Skip to main content
SpringerLink
Log in

Aberrant back muscle function correlates with intramuscular architecture of dorsovertebral muscles in two-toed sloths

  • Original Investigation
  • Published:
Mammalian Biology Aims and scope Submit manuscript

Abstract

Sloths are morphologically specialized in upside-down quadrupedal suspensory locomotion. The evolution of this locomotor mode lead to a loss of asymmetrical gaits and thus a reduced necessity of powerful extension of the spine in the sagittal plane. It is here tested whether this aberrant locomotor mode is reflected in the three-dimensional (3D) intramuscular architecture of the dorsovertebral muscles of the two-toed sloth. Layer wise dissection of the transversospinal system, the longissimus, and the iliocostalis allowed for the 3D digitization of individual muscle fascicles. Fascicle length and orientation is quantified, and anatomical cross sectional area and muscle volume is calculated. Moment arms of the dorsovertebral muscles to the intervertebral joints are determined. Architectural properties of the dorsovertebral muscles in the sloth are in agreement with previous kinematic studies and in contrast to hitherto sampled upright quadrupedal mammals. The agreement of architectural properties with in vivo function documented in this study further characterizes the specific functional morphology of sloths, but also suggests a close relationship of back muscle architectural properties with locomotor mode of mammals in general.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Abdala, V., Moro, S., 2006. Comparative myology of the forelimb of Liolaemus sand lizards (Liolaemidae). Acta Zool. 87, 1–12.

    Article  Google Scholar 

  • Biewener, A.A., Konieczynski, D.D., Baudinette, R.V., 1998. In vivo muscle force-length behavior during steady-speed hopping in tammar wallabies. J. Exp. Biol. 201, 1681–1694.

    CAS  PubMed  Google Scholar 

  • Blemker, S.S., Delp, S.L., 2005. Three-dimensional representation of complex muscle architectures and geometries. Ann. Biomed. Eng. 33, 661–673.

    Article  PubMed  Google Scholar 

  • Cutts, A., Seedhom, B.B., 1993. Validity of cadaveric data for muscle physiological cross-sectional area ratios: a comparative study of cadaveric and in-vivo data in human thigh muscles. Clin. Biomech. (Bristol, Avon) 8, 156–162.

    Article  CAS  Google Scholar 

  • Dickinson, M.H., Farley, C.T., Full, R.J., Koehl, M., Kram, R., Lehman, S., 2000. How animals move: an integrative view. Science 288, 100–106.

    Article  CAS  PubMed  Google Scholar 

  • Dumas, G.A., Poulin, M.J., Roy, B., Gagnon, M., Jovanovic, M., 1988. A three-dimensional digitization method to measure trunk muscle lines of action. Spine 13, 532–541.

    Article  CAS  PubMed  Google Scholar 

  • Dumas, G.A., Poulin, M.J., Roy, B., Gagnon, M., Jovanovic, M., 1991. Orientation and moment arms of some trunk muscles. Spine 16, 293–303.

    Article  CAS  PubMed  Google Scholar 

  • Farfan, H.F., 1995. Form and function of the musculoskeletal system as revealed by mathematical analysis of the lumbar spine. An essay. Spine 20, 1462–1474.

    Article  CAS  PubMed  Google Scholar 

  • Fischer, M.S., 2001. Locomotory organs of mammals: new mechanics and feed-back pathways but conservative central control. Zoology 103, 230–239.

    Google Scholar 

  • Fisher, R.E., Scott, K.M., Naples, V.L., 2007. Forelimb myology of the pygmy hippopotamus (Choeropsis liberiensis). Anat. Rec. (Hoboken) 290, 673–693.

    Article  Google Scholar 

  • Gans, C., 1982. Fiber architecture and muscle function. Exercise Sport Sci. Rev. 10, 160–207.

    Article  CAS  Google Scholar 

  • Gillis, G.B., Biewener, A.A., 2001. Hindlimb muscle function in relation to speed and gait: in vivo patterns of strain and activation in a hip and knee extensor of the rat (Rattus norvegicus). J. Exp. Biol. 204, 2717–2731.

    CAS  Google Scholar 

  • Goffart, M., 1971. Function and Form in the Sloth. Pergamon Press, Oxford.

    Google Scholar 

  • Gorb, S.N., Fischer, M.S., 2000. Three-dimensional analysis of the arrangement and length distribution of fascicles in the triceps muscle of Galea musteloides (Roden-tia, Cavimorpha). Zoomorphology 120, 91–97.

    Article  Google Scholar 

  • Haas, A., Fischer, M.S., 1997. Three-dimensional reconstruction of histological sections using modern product-design software. Anat. Rec. 249, 510–516.

    Article  CAS  PubMed  Google Scholar 

  • Herrel, A., Vanhoydonck, B., Porck, J., Irschick, D.J., 2008. Anatomical basis of differences in locomotor behavior in Anolis lizards: a comparison between two ecomorphs. Bull. Mus. Comp. Zool. 159, 213–238.

    Article  Google Scholar 

  • Hesse, B., 2011. Funktionsmorphologische Anpassungen an den aufrechten Gang in der perivertebralen Lumbalmuskulatur des Menschen. In: Biologisch-Pharmazeutische Fakultät). Friedrich-Schiller-University, Jena, pp. 108.

    Google Scholar 

  • Hildebrand, M., 1977. Analysis of asymmetrical gaits. J. Mammal. 58, 131–156.

    Article  Google Scholar 

  • Humphry, G.M., 1869. The myology of the limbs of the Unau, the Ai, the two-toed anteater, and the Pangolin. J. Anat. Physiol. 3, 2–78.

    Google Scholar 

  • Kawakami, Y., Ichinose, Y., Fukunaga, T., 1998. Architectural and functional features of humantriceps surae muscles during contraction. J. Appl. Physiol. 85, 398–404.

    Article  CAS  PubMed  Google Scholar 

  • Kim, S.Y., Boynton, E.L., Ravichandiran, K., Fung, L.Y., Bleakney, R., Agur, A.M., 2007. Three-dimensional study of the musculotendinous architecture of supraspina-tus and its functional correlations. Clin. Anat. (New York, NY) 20, 648–655.

    Article  Google Scholar 

  • Lee, D., Ravichandiran, K., Jackson, K., Fiume, E., Agur, A., 2012. Robust estimation of physiological cross-sectional area and geometric reconstruction for human skeletal muscle. J. Biomech. 45, 1507–1513.

    Article  PubMed  Google Scholar 

  • Lieber, R.L., 2002. Skeletal Muscle Structure, Function, and Plasticity. Lippincott Williams & Wilkins, Baltimore, MD, USA.

    Google Scholar 

  • Lieber, R.L., Fridén, J., 2001. Clinical significance of skeletal muscle architecture. Clin. Orthop. Relat. Res. 23, 140–151.

    Article  Google Scholar 

  • Lucae, J.C.G., 1883. Die Statik und Mechanik der Quadrupeden an dem Skelet und den Muskelneines Lemur und eines Choloepus. Mahlau, Frankfurt am Main, Germany.

    Google Scholar 

  • Mackintosh, H., 1870. On the myology of the genus Bradypus. Proc. R. Ir. Acad. Sci. 1, 517–529.

    Google Scholar 

  • Mackintosh, H., 1875. On the muscular anatomy of Choloepus didactylus. Proc. R. Ir. Acad. Sci., 66–78.

  • McNeill Alexander, R., 2002. Tendon elasticity and muscle function. Comp. Biochem. Physiol., A: Mol. Integr. Physiol. 133, 1001–1011.

    Article  Google Scholar 

  • Mendel, F.C., 1985. Adaptations for suspensory behavior in the limbs of two-toed sloths. In: Montgomery, G.G. (Ed.), The Evolution and Ecology of Armadillos, Sloths, and Vermilinguas. Smithsonian Institution Press, Washington, pp. 151–162.

    Google Scholar 

  • Mendel, F.C., 1981a. Foot of two-toed sloths: its anatomy and potential uses relative to size of support. J. Morphol. 170, 357–372.

    Article  PubMed  Google Scholar 

  • Mendel, F.C., 1981b. The hand of two-toed sloths (Choloepus): its anatomy and potential uses relative to size of support. J. Morphol. 169, 1–19.

    Article  PubMed  Google Scholar 

  • Miller, R.A., 1935. Functional adaptations in the forelimb of the sloths. J. Mamm. 16, 38–51.

    Article  Google Scholar 

  • Molnar, J.L., Pierce, S.E., Hutchinson, J.R., 2014. An experimental and morphometric test of the relationship between vertebral morphology and joint stiffness in Nile crocodiles (Crocodylus niloticus). J. Exp. Biol. 217, 758–768.

    Article  Google Scholar 

  • Moon, B.R., Gans, C., 1998. Kinematics, muscular activity and propulsion in gopher snakes. J. Exp. Biol. 201, 2669–2684.

    PubMed  Google Scholar 

  • Norris, CM., 1995. Spinal stabilisation. 3. Stabilisation mechanisms of the lumbar spine. Physiotherapy 81, 72–79.

    Google Scholar 

  • Nyakatura, J.A., 2012. The convergent evolution of suspensory posture and locomotion in tree sloths. J. Mamm. Evol. 19, 225–234.

    Article  Google Scholar 

  • Nyakatura, J.A., Andrada, E., 2013. A mechanical link model of two-toed sloths: no pendular mechanics during suspensory locomotion. Acta Theriol. 58, 83–93.

    Article  Google Scholar 

  • Nyakatura, J.A., Fischer, M.S., 2010a. Functional morphology and three-dimensional kinematics of the thoraco-lumbar region of the spine of the two-toed sloth. J. Exp. Biol. 213, 4278–4290.

    Article  PubMed  Google Scholar 

  • Nyakatura, J.A., Fischer, M.S., 2010b. Three-dimensional kinematic analysis of the pectoral girdle during upside-down locomotion of two-toed sloths (Choloepus didactylus, Linne 1758). Front. Zool. 7, 21.

    Article  PubMed  PubMed Central  Google Scholar 

  • Nyakatura, J.A., Fischer, M.S., 2011. Functional morphology of the muscular sling at the pectoral girdle in tree sloths: convergent morphological solutions to new functional demands? J. Anat. 219, 360–374.

    Article  PubMed  PubMed Central  Google Scholar 

  • Nyakatura, J.A., Petrovitch, A., Fischer, M.S., 2010. Limb kinematics during locomotion in the two-toed sloth (Choloepus didactylus, Xenarthra) and its implications for the evolution of the sloth locomotor apparatus. Zoology (Jena) 113, 221–234.

    Article  Google Scholar 

  • Panjabi, M.M., Oxland, T.R., Yamamoto, I., Crisco, J.J., 1994. Mechanical behavior of the human lumbar and lumbosacral spine as shown by three-dimensional load-displacement curves. J. Bone Joint Surg. Am. Vol. 76, 413–424.

    Article  CAS  Google Scholar 

  • Poelstra, K.A., Eijkelkamp, M.F., Veldhuizen, A.G., 2000. The geometry of the human paraspinal muscles with the aid of three-dimensional computed tomography scans and 3-Space Isotrak. Spine 25, 2176–2179.

    Article  CAS  PubMed  Google Scholar 

  • Ritter, D.A., 1995. Epaxial muscle function during locomotion in a lizard (Varanus salvator) and the proposal of a key innovation in the vertebrate axial musculoskeletal system. J. Exp. Biol. 198, 2477–2490.

    CAS  PubMed  Google Scholar 

  • Ritter, DA, 1996. Axial muscle function during lizard locomotion. J. Exp. Biol. 199, 2499–2510.

    CAS  PubMed  Google Scholar 

  • Roberts, T.J., 1997. Muscular force in running Turkeys: the economy of minimizing work. Science 275, 1113–1115.

    Article  CAS  PubMed  Google Scholar 

  • Roberts, T.J., 2002. The integrated function of muscles and tendons during locomotion. Comp. Biochem. Physiol., A: Mol. Integr. Physiol. 133, 1087–1099.

    Article  Google Scholar 

  • Roberts, T.J., Azizi, E., 2011. Flexible mechanisms: the diverse roles of biological springs in vertebrate movement.J. Exp. Biol. 214, 353–361.

    Article  Google Scholar 

  • Rome, L.C., Funke, R.P., Alexander, R.M., Lutz, G., Aldridge, H., Scott, F., Freadman, M., 1988. Why animals have different muscle fibre types. Nature 335, 824–827.

    Article  CAS  PubMed  Google Scholar 

  • Rosatelli, A.L., Ravichandiran, K., Agur, A.M., 2008. Three-dimensional study of the musculotendinous architecture of lumbar multifidus and its functional implications. Clin. Anat. (New York, NY) 21, 539–546.

    Article  Google Scholar 

  • Schilling, N., 2009. Metabolic profile of the perivertebral muscles in small therian mammals: implications for the evolution of the mammalian trunk musculature. Zoology 112, 279–304.

    Article  CAS  PubMed  Google Scholar 

  • Schilling, N., 2011. Evolution of the axial system incraniates: morphology and function of the perivertebral musculature. Front. Zool. 8, 4.

    Article  PubMed  PubMed Central  Google Scholar 

  • Schilling, N., Carrier, D.R., 2010. Function of the epaxial muscles in walking, trotting and galloping dogs: implications for the evolution of epaxial muscle function in tetrapods.J. Exp. Biol. 213, 1490–1502.

    Article  Google Scholar 

  • Schilling, N., Hackert, R., 2006. Sagittal spine movements of small therian mammals during asymmetrical gaits. J. Exp. Biol. 209, 3925–3939.

    Article  PubMed  Google Scholar 

  • Scholle, H.C., Schumann, N.P., Biedermann, F., Stegeman, D.F., Graßme, R., Roeleveld, K., Schilling, N., Fischer, M.S., 2001. Spatiotemporal surface EMG characteristics from rat triceps brachii muscle during treadmill locomotion indicate selective recruitment of functionally distinct muscle regions. Exp. Br. Res. 138, 26–36.

    Article  CAS  Google Scholar 

  • Slijper, E.J., 1942. Biologic-anatomical investigations on the bipedal gait and upright posture in mammals, with special reference to a little goat, born without forelegs. Proc. K. Ned. Akad. Wet. 45, 288–295.

    Google Scholar 

  • Slijper, E.J., 1946. Comaprative biologic-anatomical investigation on the vertebral column and spinal musculature of mammals. Verh. K. Ned. Akad. Wet. Tweede Sectie 42, 1–128.

    Google Scholar 

  • Stark, H., Fröber, R., Schilling, N., 2013. Intramuscular architecture of the autochthonous back muscles in humans. J. Anat. 222, 214–222.

    Article  PubMed  Google Scholar 

  • Stark, H., Schilling, N., 2010. A novel method of studying fascicle architecture in relaxed and contracted muscles. J. Biomech. 43, 2897–2903.

    Article  PubMed  Google Scholar 

  • van Eijden, T.M., Koolstra, J.H., Brugman, P., 1996. Three-dimensional structure of the human temporalis muscle. Anat. Rec. 246, 565–572.

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Systematic Zoology and Evolutionary Biology, Friedrich-Schiller-University, Erbertstraße 1, 07737, Jena, Germany

    John A. Nyakatura & Heiko Stark

  2. Image Knowledge Gestaltung: An Interdisciplinary Laboratory and Institute of Biology, Humboldt University, Philippstraße 13, 10115, Berlin, Germany

    John A. Nyakatura

  3. Department of Bioinformatics, Friedrich-Schiller-University, Ernst-Abbe-Platz 2, 07737, Jena, Germany

    Heiko Stark

Authors
  1. John A. Nyakatura
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Heiko Stark
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to John A. Nyakatura.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nyakatura, J.A., Stark, H. Aberrant back muscle function correlates with intramuscular architecture of dorsovertebral muscles in two-toed sloths. Mamm Biol 80, 114–121 (2015). https://doi.org/10.1016/j.mambio.2015.01.002

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1016/j.mambio.2015.01.002

Keywords

Search

Navigation