Abstract
The non-linear viscoelasticity of tendons and ligaments, for which much of their mechanical behavior reflects the properties of their collagen I fibrils, is well suited to absorbing and returning energy associated with the transmission of tensile forces across joints of the body. The high resilience of tendon means that it can serve as an effective biological spring. At the same time, the flexibility of tendons and ligaments allows them to accommodate a wide range of joint movement (or, in the case of ligaments, to restrict movement within a certain range). The high strength of tendons and ligaments also provides considerable weight savings, but this is traded off against the ability to control position and movements of the musculoskeletal system. Tendon and ligament compliance allows elastic energy to be stored and returned to offset energy fluctuations of the body’s center of mass during locomotion, conserving muscle work and reducing the metabolic energy cost of locomotor movement. Tendon architecture greatly affects the storage and recovery of elastic strain energy, with long, thin tendons favoring greater strain energy/volume (and weight) of the tendon. It is likely that other elastic elements, such as muscle aponeuroses, also contribute significant energy savings. Tendon compliance may also reduce the cost of muscle contraction, by reducing a muscle’s contractile velocity and length change for a given movement, as well as increasing the power output of muscle–tendon units that is key to rapid acceleration and jumping performance. This power enhancement requires a temporal decoupling of muscle work to stretch the tendon from the subsequent more rapid release of elastic strain energy from the tendon. This decoupling may be achieved by changes in inertia and mechanical advantage in vertebrates, but is facilitated by catch mechanisms in invertebrate jumpers. Although it is critical that tendons and ligaments have sufficient strength and an adequate safety factor to limit the risk of failure, tendons are likely subject to damage during their use, which favors a greater safety factor. In addition, because tendon compliance impedes position control, the thickness of many tendons suggests that having sufficient stiffness, rather than strength, is a key structural requirement. Indeed, the majority of tendons that have been studied to date appear to operate at lower stresses and strains, have larger safety factors, and are stiffer, compared with “high-stress” tendons of animals specialized for elastic energy savings.
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Reference
Aerts, P. (1998). Vertical jumping in Galago senegalensis: the quest for an obligate power amplifier. Philos. Trans. R. Soc. Lond. B 353, 1607–1620.
Alexander, R. M. (1983). Animal Mechanics, 2nd ed. London: Blackwell Scientific.
Alexander, R. M. (1988). Elastic Mechanisms in Animal Movement. Cambridge: Cambridge University Press.
Alexander, R. M. (1995). Leg design and jumping technique for humans, other vertebrates and insects. Philos. Trans. R. Soc. Lond. B 347, 235–248.
Alexander, R. M. (2002). Tendon elasticity and muscle function. Comp. Biochem. Physiol. A 133, 1001–1011.
Alexander, R. M. and Dimery, N. J. (1985). Elastic properties of the forefoot of the donkey (Equus asinus). J. Zool. Lond. 205, 511–524.
Alexander, R. M. and Vernon, A. (1975). The mechanics of hopping by kangaroos (Macropodidae). J. Zool. Lond. 177, 265–303.
Baudinette, R. V. and Biewener, A. A. (1998). Young wallabies get a free ride. Nature 395, 653–654.
Benjamin, M. and Ralphs, J. R. (1997). Tendons and ligaments—an overview. Histol. Histopathol. 12, 1135–1144.
Bennet-Clark, H. C. (1975). The energetics of the jump of the locust, Schistocerca gregaria. J. Exp. Biol. 63, 53–83.
Bennett, M. B., Ker, R. F., Dimery, N. J. and Alexander, R. M. (1986). Mechanical properties of various mammalian tendons. J. Zool. Lond. 209, 537–548.
Biewener, A. A. (1998). Muscle-tendon stresses and elastic energy storage during locomotion in the horse. Comp. Biochem. Physiol. B 120, 73–87.
Biewener, A. A. (2003). Animal Locomotion. Oxford: Oxford University Press.
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). J. Exp. Biol. 198, 1829–1841.
Biewener, A. A. and Bertram, J. E. A. (1990). Design and optimization in skeletal support systems. In Concepts of Efficiency in Biological Systems., vol. (in press) (ed. R. W. Blake), pp. xx. Cambridge: Cambridge University Press.
Biewener, A. A. and Blickhan, R. (1988). Kangaroo rat locomotion: design for elastic energy storage or acceleration? J. Exp. Biol. 140, 243–255.
Biewener, A. A. and Corning, W. R. (2001). Dynamics of mallard (Anas platyrynchos) gastrocnemius function during swimming versus terrestrial gait. J. Exp. Biol. 204, 1745–1756.
Biewener, A. A. and Roberts, T. J. (2000). Muscle and tendon contributions to force, work, and elastic energy savings: a comparative perspective. Exerc. Sport Sci. Rev. 28, 99–107.
Cavagna, G. A., Heglund, N. C. and Taylor, C. R. (1977). Mechanical work in terrestrial locomotion: two basic mechanisms for minimizing energy expenditures. Am. J. Physiol. 233, R243–261.
Daley, M. A. and Biewener, A. A. (2003). Muscle force-length dynamics during level versus incline locomotion: a comparison of in vivo performance of two guinea fowl ankle extensors. J. Exp. Biol. 206, 2941–2958.
Daley, M. A. and Biewener, A. A. (2006). Running over rough terrain reveals limb control for intrinsic stability. PNAS 103, 15681–15686.
Fenn, W. O. (1924). The relation between the work performed and the energy liberated in muscular contraction. J. Physiol. 58:373–395.
Fratzl, P., Misof, K., Zizak, I., Rapp, G., Amenitsch, H. and Bernstorff, S. (1998). Fibrillar structure and mechanical properties of collagen. J. Struct. Biol. 122, 119–122.
Fukunaga, T., Kubo, K., Kawakami, Y., Fukashiro, S., Kanehisa, H. and Maganaris, C. N. (2001). In vivo behavior of human muscle tendon during walking. Proc. R. Soc. Lond. B 268, 229–233.
Hill, A. V. (1938). The heat of shortening and the dynamic constants of muscle. Proc. R. Soc. Lond. B 126, 136–195.
Kawakami, Y., Muraoka, T., Ito, S., Kanehisa, H. and Fukunaga, T. (2002). In vivo muscle fibre behaviour during counter-movement exercise in humans reveals a significant role for tendon elasticity. J. Physiol. 540, 635–646.
Ker, R. F., Bennett, M. B., Bibby, S. R., Kester, R. C. and Alexander, R. M. (1987). The spring in the arch of the human foot. Nature 325, 147–149.
Ker, R. F., Alexander, R. M. and Bennett, M. B. (1988). Why are mammalian tendons so thick? J. Zool. Lond. 216, 309–324.
Ker, R. F., Wang, X. T. and Pike, A. V. L. (2000). Fatigue quality of mammalian tendons. J. Exp. Biol. 203, 1317–1327.
Lichtwark, G. A., Bougoulias, K. and Wilson, A. M. (2007). Muscle fascicle and series elastic element length changes along the length of the human gastrocnemius during walking and running. J. Biomech. 40, 157–164.
Lieber, R. L. (1992). Skeletal Muscle Structure and Function. Baltimore: Williams and Wilkins.
Lieber, R. L., Leonard, M. E. and Brown-Maupin, C. G. (2000). Effects of muscle contraction on the load-strain properties of frog aponeurosis and tendon. . Cells Tissues Organs 166, 48–54.
Loren, G. J. and Lieber, R. L. (1995). Tendon biomechanical properties enhance human wrist muscle specialization. J. Biomech. 28, 791–799.
Maganaris, C. N. and Paul, J. P. (2002). Tensile properties of the in vivo human gastrocnemius tendon. J. Biomech. 35, 1639–1646.
Magnusson, S. P., Hansen, P., Aagaard, P., Brond, J., Dyhre-Poulsen, P., Bojsen-Moller, J. and Kjær, M. (2003). Differential strain patterns of the human gastrocnemius aponeurosis and free tendon, in vivo. Acta. Physiol. Scand. 177, 185–195.
McGowan, C. P., Baudinette, R. V. and Biewener, A. A. (2008). Differential design for hopping in two species of wallabies. Comp. Biochem. Physiol. in press.
McGuigan, M. P., Yoo, E. and Biewener, A. A. (2007). In vivo dynamics of distal limb muscle function during level versus graded locomotion in goats. J. Appl. Physiol. unpublished.
Peplowski, M. M. and Marsh, R. L. (1997). Work and power output in the hindlimb muscles of Cuban tree frogs Osteopilus septentrionalis during jumping. J. Exp. Biol. 200, 2861–2870.
Pollock, C. M. and Shadwick, R. E. (1994). Relationship between body mass and biomechanical properties of limb tendons in adult mammals. Am. J. Physiol. 266, R1016–1021.
Provenzano, P., Lakes, R., Keenan, T. and Vanderby Jr., R. (2001). Nonlinear ligament viscoelasticity. Ann. Biomed. Eng. 29, 908–914.
Rack, P. M. H. and Ross, H. F. (1984). The tendon of flexor pollicis longus; its effects on the muscular control of force and position in the human thumb. J. Physiol. Lond. 351, 99–110.
Richards, C. T. and Biewener, A. A. (2007). Modulation of in vivo muscle power output during swimming in the African clawed frog (Xenopus laevis). J. Exp. Biol. 210, 3147–3159.
Roberts, T. J. (2002). The integrated function of muscles and tendons during locomotion. Comp. Biochem. Physiol. A 133, 1087–1099.
Roberts, T. J. and Marsh, R. L. (2003). Probing the limits to muscle-powered accelerations: lessons from jumping bullfrogs. J. Exp. Biol. 206, 2567–2580.
Roberts, T. J. and Scales, J. A. (2002). Mechanical power ouput during running accelerations in wild turkeys. J. Exp. Biol. 205, 1485–1494.
Rumian, A. P., Wallace, A. L. and Birch, H. L. (2007). Tendons and ligaments are anatomically distinct but overlap in molecular and morphological features–a comparative study in an ovine model. J. Orthop. Res. 25, 458–464.
Schechtman, H. and Bader, D. L. (1997). In vitro fatigue of human tendons. J. Biomech. 30, 829–835.
Shadwick, R. E. (1990). Elastic energy storage in tendons: mechanical differences related to function and age. J. Appl. Physiol. 68, 1033–1040.
Wilson, A. M., McGuigan, M. P. Su, A. and van den Bogert, A. J. (2001). Horses damp the spring in their step. Nature 414, 895–899.
Woo, S. L.-Y. (1982). Mechanical properties of tendons and ligaments. I. Quasistatic and nonlinear viscoelastic properties. Biorheology 19, 385–396.
Woo, S. L.-Y., Abramowitch, S. D., Kilger, R. Land Liang, R. (2006). Biomechanics of knee ligaments: injury, healing, and repair. J. Biomech. 39, 1–20.
Wren, T. A., Yerby, S. A., Beaupre, G. S. and Carter, D. R. (2001). Mechanical properties of the human Achilles tendon. Clin. Biomech. 16, 245–251.
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Biewener, A. (2008). Tendons and Ligaments: Structure, Mechanical Behavior and Biological Function. In: Fratzl, P. (eds) Collagen. Springer, Boston, MA. https://doi.org/10.1007/978-0-387-73906-9_10
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DOI: https://doi.org/10.1007/978-0-387-73906-9_10
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