring (Gębczyński, 1965;Schaeffer et al, 2020;Taylor et al, 2013). This would then compensate for the disadvantages of being small, such as an increasingly unfavorable volume to surface area ratio in winter (Bergmann, 1848;Yom-Tov & Yom-Tov, 2005).…”

“…The reversible changes of body and brain were hypothesized to be a winter adaptation to save energy and reduce resource requirement during harsh conditions (Mezhzherin, 1964; Pucek, 1970; Yaskin, 2011). While direct evidence of a link between the changes in overall size or specific organs, such as the brain and individual survival is still lacking, reducing metabolically expensive organs, including the brain during winter, is thought to decrease overall energetic needs and thus food intake (Churchfield, 1982; Schaeffer et al., 2020). Shrews use additional strategies to save energy in winter; important, for example, is increased insulation by 19% through winter fur (Taylor et al., 2013).…”

“…However, this is not the complete story, as there is no seasonal overall difference in relative oxygen consumption. Winter shrews use the same amount of energy per unit of mass as summer shrews, under constant (Taylor et al., 2013) and even at ambient temperatures that differ by as much as 30°C (Schaeffer et al., 2020). The decrease in mass from summer to winter then leads to large absolute energy savings, which are not yet physiologically understood but may at least partly be due to the reduction in size of energetically expensive organs.…”

Production efficiency differences between poikilotherms and homeotherms have little to do with metabolic rate

“…Apparently, the high volume‐related maintenance costs, which include activity, etc., substitute for all thermoregulation costs (Humphries and Careau, 2011). The underlying idea that animals spend most of their time in their thermoneutral zone (with respect to the field metabolic rate) is also confirmed by the fact that in many birds and mammals even basal metabolic rate hardly differs between summer and winter (McKechnie et al, 2015; Schaeffer et al ., 2020). When differences are observed they rarely exceed more than 30%, whereas a factor of 10‐15 would be required if the productivity of mammalian or avian populations were to be brought into line with the productivity of individual mammals or birds.…”