Stable carbon isotopes in breath reveal fast incorporation rates and seasonally variable but rapid fat turnover in the common shrew (Sorex araneus)

Abstract

Small non-migratory mammals with Northern distribution ranges apply a variety of behavioural and physiological wintering strategies. A rare energy-saving strategy is Dehnel's phenomenon, involving a reduction and later regrowth of the body size, several organs and parts of the skeleton in red-toothed shrews (Soricidae). The size extremes coincide with major life stages. However, the physiological consequences for the shrew's metabolism remain poorly understood. In keeping with the energetic limitations that may induce the size changes, we hypothesised that metabolic incorporation rates should remain the same across the shrews' lifetimes. In contrast, fat turnover rates should be faster in smaller subadults than in large juveniles and regrown adults, as the metabolic activity of fat tissue increases in winter individuals (subadults). Measuring the changes in the ratio of exhaled stable carbon isotopes, we found that the baseline diet of shrews changed across the season. A diet switch experiment showed that incorporation rates were consistently rapid (=38.2±21.1-69.3±53.5 min) and did not change between seasons. As predicted, fat turnover rates were faster in size-reduced subadults (=2.1±1.3 h) compared with larger juveniles (=5.5±1.7 h) and regrown adults (=5.0±4.4 h). In all three age/size classes, all body fat was turned over after 9-24 h. These results show that high levels of nutrient uptake are independent of body size, whereas fat turnover rates are negatively correlated with body size. Thus, the shrews might be under higher pressure to save energy in winter and this may have supported the evolution of Dehnel's phenomenon.

Metabolic partitioning of sucrose and seasonal changes in fat turnover rate in ruby-throated hummingbirds (Archilochus colubris)

“…where f exo∞ is the asymptote, k is the rate of carbon incorporation per hour and t is time in hours. We estimated the t 50 , the time it takes for 50% of the carbons in the fat pool to turn over, as follows (Keicher et al, 2017):…”

“…For example, broad-tailed hummingbirds (Selasphorus platycercus) turn over 50% of carbon in fat stores (termed t 50 ) in approximately 25 h (Carleton et al, 2006). Small mammals also exhibit rapid fat turnover rates, with a t 50 of 21 h in Peters' tent-making bat (Urogerma bilobatum; O'Mara et al, 2017), and the exceptionally fast t 50 of less than 5 h in the common shrew (Sorex araneus; Keicher et al, 2017). Turnover rates decrease when examining slightly larger animals, such as gerbils (Merion unguierlatus), that have a t 50 of ∼15.6 days (Tieszen et al, 1983).…”

“…In common shrews, life stage, in combination with changes in body mass, influences fat turnover rate. Larger juveniles have slower turnover rates than smaller subadult individuals (Keicher et al, 2017). Furthermore, the rate of carbon incorporation generally scales negatively with body mass in birds (Carleton and Martinez del Rio, 2005).…”

“…Furthermore, the rate of carbon incorporation generally scales negatively with body mass in birds (Carleton and Martinez del Rio, 2005). Thus, changes in body mass, fat reserves, energy expenditure and life history traits may influence the rate of fat turnover in animals (Brown, 2000;Keicher et al, 2017). Seasonal and environmental differences contributed to a 3-fold difference in daily energy expenditure in broad-tailed hummingbirds (Shankar et al, 2019).…”

“…Fat turnover rates have been studied by assessing variation in the stable carbon isotopic breath signatures of animals when lipid stores have been isotopically labeled (Carleton et al, 2006;Keicher et al, 2017;O'Mara et al, 2017). This is achieved by switching animals from a diet with one carbon stable isotope signature to a diet with another stable isotope signature.…”