Functional capacities of marsupial hearts: size and mitochondrial parameters indicate higher aerobic capabilities than generally seen in placental mammals

Abstract

This study of marsupial hearts explored the aerobic capacities of this group of mammals; recent information suggests that marsupials possess higher aerobic abilities than previously accepted. Characteristics such as heart mass, mitochondrial features and capillary parameters were examined. A comprehensive study of the heart of red kangaroos was included because of the high maximum oxygen consumption of this species. Goats were also included as a reference placental mammal. Marsupials have a heart that is generally larger than that of placentals. The allometric equation for the relationship between heart mass and body mass for marsupials was M(h)=7.5M(b)(0.944) (M(h) in g and M(b) in kg); the equivalent equation for placental mammals was M(h)=6.0M(b)(0.97). Mitochondrial volume density and inner mitochondrial surface density do not differ between the two mammal groups; although capillary parameters indicated a lower capillary volume in marsupials. Heart size appears to be the major difference between the two groups. The overall pattern seen in marsupials is similar to that of "athletic" placentals and indicates a relatively high aerobic potential.

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

“…The strength of this paradigm was such that when the unusual energetic characteristics of the hopping of M. rufus were uncovered (Dawson and Taylor, 1973) they were seen to represent a strategy to overcome metabolic limitations (Dawson, 1977). However, from further work on M. rufus, this was seen not to be true; via a large factorial aerobic scope (fAS) of 54, it achieves a maximal aerobic oxygen consumption (V O2,max ) comparable to that of athletic placentals (Kram and Dawson, 1998;Dawson et al, 2003). Studies point to other marsupials, including quadrupedal species, having similar V O2,max to some placentals, due to expanded aerobic scopes (Dawson and Dawson, 1982;Hinds et al, 1993), but their fAS values do not approach those of M. rufus.…”

The kangaroo's tail propels and powers pentapedal locomotion

“…Lett. 10: 20140381 may have freed the kangaroo's front limbs to play a reduced role during slow-speed grazing [2,10]. Kangaroo tails have evolved considerably from the prehensile role they played in arboreal ancestors to modern-day terrestrial kangaroos [15].…”

“…Kangaroo tails appear to be biomechanically and physiologically capable structures-the tail muscles are much larger than the muscles of the front limbs and they are dense with mitochondria suggesting a large aerobic capacity [10]. The kangaroo's tail anatomy, however, is quite distinct from the front and hind limbs-it comprises more than 20 caudal vertebrae rather than a few long bones [11].…”

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.

“…Following this concept, there are numerous other studies that lend support for a generally high MMR in marsupials. These examined lung structure and function of the respiratory system (Dawson and Needham, 1981;Hallam et al, 1989;Chappell and Dawson, 1994;Dawson et al, 2000b), heart structure and capacities (Dawson and Needham, 1981;Dawson et al, 2003), blood oxygen affinities (Hallam et al, 1995) and relative haematocrit levels (Agar et al, 2000). Broadly then, clades of mammals, both placental and marsupial, have evolved elevated aerobic capacities that can be sustained by small species for at least several minutes and for relatively longer periods in larger species.…”

“…Evidence for 'athletic' level aerobic capacities in other marsupials is strong and comes from disparate studies of their cardio-respiratory features (e.g. Dawson and Needham, 1981;Hallam et al, 1989;Hallam et al, 1995;Agar et al, 2000;Dawson et al, 2003). 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.…”