Aerobic characteristics of red kangaroo skeletal muscles: is a high aerobic capacity matched by muscle mitochondrial and capillary morphology as in placental mammals?
Marsupials and placentals together comprise the Theria, the advanced mammals, but they have had long independent evolutionary histories, with the last common ancestor occurring more than 125 million years ago. Although in the past the marsupials were considered to be metabolically 'primitive', the red kangaroo Macropus rufus has been reported to have an aerobic capacity (VO2max) comparable to that of the most 'athletic' of placentals such as dogs. However, kangaroos travel at moderate speeds with lower relative cost than quadrupedal placentals. Given the long independent evolution of the two therian groups, and their unusual locomotor energetics, do kangaroos achieve their high aerobic capacity using the same structural and functional mechanisms used by (athletic) placentals? Red kangaroo skeletal muscle morphometry matched closely the general aerobic characteristics of placental mammals. The relationship between total mitochondrial volume in skeletal muscle and VO2max during exercise was identical to that in quadrupedal placentals, and differed from that in bipedal humans. As for placentals generally, red kangaroo mitochondrial oxygen consumption at VO2max was 4.7 ml O2 min(-1) ml(-1) of mitochondria. Also, the inner mitochondrial membrane densities were 35.8 +/- 0.7 m2 ml(-1) of mitochondria, which is the same as for placental mammals, and the same pattern of similarity was seen for capillary densities and volumes. The overall data for kangaroos was equivalent to that seen in athletic placentals such as dogs and pronghorns. Total skeletal muscle mass was high, being around 50% of body mass, and was concentrated around the pelvis and lower back. The majority of the muscles sampled had relatively high mitochondrial volume densities, in the range 8.8-10.6% in the major locomotor muscles. Again, capillary densities and capillary blood volumes followed the pattern seen for mitochondria. Our results indicate that the red kangaroo, despite its locomotion and extreme body form, shows fundamental aerobic/muscular relationships that appear common to both marsupials and placentals. The evolution of such metabolic relationships apparently predates the divergence of the therian groups in the early Cretaceous, and perhaps evolved in the mammal-like reptiles during the Triassic (220 million years ago) before the actual evolution of the mammals.
Dawson
Terence J
TJ
School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, NSW 2052, Australia. t.dawson@unsw.edu.au
Mifsud
Brock
B
Raad
Matthew C
MC
Webster
Koa N
KN
D000704:Analysis of Variance; D000818:Animals; D005075:Biological Evolution; D001810:Blood Volume; D001824:Body Constitution; D001837:Body Weights and Measures; D002196:Capillaries / Q000033:anatomy & histology*; D007614:Macropodidae / Q000033:anatomy & histology* / Q000502:physiology*; D008854:Microscopy, Electron; D008931:Mitochondria, Muscle / Q000502:physiology*; D018482:Muscle, Skeletal / Q000502:physiology* / Q000648:ultrastructure; D010101:Oxygen Consumption / Q000502:physiology*