Muscle mitochondrial volume and aerobic capacity in a small marsupial (Sminthopsis crassicaudata) match those of 'athletic' placentals, reflecting flexible links between energy-use levels in mammals generally.

Abstract

SummaryWe investigated the muscle structure/function relationships that underlie the aerobic capacities of an insectivorous, small (~15 g) marsupial, Sminthopsis crassicaudata (Family: Dasyuridae). This was for further insight into energy use patterns in marsupials, relative to those in placentals, their sister clade within the Theria (advanced mammals). Disparate hopping marsupials (Suborder Macropodiformes), a kangaroo (Macropus rufus) and a rat-kangaroo (Bettongia penicillata), show aerobic capabilities as high as those of athletic placentals. Equivalent muscle mitochondrial volumes and cardiovascular features support these capabilities. We examined S. crassicaudata to determine whether highly developed aerobic capabilities are widespread in marsupials, rather than just being in the lately evolved Macropodiformes. This was the case. Treadmill-trained S. crassicaudata attained a maximal aerobic metabolic rate (V.O2max or MMR) of 272 mlO2 min-1 kg-1 (N=8), similar to that reported for a small (~20g), athletic placental, Apodemus sylvaticus, 264 mlO2 min-1 kg-1. Hopping marsupials have comparable aerobic levels when body mass variation is considered. S. crassicaudata has a basal metabolic rate (BMR) about 75% of placental values but it has a notably large factorial aerobic scope (fAS) of 13; elevated fAS also feature in hopping marsupials. The V.O2max of S. crassicaudata was supported by an elevated total muscle mitochondria volume, which was largely achieved through high muscle mitochondria volume densities, Vv(mt,f), the mean value being 14.0 ± 1.33%. These data were considered in relation to energy use levels in mammals, particularly field metabolic rate (FMR). BMR is consistently lower in marsupials, but this is balanced out by a high fAS, such that marsupial MMR matches that of placentals. However, FMR shows different mass relationships in the two clades, with the FMR of small (<125 g) marsupials being higher than in comparable placentals with the reverse applying for larger marsupials. The flexibility of energy output in marsupials provides explanations for this pattern. Overall our data refute widely held notions of mechanistically closely linked relationships between body mass, BMR, FMR and MMR in mammals.