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Kinematic scaling of locomotion by hydrostatic animals: ontogeny of peristaltic crawling by the earthworm lumbricus terrestris
K.J. Quillin
Journal of Experimental Biology 1999 202: 661-674;

Summary

This study examined the relationship between ontogenetic increase in body size and the kinematics of peristaltic locomotion by the earthworm Lumbricus terrestris, a soft-bodied organism supported by a hydrostatic skeleton. Whereas the motions of most vertebrates and arthropods are based primarily on the changes in the joint angles between rigid body segments, the motions of soft-bodied organisms with hydrostatic skeletons are based primarily on the changes in dimensions of the deformable body segments themselves. The overall kinematics of peristaltic crawling and the dynamic shape changes of individual earthworm segments were measured for individuals ranging in body mass (mb) by almost three orders of magnitude (0.012-8.5 g). Preferred crawling speed varied both within and among individuals: earthworms crawled faster primarily by taking longer strides, but also by taking more strides per unit time and by decreasing duty factor. On average, larger worms crawled at a greater absolute speed than smaller worms (U p2finity mb0.33) and did so by taking slightly longer strides (l p2finity mb0.41, where l is stride length) than expected by geometric similarity, using slightly lower stride frequencies (f p2finity mb-0.07) and the same duty factor (df p2finity mb-0.03). Circumferential and longitudinal body wall strains were generally independent of body mass, while strain rates changed little as a function of body mass. Given the extent of kinematic variation within and among earthworms, the crawling of earthworms of different sizes can be considered to show kinematic similarity when the kinematic variables are normalized by body length. Since the motions of peristaltic organisms are based primarily on changes in the dimensions of the deformable body wall, the scaling of the material properties of the body wall is probably an especially important determinant of the scaling of the kinematics of locomotion.

REFERENCES

    1. Bennett, A. F.,
    2. Garland, T. and
    3. Else, P. L.
    (1989). Individual correlation of morphology, muscle mechanics and locomotion in a salamander. Am. J. Physiol 256, 1200–.
    OpenUrl
    1. Berrigan, D. and
    2. Lighton, J. R. B.
    (1993). Bioenergetic and kinematic consequences of limblessness in larval Diptera. J. Exp. Biol 179, 245–.
    OpenUrlAbstract
    1. Brackenbury, J.
    (1997). Caterpillar kinematics. Nature 390, 453–.
    OpenUrlCrossRef
    1. Burr, A. H. J. and
    2. Gans, C.
    (1988). Mechanical significance of obliquely striated architecture in nematode muscle. Biol. Bull 194, 1–.
    OpenUrlAbstract/FREE Full Text
    1. Casey, T. M.
    (1991). Energetics of caterpillar locomotion: Biomechanical constraints of a hydraulic skeleton. Science 252, 112–.
    OpenUrlAbstract/FREE Full Text
    1. Chapman, G.
    (1950). On the movement of worms. J. Exp. Biol 27, 29–.
    OpenUrlAbstract
    1. Chapman, G.
    (1958). The hydrostatic skeleton in the invertebrates. Biol. Rev 33, 338–.
    OpenUrlCrossRef
    1. Clark, R. B. and
    2. Cowey, J. B.
    (1958). Factors controlling the change of shape of certain nemertean and turbellarian worms. J. Exp. Biol 35, 731–.
    OpenUrlAbstract
    1. Delcomyn, F.
    (1980). Neural basis of rhythmic behavior in animals. Science 210, 492–.
    OpenUrlAbstract/FREE Full Text
    1. Drucker, E. G. and
    2. Jensen, J. S.
    (1996). Pectoral fin locomotion in the striped surfperch. II. Scaling swimming kinematics and performance at a gait transition. J. Exp. Biol 199, 2243–.
    OpenUrlAbstract/FREE Full Text
    1. Gray, J. and
    2. Lissmann, H. W.
    (1938). Studies in locomotion. VII. Locomotory reflexes in the earthworm. J. Exp. Biol 15, 506–.
    OpenUrlAbstract
    1. Heffernan, J. M. and
    2. Wainwright, S. A.
    (1974). Locomotion of the holothurian Euapta lappa and redefinition of peristalsis. Biol. Bull 147, 95–.
    OpenUrlAbstract/FREE Full Text
    1. Heglund, N. C. and
    2. Taylor, C. R.
    (1988). Speed, stride frequency and energy cost per stride: how do they change with body size and gait?. J. Exp. Biol 138, 301–.
    OpenUrlAbstract/FREE Full Text
    1. Heglund, N. C.,
    2. Taylor, C. R. and
    3. McMahon, T. A.
    (1974). Scaling stride frequency and gait to animal size: mice to horses. Science 186, 1112–.
    OpenUrlAbstract/FREE Full Text
    1. Hidaka, T.,
    2. Kuriyama, H. and
    3. Yamamoto, T.
    (1969). The mechanical properties of the longitudinal muscle in the earthworm. J. Exp. Biol 50, 431–.
    OpenUrlAbstract/FREE Full Text
    1. Hill, A. V.
    (1950). The dimensions of animals and their muscular dynamics. Sci. Prog 38, 209–.
    OpenUrl
    1. Huey, R. B. and
    2. Hertz, P. E.
    (1982). Effects of body size and slope on sprint speed of a lizard (Stellio (Agama) stellio). J. Exp. Biol 97, 401–.
    OpenUrlAbstract/FREE Full Text
    1. Keller, J. B. and
    2. Falkovitz, M. S.
    (1983). Crawling of worms. J. Theor. Biol 104, 417–.
    OpenUrlCrossRef
    1. Kram, R. and
    2. Taylor, C. R.
    (1990). Energetics of running: A new perspective. Nature 346, 265–.
    OpenUrlCrossRefPubMedWeb of Science
    1. Lissmann, H. W.
    (1945). The mechanism of locomotion in gastropod molluscs. I. Kinematics. J. Exp. Biol 21, 58–.
    OpenUrlWeb of Science
    1. Maitland, D. P.
    (1992). Locomotion by jumping in the Mediterranean fruit-fly larva Ceratitis capitata. Nature 355, 159–.
    OpenUrlCrossRef
    1. Marsh, R. L.
    (1988). Ontogenesis of contractile properties of skeletal muscle and sprint performance in the lizard Dipsosaurus dorsalis. J. Exp. Biol 137, 119–.
    OpenUrlAbstract/FREE Full Text
    1. McMahon, T.
    (1973). Size and shape in biology. Science 179, 1201–.
    OpenUrlAbstract/FREE Full Text
    1. McMahon, T. A.
    (1975). Using body size to understand the structural design of animals: Quadrupedal locomotion. J. Appl. Physiol 39, 619–.
    OpenUrlAbstract/FREE Full Text
    1. Miller, J. B.
    (1975). The length—tension relationship of the dorsal longitudinal muscle of the leech. J. Exp. Biol 62, 43–.
    OpenUrlAbstract/FREE Full Text
    1. Milligan, B. J.,
    2. Curtin, N. A. and
    3. Bone, Q.
    (1997). Contractile properties of obliquely striated muscle from the mantle of squid (Alloteuthis subulata) and cuttlefish (Sepia officinalis). J. Exp. Biol 200, 2425–.
    OpenUrlAbstract
    1. Newell, G. E.
    (1950). The role of the coelomic fluid in the movements of earthworms. J. Exp. Biol 27, 110–.
    OpenUrlAbstract
    1. Pennycuick, C. J.
    (1975). On the running of the gnu and other animals. J. Exp. Biol 63, 775–.
    OpenUrlAbstract/FREE Full Text
    1. Queathem, E.
    (1991). The ontogeny of grasshopper jumping performance. J. Insect Physiol 37, 129–.
    OpenUrlCrossRef
    1. Quillin, K. J.
    (1998). Ontogenetic scaling of hydrostatic skeletons: geometric, static stress and dynamic stress scaling of the earthworm Lumbricus terrestris. J. Exp. Biol 201, 1871–.
    OpenUrlAbstract/FREE Full Text
    1. Richard, B. A. and
    2. Wainwright, P. C.
    (1995). Scaling of the feeding mechanism of largemouth bass (Mictropterus salmoides). I. Kinematics of prey capture. J. Exp. Biol 198, 419–.
    OpenUrlAbstract/FREE Full Text
    1. Rome, L. C.
    (1992). Scaling of muscle fibres and locomotion. J. Exp. Biol 168, 243–.
    OpenUrlAbstract/FREE Full Text
    1. Rubin, C. T. and
    2. Lanyon, L. E.
    (1984). Dynamic strain similarity in vertebrates; an alternative to allometric limb bone scaling. J. Theor. Biol 107, 321–.
    OpenUrlPubMedWeb of Science
    1. Tashiro, N.
    (1971). Mechanical properties of the longitudinal and circular muscle in the earthworm. J. Exp. Biol 54, 101–.
    OpenUrl
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Journal Articles
Kinematic scaling of locomotion by hydrostatic animals: ontogeny of peristaltic crawling by the earthworm lumbricus terrestris
K.J. Quillin
Journal of Experimental Biology 1999 202: 661-674;
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