The gaits of primates: Center of mass mechanics in walking, cantering and galloping ring-tailed lemurs, Lemur catta

Journal of Experimental Biology

Volumn 215, Issue 10, 2012, Pages 1728-1739

  O'Neill, Matthew C ^a   Schmitt, Daniel ^b  

^a STONY BROOK UNIVERSITY   (United States)

^b DUKE UNIVERSITY   (United States)

Author keywords

Center of mass; Collision; Gait; Lemur; Lemur catta; Locomotion; Mechanical work; Quadruped

Indexed keywords

ALGORITHM; ANIMAL; ANIMAL BEHAVIOR; ARTICLE; BIOMECHANICS; FEMALE; GAIT; GRAVITY; KINETICS; LEMURIDAE; MALE; MOVEMENT (PHYSIOLOGY); PHYSIOLOGY; PRIMATE; RUNNING; STATISTICAL MODEL; WALKING;

ALGORITHMS; ANIMALS; BEHAVIOR, ANIMAL; BIOMECHANICS; FEMALE; GAIT; GRAVITATION; KINETICS; LEMUR; MALE; MODELS, STATISTICAL; MOVEMENT; PRIMATES; RUNNING; WALKING;

ANIMALIA; LEMUR; LEMUR CATTA; LEMURIDAE; PRIMATES;

EID: 84861119819     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.052340     Document Type: Article

References (87)

1. Adamczyk, P. G. and Kuo, A. D. (2009). Redirection of center-of-mass velocity during the step-to-step transition of human walking. J. Exp. Biol. 212, 2668-2678.
2. Adamczyk, P. G., Collins, S. H. and Kuo, A. D. (2006). The advantages of a rolling foot in human walking. J. Exp. Biol. 209, 3953-3963. (Pubitemid 44769364)
3. Aerts, P. (1998). Vertical jumping in Galago senegalensis: Quest for an obligate mechanical power amplifer. Philos. Trans. R. Soc. Lond. B 353, 1607-1620. (Pubitemid 28490552)
4. Ahn, A. N., Furrow, E. and Biewener, A. A. (2004). Walking and running in the redlegged running frog, Kassina maculata. J. Exp. Biol. 207, 399-410. (Pubitemid 38162375)
5. Alexander, R. M. (1977). Terrestrial locomotion. In Mechanics and Energetics of Terrestrial Locomotion (ed. R. M. Alexander and G. Goldspink), pp. 106-203. New York: John Wiley & Sons, Inc.
6. Alexander, R. M. (1988). Elastic Mechanisms in Animal Movement. Cambridge: Cambridge University Press.
7. Alexander, R. M. (1989). Optimization and gaits in the locomotion of vertebrates. Physiol. Rev. 69, 1199-1227.
8. Alexander, R. M. and Jayes, A. S. (1980). Fourier analysis of forces exerted in walking and running. J. Biomech. 13, 383-390.
9. Alexander, R. M. and Jayes, A. S. (1983). The dynamic similarity hypothesis for the gaits of quadrupedal mammals. J. Zool. 201, 135-152.
10. Azizi, E., Halenda, G. M. and Roberts, T. J. (2009). Mechanical properties of the gastrocnemius aponeurosis in wild turkeys. Integr. Comp. Biol. 49, 51-58.
11. Bennett, M. B., Ker, R. F., Dimery, N. J. and Alexander, R. M. (1986). Mechanical properties of various mammalian tendons. J. Zool. 209, 537-548.
12. Bertram, J. E. A. and Gutmann, A. (2009). Motions of the running horse and cheetah revisited: Fundamental mechanics of the transverse and rotary gallop. J. R. Soc. Interface 6, 549-559.
13. Biknevicius, A. R. and Reilly, S. M. (2006). Correlation of symmetrical gaits and whole body mechanics: Debunking myths in locomotor biodynamics. J. Exp. Zool. 305A, 923-934. (Pubitemid 44744425)
14. Bishop, K. L., Pai, A. K. and Schmitt, D. L. (2008). Whole body mechanics of stealthy walking in cats. PLoS ONE 3, e3808.
15. Blickhan, R. (1989). The spring-mass model for running and hopping. J. Biomech. 22, 1217-1227. (Pubitemid 20097590)
16. Bobbert, M. F., Gómez Álvarez, C. B., van Weeren, P. R., Roepstorff, L. and Weishaupt, M. A. (2007). Validation of vertical ground reaction forces on individual limbs calculated form kinematics and horse locomotion. J. Exp. Biol. 210, 1885-1896. (Pubitemid 46998734)
17. Cartmill, M., Lemelin, P. and Schmitt, D. (2002). Support polygons and symmetrical gaits in mammals. Zool. J. Linn. Soc. Lond. 136, 401-420. (Pubitemid 35259154)
18. Cavagna, G. A. (1975). Fore platforms as ergometers. J. Appl. Physiol. 39, 174-179.
19. Cavagna, G. A., Thys, H. and Zamboni, A. (1976). The sources of external work in level walking and running. J. Physiol. 262, 639-657.
20. Cavagna, G. A., Heglund, N. C. and Taylor, C. R. (1977). Mechanical work in terrestrial locomotion: Two basic mechanisms for minimizing energy expenditure. Am. J. Physiol. Regul. Integr. Comp. Physiol. 233, R243-R261. (Pubitemid 8240886)
21. Demes, B., Jungers, W. L. and Nieschalk, U. (1990). Size-and speed-related aspects of quadrupedal walking in slender lorises. In Gravity, Posture and Locomotion in Primates (ed. F. K. Jouffroy, M. H. Stack, and C. Niemitz), pp. 175-198. Florence: Il Sedicesimo.
22. Demes, B., Larson, S. G., Stern, J. T., Jr, Jungers, W. L., Biknevicus, A. R. and Schmitt, D. (1994). The kinetics of primate quadrupedalism: "hindlimb drive" reconsidered. J. Hum. Evol. 26, 353-374. (Pubitemid 124013677)
23. Donelan, J. M., Kram, R. and Kuo, A. D. (2002). Simultaneous positive and negative external mechanical work in human walking. J. Biomech. 35, 117-124. (Pubitemid 34017357)
24. Farley, C. T., Glasheen, J. and McMahon, T. A. (1993). Running springs: Speed and animal size. J. Exp. Biol. 185, 71-86.
25. Franz, T. M., Demes, B. and Carlson, K. J. (2005). Gait mechanics of lemurid primates on terrestrial and arboreal substrates. J. Hum. Evol. 48, 199-217. (Pubitemid 40205314)
26. Full, R. J. (1989). Mechanics and energetics of terrestrial locomotion: From bipeds to polypeds. In Energy Transformation in Cells and Animals (ed. W. Wieser and E. Gnaiger), pp. 175-182. Stuttgart: Georg Thieme Verlag.
27. Gebo, D. L. (1987). Locomotor diversity in prosimian primates. Am. J. Primatol. 13, 271-281.
28. Gein, J. J., Willems, P. A., Cavagna, C. A., Lair, R. and Heglund, N. C. (2010). Biomechanics of locomotion in Asian elephants. J. Exp. Biol. 213, 694-706.
29. Geyer, H., Seyfarth, A. and Blickhan, R. (2006). Compliant leg behaviour explains basic dynamics of walking and running. Proc. R. Soc. Lond. B 273, 2861-2867. (Pubitemid 44764371)
30. Griffin, T. M., Main, R. P. and Farley, C. T. (2004a). Biomechanics of quadrupedal walking: How do four-legged animals achieve inverted pendulum-like movements? J. Exp. Biol. 207, 3545-3558. (Pubitemid 39384810)
31. Griffin, T. M., Kram, R., Wickler, S. J. and Hoyt, D. F. (2004b). Biomechanical and energetic determinates of the walk-trot transition in horses. J. Exp. Biol. 207, 4215-4223. (Pubitemid 40099372)
32. Hanna, J. B., Polk, J. D. and Schmitt, D. (2006). Forelimb and hindlimb forces in walking and galloping primates. Am. J. Phys. Anthropol. 130, 529-535. (Pubitemid 44099971)
33. Hedrick, T. L. (2008). Software techniques for two-and three-dimensional kinematic measurements of biological and biomimetic systems. Bioinsp. Biomim. 3, 1-6.
34. Heglund, N. C. and 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, 301-318.
35. Heglund, N. C., Cavagna, G. A. and Taylor, C. R. (1982). Energetics and mechanics of terrestrial locomotion: III. Energy change as a function of speed and body size in birds and mammals. J. Exp. Biol. 97, 41-56.
36. Herr, H. M., Huang, G. T. and McMahon, T. A. (2002). A model of scale effects in mammalian quadrupedal running. J. Exp. Biol. 205, 959-967. (Pubitemid 34861232)
37. Hildebrand, M. H. (1967). Symmetrical gaits of primates. Am. J. Phys. Anthropol. 26, 119-130.
38. Howell, A. B. (1944). Speed in Animals. Chicago, IL: University of Chicago Press.
39. Hutchinson, J. R., Famini, D., Lair, R. and Kram, R. (2003). Are fast-moving elephants really running? Nature. 422, 493-494. (Pubitemid 36433637)
40. Jayes, A. S. and Alexander, R. M. (1978). Mechanics of locomotion of dogs (Canis familiaris) and sheep (Ovis aries). J. Zool. 185, 289-308.
41. Kimura, T., Okada, M. and Ishida, H. (1979). Kinesiological characteristics of primate walking: Its significance in nonhuman walking. In Environment, Behavior and Morphology: Dynamic Interactions in Primates (ed. M. Morbeck, H. Presuchoft and N. Gromberg), pp. 297-311. New York: G. Fischer.
42. Larson, S. G. (1998). Unique aspects of quadrupedal locomotion in nonhuman primates. In Primate Locomotion: Recent Advances (ed. E. Strasser, J. Fleagle, A. Rosenberger and H. McHenry), pp. 157-173. New York: Plenum Press.
43. Larson, S. G. and Stern, J. T., Jr (2008). Humeral rectractor EMG during quadrupedal walking in primates. J. Exp. Biol. 210, 1204-1215. (Pubitemid 46731929)
44. Lee, D. V., Bertram, J. E. A. and Todhunter, R. J. (1999). Acceleration and balance in trotting dogs. J. Exp. Biol. 202, 3565-3573. (Pubitemid 30044675)
45. Lee, D. V., Stakebake, E. F., Walter, R. M. and Carrier, D. R. (2004). Effects of mass distribution on the mechanics of level trotting in dogs. J. Exp. Biol. 207, 1715-1728. (Pubitemid 38630501)
46. Lee, D. V., Bertramn, J. E. A., Anttonen, J. T., Ros, I. G., Harris, S. L. and Biewener, A. A. (2011). A collisional perspective on quadrupedal gait dynamics. J. R. Soc. Interface 8, 1480-1486.
47. Lemelin, P. and Schmitt, D. (2006). Origins of grasping and locomotor adaptations in primates: Comparative and experimental approaches using an opossum model. In Primate Origins: Adaptations and Evolution (ed. M. J. Ravosa and M. Dagosto), pp. 329-380. New York: Kluwer Academic Publishers.
48. Lutz, G. J. and Rome, L. C. (1994). Built for jumping: The design of the frog muscular system. Science. 263, 370-372. (Pubitemid 24067940)
49. Margaria, R. (1976). Biomechanics and Energetics of Exercise. Oxford: Oxford University Press.
50. McMahon, T. A. (1985). The role of compliance in mammalian running gaits. J. Exp. Biol. 115, 263-282. (Pubitemid 15068831)
51. McMahon, T. A. and Cheng, G. C. (1990). The mechanics of running: How does stiffness couple with speed? J. Biomech. 23, 65-78.
52. Merkens, H. W., Schamhardt, H. C., van Osch, G. J. V. M. and Hartman, W. (1993a). Ground reaction force patterns of Dutch warmbloods at the canter. Am. J. Vet. Res. 54, 670-674.
53. Merkens, H. W., Schamhardt, H. C., van Osch, G. J. V. M. and van den Bogert, A. J. V. (1993b). Ground reaction force patterns of Dutch warmblood horses at normal trot. Equine Vet. J. 25, 134-137.
54. Minetti, A. E., Ardigò, L. P., Reinach, E. and Saibene, F. (1999). The relationship between mechanical work and energy expenditure of locomotion in horses. J. Exp. Biol. 202, 2329-2338. (Pubitemid 29452171)
55. O'Neill, M. C. (2009). The Structural Basis of Locomotor Cost: Gait, Mechanics and Limb Design in Ringtailed Lemurs (Lemur catta). PhD thesis, Johns Hopkins University, Baltimore, MD.
56. Orelien, J. G. and Edwards, L. J. (2008). Fixed-effect variable selection in linear mixed models using R2 statistics. Comp. Statist. Data Anal. 52, 1896-1907. (Pubitemid 350051436)
57. Patel, B. (2009). Not so fast: Speed effects on forelimb kinematics in cercopithecine monkeys and implications for digitgrade postures in primates. Am. J. Phys. Anthropol. 140, 92-112.
58. Pollock, C. M. and Shadwick, R. E. (1994). Relationships between body mass and biomechanical properties of limb tendons in adult mammals. Am. J. Physiol. Regul. Integr. Comp. Physiol. 226, R1016-R1021. (Pubitemid 24121399)
59. R Development Core Team (2008). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
60. Rauwerdink, G. P. (1993). Muscle fiber and tendon lengths in primate extremities. In Hands of Primates (ed. H. Preuschoft and D. J. Chivers), pp. 207-223. New York: Springer-Verlag.
61. Ren, L., Miller, C. E., Lair, R. and Hutchinson, J. R. (2010). Integration of biomechanical compliance, leverage, and power in elephant limbs. Proc. Natl. Acad. Sci. USA 107, 7078-7082.
62. Reynolds, T. R. (1985). Stresses on the limbs of quadrupedal primates. Am. J. Phys. Anthropol. 67, 351-362.
63. Reynolds, T. R. (1987). Stride length and its determinants in humans, early hominids, primates and mammals. Am. J. Phys. Anthropol. 72, 101-115. (Pubitemid 17230297)
64. Rollinson, J. and Martin, R. D. (1981). Comparative aspects of primate locomotion with special reference to arboreal cercopithecines. Symp. Zool. Soc. Lond. 48, 377-427.
65. Ruina, A., Bertram, J. E. A. and Srinivasan, M. (2005). A collisional model of the energetic cost of support work qualitatively explains leg sequencing in walking and galloping, pseudo-elastic leg behavior in running and the walk-to-run transition. J. Theor. Biol. 237, 170-192. (Pubitemid 41406403)
66. Schloz, M. N., D'Août, K., Bobbert, M. F. and Aerts, P. (2006). Vertical jumping performance of bonobo (Pan paniscus) suggests superior muscle properties. Proc. R. Soc. Lond. B 273, 2177-2184. (Pubitemid 44318307)
67. Schmitt, D. (1999). Compliant walking in primates. J. Zool. 248, 149-160. (Pubitemid 29311700)
68. Schmitt, D. (2003). Insights into the evolution of human bipedalism from experimental studies of humans and other primates. J. Exp. Biol. 206, 1437-1448. (Pubitemid 36573057)
69. Schmitt, D. and Lemelin, P. (2002). Origins of primate locomotion: Gait mechanics of the woolly opossum. Am. J. Phys. Anthropol. 118, 231-238. (Pubitemid 34680699)
70. Schmitt, D., Cartmill, M., Griffin, T. M., Hanna, J. B. and Lemelin, P. (2006). Adaptive value of ambling in primates and other mammals. J. Exp. Biol. 209, 2042-2049. (Pubitemid 43987881)
71. Thorpe, S. K. S., Crompton, R. H., Günther, M. M., Ker, R. F. and Alexander, R. M. (1999). Dimensions and moment arms of the hind-and forelimb muscles of common chimpanzees (Pan troglodytes). Am. J. Phys. Anthropol. 110, 179-199. (Pubitemid 29466218)
72. Usherwood, J. R. (2005). Why not walk faster? Biol. Lett. 1, 338-341. (Pubitemid 41374898)
73. Usherwood, J. R., Williams, S. B. and Wilson, A. M. (2007). Mechanics of dog walking compared with a passive, stiff-limbed, 4-bar linkage model, and their collisional implications. J. Exp. Biol. 210, 533-540. (Pubitemid 46347926)
74. Vilensky, J. A. (1979). A Biomechanical Analysis of Rhesus Monkey (Macaca mulatta). PhD thesis, University of Wisconsin, Madison, WI.
75. Vilensky, J. A. (1980). Trot-gallop transition in a macaque. Am. J. Phys. Anthropol. 53, 347-348. (Pubitemid 11144654)
76. Vilensky, J. A. (1983). Gait characteristics of two macaques, with emphasis on relationships with speed. Am. J. Phys. Anthropol. 61, 255-265. (Pubitemid 13051826)
77. Vilensky, J. A. (1987). Locomotor behavior and control in human and non-human primates: Comparisons with cats and dogs. Neurosci. Biobehav. Rev. 11, 263-274. (Pubitemid 17135593)
78. Vilensky, J. A. (1989). Primate quadrupedalism: How and why does it differ from that of typical quadrupeds? Brain Behav. Evol. 34, 357-364. (Pubitemid 20055864)
79. Vonesh, E. F. and Chinchilli, V. M. (1997). Linear and Nonlinear Models for the Analysis of Repeated Measurements. New York: Marcel Dekker, Inc.
80. Walker, J. A. (1998). Estimating velocities and accelerations of animal locomotion: Simulation experiment comparing numerical differentiation algorithms. J. Exp. Biol. 201, 981-995. (Pubitemid 28203144)
81. Weis-Fogh, T. and Alexander, R. M. (1977). The sustained power output from striated muscle. In Scale Effects in Animal Locomotion (ed. T. J. Pedley), pp. 511-525. London: Academic Press.
82. Willey, J. S., Biknevicius, A. R., Reilly, S. M. and Earls, K. D. (2004). The tale of the tail: Limb function and locomotor mechanics in Alligator mississippiensis. J. Exp. Biol. 207, 553-563. (Pubitemid 38162391)
83. Witte, T. H., Knill, K. and Wilson, A. M. (2004). Determination of peak vertical ground reaction force from duty factor in the horse (Equus caballus). J. Exp. Biol. 207, 3639-3648. (Pubitemid 39484182)
84. Woltring, H. J. (1985). On optimal smoothing and derivative estimation from noisy displacement data in biomechanics. Hum. Mov. Sci. 4, 229-245. (Pubitemid 15235403)
85. Woltring, H. J. (1986). A Fortran package for generalized cross-validatory spline smoothing and differentiation. Adv. Eng. Software 8, 104-107.
86. Young, J. W. (2009). Substrate determines asymmetrical gait dynamics in marmosets (Callithrix jacchus) and squirrel monkeys (Samiri boliviensis). Am. J. Phys. Anthropol. 138, 403-420.
87. Zani, P. A., Gottschall, J. S. and Kram, R. (2005). Giant Galápogos tortoises walk without inverted pendulum mechanical-energy exchange. J. Exp. Biol. 208, 1489-1494. (Pubitemid 40697537)