The high aerobic capacity of a small, marsupial rat-kangaroo (Bettongia penicillata) is matched by the mitochondrial and capillary morphology of its skeletal muscles

Abstract

Summary We examined the structure-function relationships that underlie the aerobic capacities of marsupial mammals that hop. Marsupials have relatively low basal metabolic rates (BMR) and historically were seen as 'low energy' mammals. However, the red kangaroo, Macropus rufus, (Family Macropodidae) has aerobic capacities equivalent to athletic placentals. It has an extreme aerobic scope (fAS) and its large locomotor muscles feature high mitochondrial and capillary volumes. M. rufus belongs to a modern group of kangaroos and its great fAS is not general for marsupials. However, other hopping marsupials may have elevated aerobic capacities. Bettongia penicillata, a rat-kangaroo (Family Potoroidae), is a small (1 kg) active hopper whose fAS is somewhat elevated. We examined the oxygen delivery system in its muscles to ascertain links with hopping. An elevated fAS of 23 provided a relatively high VO2max in B. penicillata; associated with this is a skeletal muscle mass of 44% of body mass. Ten muscles were sampled to estimate the total mitochondrial and capillary volume of the locomotor muscles. Values in B. penicillata were similar to those in M. rufus and in athletic placentals. This small hopper had high muscle mitochondrial volume densities (7.1-11.9%), and both a large total capillary volume (6 ml kg-1 body mass) and total capillary erythrocyte volume (3.2 ml kg-1). Apparently, a considerable aerobic capacity is required to achieve the benefits of the extended stride in fast hopping. Of note, the ratio of VO2max to total muscle mitochondrial volume in B. penicillata was 4.9 ml O2 min-1 ml-1. Similar values occur in M. rufus and also placental mammals generally, not only athletic species. If such relationships occur in other marsupials, a fundamental structure-function relationship for oxygen delivery to muscles likely originated with or before the earliest mammals.

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.

“…) is, as initially proposed (Hoppeler and Lindstedt, 1985), consistent in placentals (Weibel et al, 2004) and macropodiform marsupials (Webster and Dawson, 2012).…”

“…The generality of this assertion is not certain because, while Hinds and colleagues (Hinds et al, 1993) measured comparatively high fAS during locomotion for several smaller species of marsupial, their reported MMR values did not reach 'athletic' placental levels. However, the MMR value obtained (Hinds et al, 1993) for B. penicillata was lower than those obtained on more extensively trained animals Webster and Dawson, 2012). The only other marsupial for which comparable data are available is a South American opossum, Monodelphis domestica (Family: Didephidae) (M b ≈90g).…”

“…To assess the muscle mitochondrial parameters of the skeletal muscle of the whole body, we followed a sampling procedure comparable to that developed previously (Hoppeler et al, 1984) and used in other studies of marsupials (Dawson et al, 2004;Webster and Dawson, 2012). The musculature of S. crassicaudata was divided into five functional regions, these being head/neck, foreleg, trunk, hindleg and tail.…”

“…Underlying this capability in M. rufus is a large mass of locomotor muscles that have comparatively high mitochondrial and capillary volumes (Dawson et al, 2004). Another hopping marsupial, Bettongia penicillata, a rat-kangaroo (Family Potoroidae), though much smaller (body mass, M b , 1kg), also shows an elevated fAS of 23 and a markedly high MMR Webster and Dawson, 2012). Again, this is associated with a large skeletal muscle mass that has relatively high muscle mitochondrial volume densities and both a large total capillary volume and a large total capillary erythrocyte volume (Webster and Dawson, 2012).…”

“…Another hopping marsupial, Bettongia penicillata, a rat-kangaroo (Family Potoroidae), though much smaller (body mass, M b , 1kg), also shows an elevated fAS of 23 and a markedly high MMR Webster and Dawson, 2012). Again, this is associated with a large skeletal muscle mass that has relatively high muscle mitochondrial volume densities and both a large total capillary volume and a large total capillary erythrocyte volume (Webster and Dawson, 2012). Overall, the muscle and cardio-respiratory structural features of M. rufus and B. penicillata are identical to those previously reported for 'athletic' placental mammals of equivalent sizes (Weibel et al, 2004).…”