Muscle fibre types in the reduced forelimb and enlarged hindlimb of the quokka (Setonix brachyurus, Macropodidae)
A. Casinos A E , N. Milne B , F. K. Jouffroy C and M. F. Médina DA Departament de Biologia Evolutiva, Ecologia i Ciències Ambientals, Universitat de Barcelona, Barcelona 08007, Spain.
B School of Anatomy, Physiology and Human Biology, University of Western Australia, Crawley, WA 6009, Australia.
C Deceased. Formerly of CNRS, Muséum National d’Histoire Naturelle, Paris 75005, France and Anatomical Sciences, University of Stony Brook, Stony Brook, NY 11790, USA.
D USM 301 Muséum National d’Histoire Naturelle, Paris 75005, France.
E Corresponding author. Email: acasinos@ub.edu
Australian Journal of Zoology 64(4) 277-284 https://doi.org/10.1071/ZO15055
Submitted: 15 September 2015 Accepted: 28 October 2016 Published: 1 December 2016
Abstract
The quokka (Setonyx brachyurus) is restricted to two offshore islands and small isolates on the mainland of south-western Australia. It displays a tendency to saltatorial locomotion and moves at speed by bipedal hopping, although it also uses its forelimbs at low speed. Its bipedal adaptation involves enlarged hind limbs, with elongated feet. The fibre type distribution of the elbow and knee extensors, and the ankle plantar flexors, in comparison with two eutherians, the quadrupedal rhesus monkey, as a locomotor generalist, and the jerboa, a small eutherian hopping species morphologically similar to the quokka, were studied. The quokka’s forelimb showed the same characteristics as that of the jerboa, lacking the fatigue-resistant Type I fibres that are used to sustain posture. As in the jerboa, the gastrocnemius lateralis was the muscle head with the highest proportion of fast twitch fibres. Muscular fibre pattern is not identical in the quokka and the jerboa hindlimb, but it appears that both species have similar anatomical adaptations to saltatorial locomotion. Differences in muscle fibre proportions could be due to several factors including, resting posture, body size and the propensity for elastic energy storage, the burrowing behaviour of the jerboa, but also to phylogenetic constraints where the adaptation to hop on the hindlimbs is a shared behaviour of the Macropodoidea (jerboas are the only Dipodidae to have elongated hindlimbs).
Additional keywords: hopping, locomotion, marsupials.
References
Alexander, R. McN., Jayes, A. S., Maloiy, G. M. O., and Wathuta, E. M. (1979). Allometry of the limb bones of mammals from shrews (Sorex) to elephant (Loxodonta). Journal of Zoology 189, 305–314.| Allometry of the limb bones of mammals from shrews (Sorex) to elephant (Loxodonta).Crossref | GoogleScholarGoogle Scholar |
Alexander, R. McN., Jayes, A. S., Maloiy, G. M. O., and Wathuta, E. M. (1981). Allometry of the leg muscles of mammals. Journal of Zoology 194, 539–552.
| Allometry of the leg muscles of mammals.Crossref | GoogleScholarGoogle Scholar |
Anapol, F., and Jungers, W. L. (1986). Architectural and histochemical diversity within the quadriceps femoris of the brown lemur (Lemur fulvus). American Journal of Physical Anthropology 69, 355–375.
| Architectural and histochemical diversity within the quadriceps femoris of the brown lemur (Lemur fulvus).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL283ht1Grtg%3D%3D&md5=6c58a2a189d63f43681dd670934788c1CAS |
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 |
Baudinette, R. V. (1977). Locomotory energetics in a marsupial, Setonix brachyurus. Australian Journal of Zoology 25, 423–428.
| Locomotory energetics in a marsupial, Setonix brachyurus.Crossref | GoogleScholarGoogle Scholar |
Bennett, M. B., and Taylor, G. C. (1995). Scaling of elastic energy in kangaroos and the benefits of being big. Nature 378, 56–59.
| Scaling of elastic energy in kangaroos and the benefits of being big.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXptVyqsr4%3D&md5=cb577a7a2be7817f310e3847a1f0e9e9CAS |
Biewener, A. A., and Baudinette, R. V. (1995). In vivo muscle force and elastic energy storage during steady-speed hopping of tammar wallabies (Macropus eugenii). The Journal of Experimental Biology 198, 1829–1841.
Bou, J., Casinos, A., and Ocaña, J. (1987). Allometry of the limb long bones of insectivores and rodents. Journal of Morphology 192, 113–123.
| Allometry of the limb long bones of insectivores and rodents.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2s3lsVahsA%3D%3D&md5=f23d98040e33350d347fa050c5ad0d6eCAS |
Bou, J., Castiella, M. J., Ocaña, J., and Casinos, A. (1990). Multivariate analysis and locomotor morphology in insectivores and rodents. Zoologischer Anzeiger 225, 287–294.
Bullimore, S. R., and Burn, J. F. (2005). Scaling of elastic energy storage in mammalian limb tendons: do small mammals really lose out? Biology Letters 1, 57–59.
| Scaling of elastic energy storage in mammalian limb tendons: do small mammals really lose out?Crossref | GoogleScholarGoogle Scholar |
Castiella, M. J., and Casinos, A. (1990). Allometry of leg muscles in insectivores and rodents. Annales des Sciences Naturelles, Zoologie 11, 165–178.
Cavagna, G. A. (1988). ‘Muscolo e Locomozione.’ (Raffaelo Cortina: Milano.)
Dawson, R., Warburton, N. M., Richards, H. L., and Milne, N. (2015). Walking on five legs: investigating tail use during slow gait in kangaroos and wallabies. Australian Journal of Zoology 63, 192–200.
| Walking on five legs: investigating tail use during slow gait in kangaroos and wallabies.Crossref | GoogleScholarGoogle Scholar |
Dennington, S., and Baldwin, J. (1988). Biochemical correlates of energy metabolism in muscles used to power hopping by kangaroos. Australian Journal of Zoology 36, 229–240.
| Biochemical correlates of energy metabolism in muscles used to power hopping by kangaroos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXkvFCnu7o%3D&md5=32a722f0ea305199cb58add976f04420CAS |
Dennis, A. J., and Johnson, P. M. (1995). Musky rat-kangaroo Hypsiprymnodon moschatus. In ‘The Mammals of Australia’. (Ed. R. Strahan.) pp. 282–284. (Reed New Holland: Sydney.)
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 |
Jouffroy, F. K. (1971). Musculature des membres. In ‘Traité de Zoologie’. (Ed. P. P. Grassé.) tome XVI, fascicule III, pp. 1–475. (Masson: Paris.)
Jouffroy, F. K., and Lessertisseur, J. (1979). Relationships between limb morphology and locomotor adaptations among prosimians: an osteometric study. In ‘Environment, Behavior and Morphology: Dynamic Interaction in Primates’. (Eds M. E. Morbeck, H. Preuschoft, and N. Gomberg.) pp. 143–181. (Fischer: New York.)
Jouffroy, F. K., and Médina, M. F. (1996). Developmental changes in the fibre composition of elbow, knee, and ankle extensor muscles in cercopithecid monkeys. Folia Primatologica 66, 55–67.
| Developmental changes in the fibre composition of elbow, knee, and ankle extensor muscles in cercopithecid monkeys.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2s7ht1Sitg%3D%3D&md5=ee728ed73fcec1a651a158b57996f468CAS |
Jouffroy, F. K., and Médina, M. F. (2004). Comparative fiber-type composition and size in the antigravity muscles of primate limbs. In ‘Shaping Primate Evolution. Form, Function and Behavior’. (Eds F. Anapol, R. Z. German, and N. G. Jabolnsky.) pp. 134–161. (Cambridge University Press: Cambridge.)
Jouffroy, F. K., Stern, J. T., Médina, M. F., and Larson, S. G. (1999). Function and cytochemical characteristics of postural limb muscles of the Rhesus monkey: a telemetered EMG and immunofluorescence study. Folia Primatologica 70, 235–253.
| Function and cytochemical characteristics of postural limb muscles of the Rhesus monkey: a telemetered EMG and immunofluorescence study.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c%2Fjs1CksQ%3D%3D&md5=6221ba125a66dbc5d3f7b4bb8d4c6935CAS |
Jouffroy, F. K., Médina, M. F., Renous, S., and Gasc, J. P. (2003). Immunocytochemical characteristics of elbow, knee and ankle extensors of the five-toed jerboa (Allactaga elater). Journal of Anatomy 202, 373–386.
| Immunocytochemical characteristics of elbow, knee and ankle extensors of the five-toed jerboa (Allactaga elater).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3s3hvVaisA%3D%3D&md5=2ad4f4b1d6556ec0ff898077fef75725CAS |
Kitchener, D. J. (1995). Quokka Setonyx brachyurus. In ‘The Mammals of Australia’. (Ed. R. Strahan.) pp. 401–403. (Reed New Holland: Sydney.)
Kojima, R., Médina, M. F., Jouffroy, F. K., and Okada, M. (2002). Effects of fixation and preservation conditions on immunohistochemical profiles of the skeletal muscle fibers in Japanese macaques. Zeitschrift fur Morphologie und Anthropologie 83, 315–324.
Macdonald, D. W. (2006). ‘The Encyclopedia of Mammals.’ (Oxford University Press: Oxford.)
McMahon, T. A. (1984). ‘Muscles, Reflexes, and Locomotion.’ (Princeton University Press: Princeton, NJ.)
Myatt, J. P., Schilling, N., and Thorpe, S. K. S. (2011). Distribution patterns of fibre types in the triceps surae muscle group of chimpanzees and orangutans. Journal of Anatomy 218, 402–412.
| Distribution patterns of fibre types in the triceps surae muscle group of chimpanzees and orangutans.Crossref | GoogleScholarGoogle Scholar |
Ngu, N. T., and Nhan, N. T. H. (2012). Analysis of troponin I gene polymorphisms and meat quality in Mongcai pigs. South African Journal of Animal Science 42, .
| Analysis of troponin I gene polymorphisms and meat quality in Mongcai pigs.Crossref | GoogleScholarGoogle Scholar |
Nowak, R. M. (1999). ‘Walker’s Mammals of the World’. Volume II. 6th edn. (The Johns Hopkins University Press: Baltimore.)
Olmos, M., Casinos, A., and Cubo, J. (1996). Limb allometry in birds. Annales des Sciences Naturelles, Zoology 17, 39–49.
Pette, D., and Staron, R. S. (1997). Mammalian skeletal muscle fiber type transitions. International Review of Cytology 170, 143–223.
| Mammalian skeletal muscle fiber type transitions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXhvFCksLY%3D&md5=c3f00338483e7555d8f1f840782207a9CAS |
Pette, D., and Staron, R. S. (2000). Myosin isoforms, muscle fibres types, and transitions. Microscopy Research and Technique 50, 500–509.
| Myosin isoforms, muscle fibres types, and transitions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXnslWhtL8%3D&md5=8c9a5176c6d25c21e28e42decf033ebdCAS |
Petter, A., and Jouffroy, F. K. (1993). Fiber type population in limb muscles of Microcebus murinus. Primates 34, 181–196.
| Fiber type population in limb muscles of Microcebus murinus.Crossref | GoogleScholarGoogle Scholar |
Pollock, C. M., and Shadwick, R. E. (1994). Allometry of muscle, tendon, and elastic energy storage capacity in mammals. American Journal of Physiology: Regulatory, Integrative and Comparative Physiology 266, R1022–R1031.
| 1:STN:280:DyaK2c3htlSquw%3D%3D&md5=12cec8116e76b94b601f494ffe3fe1acCAS |
Prats, C., Gómez-Cabello, C., Nordby, P., Andersen, J. L., Helhe, J. W., Dela, F., Baba, O., and Ploug, T. (2013). An optimized histochemical method to assess skeletal muscle glycogen and lipid stores reveals two metabolically distinct populations of Type I muscle fibers. PLoS ONE 8, e77774.
| An optimized histochemical method to assess skeletal muscle glycogen and lipid stores reveals two metabolically distinct populations of Type I muscle fibers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsleqtr%2FF&md5=3d2f40a9e46c320f76937e4ec70b6dc6CAS |
Richards, H. L., Grueter, C. C., and Milne, N. (2015). Strong arm tactics: sexual dimorphism in macropodid limb proportions. Journal of Zoology 297, 123–131.
| Strong arm tactics: sexual dimorphism in macropodid limb proportions.Crossref | GoogleScholarGoogle Scholar |
Schiaffino, S, and Reggiani, C (2011). Fiber types in mammalian skeletal muscles. Physiological Reviews 91, 1447–1531.
| Fiber types in mammalian skeletal muscles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsVOjsbrF&md5=7b3259d0e89809091b842864b8bb150aCAS |
Schiaffino, S., Gorza, L., Sartore, S., Saggin, L., Ausoni, S, Vianello, M., Gundersen, K., and LØmo, T (1989). Three myosin heavy chain isoforms in type 2 skeletal muscle fibres. Journal of Muscle Research and Cell Motility 10, 197–205.
| Three myosin heavy chain isoforms in type 2 skeletal muscle fibres.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXltFalsrg%3D&md5=6255bce2465c4cfd5fc4d1c704e5aabcCAS |
Spiegel, N. B., Beaton, A. J. W., McGrath, J., Thompson, J. M., Wynn, P. C., and Greenwood, P. L. (2002). Myofibre types in eight skeletal muscles from the eastern grey kangaroo (Macropus giganteus). Animal Production in Australia 24, 225–228.
Stephenson, G. M. M. (2006). Diversity and plasticity of vertebrate skeletal muscle: insights from hybrid fibres. Brazilian Journal of Morphological Sciences 23, 187–194.
Strahan, R. (1995). Family Macropodidae. In ‘The Mammals of Australia’. (Ed. R. Strahan.) pp. 303–305. (Reed New Holland: Sydney.)
Torrella, J. R., Whitmore, J. M., Casas, M., Fouces, V., and Viscor, G. (2000). Capillarity, fibre-types and fibre morphometry in different sampling sites across and along the tibialis anterior muscle of the rat. Cells, Tissues, Organs 167, 153–162.
| Capillarity, fibre-types and fibre morphometry in different sampling sites across and along the tibialis anterior muscle of the rat.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3cvls1KgtA%3D%3D&md5=cb3a0b77dbcdc2b596c4b71b728ee579CAS |
Wetzel, M. C., and Stuart, D. G. (1977). Activation and co-ordination of vertebrate locomotion. In ‘Mechanics and Energetics of Animal Locomotion’. (Eds R. McN. Alexander, and G. Goldspink) pp. 115–152. (Chapman and Hall: London.)
Zhong, W. W. H., Lucas, C. A., Kang, L. H., and Hoh, J. F. Y. (2001). Electrophoretic and immunochemical evidence showing that marsupial limb muscles express the same fast and slow myosin heavy chains as eutherians. Electrophoresis 22, 1016–1020.
| Electrophoretic and immunochemical evidence showing that marsupial limb muscles express the same fast and slow myosin heavy chains as eutherians.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjslWiurc%3D&md5=a033f7f49e1a10f24164cd9dc5f0d8e9CAS |
Zhong, W. W. H., Lucas, C. A., and Hoh, J. F. Y. (2008). Myosin isoforms and fibre types in limb muscles of Australian marsupials: adaptations to hopping and non-hopping locomotion. Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology 178, 47–55.
| Myosin isoforms and fibre types in limb muscles of Australian marsupials: adaptations to hopping and non-hopping locomotion.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmsFWlsg%3D%3D&md5=0fd13e859e9a1360b1c2f8842963b1d7CAS |