Anatomical adaptations of the hind limb musculature of tree-kangaroos for arboreal locomotion (Marsupialia : Macropodinae)
Natalie M. Warburton A B D , Maud Yakovleff C and Auréline Malric C
+ Author Affiliations
- Author Affiliations
A School of Veterinary and Biomedical Science, Murdoch University, South Street, Murdoch, WA 6150, Australia.
B Department of Earth and Planetary Sciences, Western Australian Museum, 49 Kew Street, Welshpool, WA 6106, Australia.
C L’Ecole Nationale Veterinaire de Toulouse, 23 Chemin des Capelles, BP 87614, 31076 Toulouse cedex 03, France.
D Corresponding author. Email: N.Warburton@murdoch.edu.au
Australian Journal of Zoology 60(4) 246-258 https://doi.org/10.1071/ZO12059
Submitted: 1 June 2012 Accepted: 18 October 2012 Published: 22 November 2012
Abstract
Tree-kangaroos (Dendrolagini) are Australasian marsupials that inhabit tropical forests of far north-eastern Queensland and New Guinea. The secondary adaptation of tree-kangaroos to an arboreal lifestyle from a terrestrial heritage offers an excellent opportunity to study the adaptation of the musculoskeletal system for arboreal locomotion, particularly from a template well adapted to terrestrial bipedal saltation. We present a detailed descriptive study of the hind limb musculature of Lumholtz’s tree-kangaroo (D. lumholtzi) in comparison to other macropodines to test whether the hind limb musculature of tree-kangaroos is functionally adapted to the different mechanical demands of locomotion in the uneven three-dimensional arboreal environment. The hind limb musculature of Lumholtz’s tree-kangaroo (Dendrolagus lumholtzi), the western brush wallaby (Macropus irma), the western grey kangaroo (Macropus fuliginosus) and the quokka (Setonix brachyurus) are described. The hind limb anatomy of D. lumholtzi differed from that of the terrestrial macropodines in that the muscles had a greater degree of internal differentiation, relatively longer fleshy bellies and very short, stout tendons of insertion. There was also a modified arrangement of muscle origins and insertions that enhance mechanical advantage. Differences in the relative proportions of the hind limb muscle mass between tree-kangaroos and terrestrial macropodines reflect adaptation of the limb musculature of tree-kangaroos for arboreal locomotion. The hind limb musculature of Setonix was different to that of both Dendrolagus and Macropus, possibly reflecting its more basal phylogenetic position within the Macropodinae.
Additional keywords: Dendrolagus, marsupial evolution, myology, Setonix.
References
Alexander, M. R., and Vernon, A. (1975). Mechanics of hopping by kangaroos (Macropodidae). Journal of Zoology 17, 265–303.Anapol, F., and Barry, K. (1996). Fiber architecture of the extensors of the hindlimb in semiterrestrial and arboreal guenons. American Journal of Physical Anthropology 99, 429–447.
| Fiber architecture of the extensors of the hindlimb in semiterrestrial and arboreal guenons.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2s%2Fgt1yntg%3D%3D&md5=208f168865660717c349e7cb8c5d0f4cCAS |
Argot, C. (2001). Functional-adaptive anatomy of the forelimb in the Didelphidae, and the paleobiology of the Paleocene marsupials Mayulestes ferox and Pucadelphys andinus. Journal of Morphology 247, 51–79.
| Functional-adaptive anatomy of the forelimb in the Didelphidae, and the paleobiology of the Paleocene marsupials Mayulestes ferox and Pucadelphys andinus.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3M7gs1WrsA%3D%3D&md5=b14e0716677164c5a556ee60f91bec10CAS |
Badoux, D. M. (1965). Some notes on the functional anatomy of Macropus giganteus Zimm. with general remarks on the mechanics of bipedal leaping. Acta Anatomica 62, 418–433.
| Some notes on the functional anatomy of Macropus giganteus Zimm. with general remarks on the mechanics of bipedal leaping.Crossref | GoogleScholarGoogle Scholar |
Bishop, N. (1997). Functional anatomy of the macropodid pes. Proceedings of the Linnean Society of New South Wales 117, 17–50.
Carlsson, A. (1914). Uber Dendrolagus dorianus. Zoologische Jahrbuecher. Abteilung fuer Systematic Oekologie und Geographie der Tiere 36, 547–617.
Carlsson, A. (1915). Zur Morphologie des Hypsiprymnodon moschatus. Kungelige Svenska Vetenskapsakademiens Handlingar 52, 1–51.
Cartmill, M. (1979). The volar skin of primates: its frictional characteristics and their functional significance. American Journal of Physical Anthropology 50, 497–509.
| The volar skin of primates: its frictional characteristics and their functional significance.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE1M3ivFaksQ%3D%3D&md5=7dc0d267179838cd9230922ee50be40fCAS |
Cartmill, M. (1985). Climbing. In ‘Functional Vertebrate Morphology’. (Eds M. Hildebrand, D. M. Bramble, K. F. Liem and D. B. Wake.) pp. 73–88. (Belknap Press: Cambridge.)
Dawson, L. (2004). A new Pliocene tree kangaroo species (Marsupialia: Macropodinae) from the Chinchilla Local Fauna, southeastern Queensland. Alcheringa 28, 267–273.
| A new Pliocene tree kangaroo species (Marsupialia: Macropodinae) from the Chinchilla Local Fauna, southeastern Queensland.Crossref | GoogleScholarGoogle Scholar |
Dublin, L. I. (1903). Adaptations to aquatic, arboreal, fossorial and cursorial habits in mammals, II. Arboreal adaptations. American Naturalist 37, 731–736.
| Adaptations to aquatic, arboreal, fossorial and cursorial habits in mammals, II. Arboreal adaptations.Crossref | GoogleScholarGoogle Scholar |
Elftman, H. O. (1929). Functional adaptations of the pelvis in marsupials. Bulletin of the American Museum of Natural History LVIII, 189–232.
Flannery, T. (1989). Phylogeny of the Macropodoidea: a study in convergence. In ‘Kangaroos, Wallabies and Rat-kangaroos’. (Eds G. Grigg, P. Jarman and I. Hume.) pp. 1–46. (Surrey Beatty: Sydney.)
Flannery, T. F. (1990). ‘Mammals of New Guinea.’ (Robert Brown and Associates: Brisbane.)
Flannery, T. F., and Szalay, F. (1982). Bohra paulae, a new giant fossil tree kangaroo (Marsupialia: Macropodidae) from New South Wales, Australia. Australian Mammalogy 5, 83–94.
Flannery, T. F., Martin, R. D., and Szalay, A. (1996). ‘Tree Kangaroos: A Curious Natural History.’ (Reed Books: Australia.)
Fleagle, J. G. (1999). ‘Primate Evolution and Adaptations.’ 2nd edn. (Academic Press: San Diego, CA.)
Grand, T. I. (1983). Body weight: its relationship to tissue composition, segmental distribution of mass, and motor function. III. The Didelphidae of French Guyana. Australian Journal of Zoology 31, 299–312.
| Body weight: its relationship to tissue composition, segmental distribution of mass, and motor function. III. The Didelphidae of French Guyana.Crossref | GoogleScholarGoogle Scholar |
Grand, T. I. (1990a). Body composition and the evolution of the Macropodidae (Potorous, Dendrolagus and Macropus). Anatomy and Embryology 182, 85–92.
| Body composition and the evolution of the Macropodidae (Potorous, Dendrolagus and Macropus).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3M%2Flt1Citg%3D%3D&md5=2022e4cf65f56d9f34b69c44253b6b81CAS |
Grand, T. I. (1990b). The functional anatomy of body mass. In ‘Body Size in Mammalian Paleobiology: Estimation and Biological Implications’. (Ed. B. J. M. J. Damuth.) pp. 39–48. (Cambridge University Press: Cambridge.)
Harvey, K. J., and Warburton, N. M. (2010). Forelimb musculature of kangaroos with particular emphasis on the tammar wallaby Macropus eugenii (Desmarest, 1817). Australian Mammalogy 32, 1–9.
Hocknull, S. A. (2005). Additional specimens of Bohra (Marsupialia: Macropodidae) from the Pliocene of Queensland. Memoirs of the Queensland Museum 51, 26.
Hopwood, P. R., and Butterfield, R. M. (1976). The musculature of the proximal pelvic limb of the eastern grey kangaroo Macropus major (Shaw) Macropus giganteus (Zimm). Journal of Anatomy 121, 259–277.
| 1:STN:280:DyaE283ht1Ohuw%3D%3D&md5=ab37a21bcfeae4928643b091dd735989CAS |
Hopwood, P. R., and Butterfield, R. M. (1990). The locomotor apparatus of the crus and pes of the eastern grey kangaroo, Macropus giganteus. Australian Journal of Zoology 38, 397–413.
| The locomotor apparatus of the crus and pes of the eastern grey kangaroo, Macropus giganteus.Crossref | GoogleScholarGoogle Scholar |
Iwaniuk, A. N., Nelson, J. E., Ivanco, T. L., Pellis, S. M., and Whishaw, I. Q. (1998). Reaching, grasping and manipulation of food objects by two tree kangaroo species, Dendrolagus lumholtzi and Dendrolagus matschiei. Australian Journal of Zoology 46, 235–248.
| Reaching, grasping and manipulation of food objects by two tree kangaroo species, Dendrolagus lumholtzi and Dendrolagus matschiei.Crossref | GoogleScholarGoogle Scholar |
Jungers, W. L. (1984). Aspects of size and scaling in primate biology with special reference to the locomotor skeleton. American Journal of Physical Anthropology 27, 73–97.
| Aspects of size and scaling in primate biology with special reference to the locomotor skeleton.Crossref | GoogleScholarGoogle Scholar |
Lodder, M. (1991). Functional morphology of the hindleg in two kangaroos Macropus giganteus and Aepyprymnus rufescens. European Journal of Morphology 29, 5–30.
| 1:STN:280:DyaK3M3otlentQ%3D%3D&md5=fd7202427e40991fd829c51b693565fcCAS |
McGowan, C. P., Skinner, J., and Biewener, A. A. (2008). Hind limb scaling of kangaroos and wallabies (superfamily Macropodoidea): implications for hopping performance, safety factor and elastic savings. Journal of Anatomy 212, 153–163.
| Hind limb scaling of kangaroos and wallabies (superfamily Macropodoidea): implications for hopping performance, safety factor and elastic savings.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1c%2Fps1Omtg%3D%3D&md5=f9f3ad94f122b5bc57c6e81194b10d1cCAS |
Organ, J. M. (2010). Structure and function of platyrrhine caudal vertebrae. The Anatomical Record: Advances in Integrative Anatomy and Evolutionary Biology 293, 730–745.
| Structure and function of platyrrhine caudal vertebrae.Crossref | GoogleScholarGoogle Scholar |
Organ, J., Teaford, M., and Taylor, A. (2009). Functional correlates of fiber architecture of the lateral caudal musculature in prehensile and nonprehensile tails of the Platyrrhini (Primates) and Procyonidae (Carnivora). The Anatomical Record 292, 827–841.
| Functional correlates of fiber architecture of the lateral caudal musculature in prehensile and nonprehensile tails of the Platyrrhini (Primates) and Procyonidae (Carnivora).Crossref | GoogleScholarGoogle Scholar |
Parsons, F. G. (1896). On the anatomy of Petrogale xanthopus, compared with that of other kangaroos. Proceedings of the Zoological Society, London, 683–714.
Prideaux, G. J., and Warburton, N. M. (2008). A new fossil tree-kangaroo (Diprotodontia: Macropodidae) from the Nullarbor Plain of south-central Australia. Journal of Vertebrate Paleontology 28, 463–478.
| A new fossil tree-kangaroo (Diprotodontia: Macropodidae) from the Nullarbor Plain of south-central Australia.Crossref | GoogleScholarGoogle Scholar |
Prideaux, G. J., and Warburton, N. M. (2009). Bohra nullarbora sp. nov., a second tree-kangaroo (Marsupialia: Macropodidae) from the Pleistocene of the Nullarbor Plain, Western Australia. Records of the Western Australian Museum 25, 165–179.
Prideaux, G. J., and Warburton, N. M. (2010). An osteology-based appraisal of the phylogeny and evolution of kangaroos and wallabies (Macropodidae: Marsupialia). Zoological Journal of the Linnean Society 159, 954–987.
| An osteology-based appraisal of the phylogeny and evolution of kangaroos and wallabies (Macropodidae: Marsupialia).Crossref | GoogleScholarGoogle Scholar |
Procter-Gray, E., and Ganslosser, U. (1986). The individual behaviors of Lumholtz’s tree-kangaroo: repertoire and taxonomic implications. Journal of Mammalogy 67, 343–352.
| The individual behaviors of Lumholtz’s tree-kangaroo: repertoire and taxonomic implications.Crossref | GoogleScholarGoogle Scholar |
Schmidt, M. (2005a). Hind limb proportions and kinematics: are small primates different from other small mammals? The Journal of Experimental Biology 208, 3367–3383.
| Hind limb proportions and kinematics: are small primates different from other small mammals?Crossref | GoogleScholarGoogle Scholar |
Schmidt, M. (2005b). Quadrupedal locomotion in squirrel monkeys (Cebidae: Saimiri sciureus): a cineradiographic study of limb kinematics and related substrate reaction forces. American Journal of Physical Anthropology 128, 359–370.
| Quadrupedal locomotion in squirrel monkeys (Cebidae: Saimiri sciureus): a cineradiographic study of limb kinematics and related substrate reaction forces.Crossref | GoogleScholarGoogle Scholar |
Schmitt, D. (2003). Substrate size and primate forelimb mechanics: implications for understanding the evolution of primate locomotion. International Journal of Primatology 24, 1023–1036.
| Substrate size and primate forelimb mechanics: implications for understanding the evolution of primate locomotion.Crossref | GoogleScholarGoogle Scholar |
Schmitt, D., and Lemelin, P. (2002). Origins of primate locomotion: gait mechanics of the woolly opossum. American Journal of Physical Anthropology 118, 231–238.
| Origins of primate locomotion: gait mechanics of the woolly opossum.Crossref | GoogleScholarGoogle Scholar |
Warburton, N. M., and Prideaux, G. J. (2010). Functional pedal morphology of the extinct tree-kangaroo Bohra (Diprotodontia: Macropodidae). In ‘Macropods: The Biology of Kangaroos, Wallabies and Rat-kangaroos’. (Eds G. Coulson and M. D. B. Eldridge.) pp. 137–151. (CSIRO Publishing: Melbourne.)
Windle, B. C. A., and Parsons, F. G. (1898). On the anatomy of Macropus rufus. Journal of Anatomy and Physiology 32, 119–134.
Windsor, D. E., and Dagg, A. I. (1971). The gaits of the Macropodinae (Marsupialia). Journal of Zoology 163, 165–175.
| The gaits of the Macropodinae (Marsupialia).Crossref | GoogleScholarGoogle Scholar |
Winter, J., Burnett, S., and Martin, R. (2008). Dendrolagus lumholtzi. In ‘IUCN Red List of Threatened Species. Version 2012.1’.
