Primate locomotor evolution, particularly the evolution of bipedalism, is often examined through morphological studies. Many of these studies have examined the uniqueness of the primate forelimb, and others have examined the primate hip and thigh. Few data exist, however, regarding the myology and function of the leg muscles, even though the ankle plantar flexors are highly important during human bipedalism. In this paper, we draw together data on the fiber type and muscle mass variation in the ankle plantar flexors of primates and make comparisons to other mammals. The data suggest that great apes, atelines, and lorisines exhibit similarity in the mass distribution of the triceps surae. We conclude that variation in triceps surae may be related to the shared locomotor mode exhibited by these groups and that triceps surae morphology, which approaches that of humans, may be related to frequent use of semiplantigrade locomotion and vertical climbing. 1. Introduction From Aristotle’s thoughts in De Motu Animalium [1], to Borelli’s [2] comprehensive review of biomechanics in the 1600s, to Muybridge’s [3] original documentation of gaits in horses around the turn of the last century, animal movement has been a vibrant and productive area of research providing insights into critical aspects of form-function relationships and selection pressures on limb and body design in many vertebrates, including primates. In addition to capturing photographic plates of the different gaits of the horse, Muybridge also took stop motion images of other mammals, including a nonhuman primate. His famous collection of plates and prose, published in 1887, was the first available to researchers interested in animal locomotion [3] and spawned a new generation of scientists interested in locomotion. Following Muybridge’s observation that the baboon “disregards the law governing the walk” (3？:？30), multiple researchers created hypotheses concerning primate locomotor evolution, which were based on observed differences between primate and nonprimate locomotion (e.g., [4, 5]). For example, building on Muybridge’s observations on footfall, in which he argued for a differential functional role of the forelimb and hindlimb in primates, forty years later, De la Croix [6] commented on the unique aspects of what he called “the pithecoid gait” (6？:？53 and Figure 3 therein), which he argued was “the gait used by the early ancestors of man.” (6？:？53, referring to [7]). These early scientists laid the foundations for research in primate locomotor evolution. Since then researchers have been
References
[1]
M. C. Nussbaum, Aristotle’s De Motu Animalium, Princeton University Press, Princeton, NJ, USA, 1978.
[2]
G. A. Borelli, On the Movement of Animals, Springer, New York, NY, USA, 1989.
[3]
E. Muybridge, in Animals in Motion, L. S. Brown, Ed., Dover Publications, New York, NY, USA, 1957.
[4]
A. Keith, “The extent to which the posterior segments of the body have been transmuted and suppressed in the evolution of man and allied primates,” Journal of Anatomy and Physiology, vol. 37, pp. 18–40, 1903.
[5]
F. W. Jones, Arboreal Man, Hafner Press, New York, NY, USA, 1916.
[6]
P. M. De la Croix , “The evolution of locomotion in mammals,” Journal of Mammalogy, vol. 17, pp. 51–54, 1936.
[7]
P. M. De la Croix, “Phylogenie de la locomotion prebipede de l'homme,” Revue de Pathologie Comparée, vol. 22, no. 326, 1932.
[8]
M. Hildebrand, “Symmetrical gaits of primates,” American Journal of Physical Anthropology, vol. 26, pp. 119–130, 1967.
[9]
J. Rollinson and R. D. Martin, “Comparative aspects of primate locomotion with special reference to arboreal cercopithecines,” Symposia of the Zoological Society of London, vol. 48, pp. 377–427, 1981.
[10]
J. A. Vilensky, “Primate quadrupedalism: how and why does it differ from that of typical quadrupeds?” Brain, Behavior and Evolution, vol. 34, no. 6, pp. 357–364, 1989.
[11]
J. A. Vilensky and S. G. Larson, “Primate locomotion: utilization and control f symmetrical gaits,” Annual Review of Anthropology, vol. 18, pp. 17–35, 1989.
[12]
M. Cartmill, P. Lemelin, and D. Schmitt, “Support polygons and symmetrical gaits in mammals,” Zoological Journal of the Linnean Society, vol. 136, no. 3, pp. 401–420, 2002.
[13]
M. Cartmill, P. Lemelin, and D. Schmitt, “Understanding the adaptive value of diagonal-sequence gaits in primates: a comment on Shapiro and Raichlen, 2005,” American Journal of Physical Anthropology, vol. 133, no. 2, pp. 822–827, 2007.
[14]
L. J. Shapiro and D. A. Raichlen, “Lateral sequence walking in infant Papio cynocephalus: implications for the evolution of diagonal sequence walking in primates,” American Journal of Physical Anthropology, vol. 126, no. 2, pp. 205–213, 2005.
[15]
L. J. Shapiro and D. A. Raichlen, “A response to Cartmill et al. : primate gaits and arboreal stability,” American Journal of Physical Anthropology, vol. 133, no. 2, pp. 825–827, 2007.
[16]
I. J. Wallace and B. Demes, “Symmetrical gaits of Cebus apella: implications for the functional significance of diagonal sequence gait in primates,” Journal of Human Evolution, vol. 54, no. 6, pp. 783–794, 2008.
[17]
B. Demes, W. L. Jungers, and U. Nieschalk, “Size- and speed-related aspects of quadrupedal walking in slender and slow lorises,” in Gravity, Posture and Locomotion in Primates, F. K. Jouffroy, M. H. Stack, and C. Niemitz, Eds., pp. 175–198, Editrice Il Sedicesimo, Florence, Italy, 1990.
[18]
H. Preuschoft and M. M. Gunther, “Biomechanics and body shape in primates compared with horses,” Zeitsscrif fur Morphologie und Anthropologie, vol. 80, pp. 149–165, 1994.
[19]
D. A. Raichlen, “Convergence of forelimb and hindlimb natural pendular period in baboons (Papio cynocephalus) and its implication for the evolution of primate quadrupedalism,” Journal of Human Evolution, vol. 46, no. 6, pp. 719–738, 2004.
[20]
D. Schmitt, M. Cartmill, T. M. Griffin, J. B. Hanna, and P. Lemelin, “Adaptive value of ambling gaits in primates and other mammals,” Journal of Experimental Biology, vol. 209, no. 11, pp. 2042–2049, 2006.
[21]
M. C. O'Neill, The structural basis of locomotor cost: gait, mechanics and limb design in ringtailed lemurs (Lemur catta), Ph.D. thesis, Johns Hopkins University, Baltimore, Md, USA, 2008.
[22]
M. O’Neill and D. Schmitt, “The gaits of a primate: center of mass mechanics in walking, cantering, and galloping ringtailed lemurs, Lemur catta,” The Journal of Experimental Biology. In review.
[23]
T. Kimura, M. Okada, and H. Ishida, “Kinesiological characteristics of primate walking: its significance in human walking,” in Environment, Behavior, and Morphology: Dynamic Interactions in Primates, M. E. Morbeck, H. Preuschoft, and N. Gomberg, Eds., pp. 297–311, Gustav Fischer, New York, NY, USA, 1979.
[24]
B. Demes, S. G. Larson, J. T. Stern, W. L. Jungers, A. R. Biknevicius, and D. Schmitt, “The kinetics of primate quadrupedalism: “hindlimb drive” reconsidered,” Journal of Human Evolution, vol. 26, pp. 353–374, 1994.
[25]
D. Schmitt and P. Lemelin, “Origins of primate locomotion: gait mechanics of the woolly opossum,” American Journal of Physical Anthropology, vol. 118, no. 3, pp. 231–238, 2002.
[26]
D. Schmitt and J. B. Hanna, “Substrate alters forelimb to hindlimb peak force ratios in primates,” Journal of Human Evolution, vol. 46, no. 3, pp. 237–252, 2004.
[27]
S. G. Larson, D. Schmitt, P. Lemelin, and M. W. Hamrick, “Uniqueness of primate forelimb posture during quadrupedal locomotion,” American Journal of Physical Anthropology, vol. 112, no. 1, pp. 87–101, 2000.
[28]
S. G. Larson, D. Schmitt, P. Lemelin, and M. W. Hamrick, “Limb excursion during quadrupedal walking: how do primates compare to other mammals?” Journal of Zoology, vol. 255, no. 3, pp. 353–365, 2001.
[29]
D. Schmitt, “Compliant walking in primates,” Journal of Zoology London, vol. 248, no. 2, pp. 149–160, 1999.
[30]
E. Larney and S. G. Larson, “Compliant walking in primates: elbow and knee yield in primates compared to other mammals,” American Journal of Physical Anthropology, vol. 125, no. 1, pp. 42–50, 2004.
[31]
J. T. Stern Jr., “Before bipedality,” Yearbook of Physical Anthropology, vol. 19, pp. 59–68, 1976.
[32]
T. R. Reynolds, “Stresses on the limbs of quadrupedal primates,” American Journal of Physical Anthropology, vol. 67, no. 4, pp. 351–362, 1985.
[33]
S. G. Larson, “Unique aspects of quadrupedal locomotion in nonhuman primates,” in Primate Locomotion: Recent Advances, E Strasser, A. Rosenberger, H. McHenry, and J. Fleagle, Eds., pp. 157–274, Plenum Press, New York, NY, USA, 1998.
[34]
M. Cartmill, D. Schmitt, and P. Lemelin, “Duty factors and lateral sequence gaits in primates and chameleons,” American Journal of Physical Anthropology, vol. 38, supplement, 73 pages, 2004.
[35]
M. Cartmill, “Arboreal adaptations and the origin of the order primates,” in The Functional and Evolutionary Biology of Primates, R. H. Tuttle, Ed., pp. 97–122, Aldine Press, Chicago, Ill, USA, 1972.
[36]
M. Cartmill, “New views on primate origins,” Evolutionary Anthropology, vol. 1, no. 3, pp. 105–111, 1992.
[37]
P. Lemelin, “Morphological correlates of substrate use in didelphid marsupials: implications for primate origins,” Journal of Zoology, vol. 247, no. 2, pp. 165–175, 1999.
[38]
P. Lemelin and D. Schmitt, “The origins of grasping and locomotor adaptations in primates: comparative and experimental approaches using an opossum model,” in Primate Origins: Adaptations and Evolution, M. Ravosa and M. Dagosto, Eds., pp. 329–380, Kluwer Academic Publishers, New York, NY, USA, 2007.
[39]
D. Schmitt, “Insights into the evolution of human bipedalism from experimental studies of humans and other primates,” Journal of Experimental Biology, vol. 206, no. 9, pp. 1437–1448, 2003.
[40]
D. Schmitt, “Primate locomotor evolution,” in Primate Neuroethology, M. E. Platt and A. A. Ghazar, Eds., pp. 31–64, Oxford University Press, New York, NY, USA, 2010.
[41]
D. Schmitt, A kinematic and kinetic analysis of forelimb use during arboreal and terrestrial quadrupedalism in Old World monkeys, Ph.D. thesis, State University of New York at Stony Brook, Stony Brook, NY, USA, 1995.
[42]
J. B. Hanna, J. D. Polk, and D. Schmitt, “Forelimb and hindlimb forces in walking and galloping primates,” American Journal of Physical Anthropology, vol. 130, no. 4, pp. 529–535, 2006.
[43]
B. Demes, J. G. Fleagle, and W. L. Jungers, “Takeoff and landing forces of leaping strepsirhine primates,” Journal of Human Evolution, vol. 37, no. 2, pp. 279–292, 1999.
[44]
E. Hirasaki, S. Matano, Y. Nakano, and H. Ishida, “Vertical climbing in Ateles geoffroyi and Macaca fuscata and its comparative neurological background,” in Topics in Primatology, S. Matano, R. H. Tuttle, H. Ishida, and M. Goodman, Eds., pp. 167–176, University of Tokyo Press, Tokyo, Japan, 1992.
[45]
E. Hirasaki, H. Kumakura, and S. Matano, “Kinesiological characteristics of vertical climbing in Ateles geoffroyi and Macaca fuscata,” Folia Primatologica, vol. 61, no. 3, pp. 148–156, 1993.
[46]
J. B. Hanna and D. Schmitt, “Interpreting the role of climbing in primate locomotor evolution: are the biomechanics of climbing influenced by habitual substrate use and anatomy?” International Journal of Primatology, vol. 32, no. 2, pp. 430–444, 2011.
[47]
J. D. Polk, B. Demes, W. L. Jungers, A. R. Biknevicius, R. E. Heinrich, and J. A. Runestad, “A comparison of primate, carnivoran and rodent limb bone cross-sectional properties: are primates really unique?” Journal of Human Evolution, vol. 29, no. 3, pp. 297–325, 2000.
[48]
J. R. Napier, “Prehensility and opposability in the hands of primates,” Symposia of the Zoological Society of London, vol. 5, pp. 115–132, 1961.
[49]
T. I. Grand, “A mechanical interpretation of terminal branch feeding,” Journal of Mammalogy, vol. 53, pp. 198–201, 1972.
[50]
M. Cartmill, “Rethinking primate origins,” Science, vol. 184, no. 4135, pp. 436–443, 1974.
[51]
M. Cartmill, “Pads and claws in arboreal locomotion,” in Primate Locomotion, F. A. Jenkins, Ed., pp. 45–83, Academic Press, New York, NY, USA, 1974.
[52]
F. K. Jouffroy, “Osteology and myology of the lemuriform postcranial skeleton,” in Lemur Biology, I. Tattersall and R. W. Sussman, Eds., pp. 149–192, Plenum Press, New York, NY, USA, 1975.
[53]
P. Lemelin and B. W. Grafton, “Grasping performance in Saguinus midas and the evolution of hand prehensility in primates,” in Primate Locomotion: Recent Advances, E. Strasser, J. Fleagle, A. Rosenberger, and H. McHenry, Eds., pp. 131–144, Plenum Press, New York, NY, USA, 1995.
[54]
J. G. Fleagle, “Locomotor behavior and muscular anatomy of sympatric Malaysian leaf monkeys (Presbytis obscura and Presbytis melalophos),” American Journal of Physical Anthropology, vol. 46, no. 2, pp. 297–307, 1977.
[55]
J. E. McArdle, “Functional morphology of the hip and thigh of the Lorisiformes,” in Contributions to Primatology, F. S. Szalay, Ed., vol. 17, Karger Press, New York, NY, USA, 1981.
[56]
J. G. Fleagle and D. J. Meldrum, “Locomotor behavior and skeletal morphology of two sympatric pitheciine monkeys, Pithecia pithecia and Chiropotes satanas,” American Journal of Primatology, vol. 16, pp. 227–249, 1988.
[57]
R. L. Anemone, “The VCL hypothesis revisited: patterns of femoral morphology among quadrupedal and saltatorial prosimian primates,” American Journal of Physical Anthropology, vol. 83, no. 3, pp. 373–393, 1990.
[58]
J. R. Connour, K. Glander, and F. Vincent, “Postcranial adaptations for leaping in primates,” Journal of Zoology, vol. 251, no. 1, pp. 79–103, 2000.
[59]
T. M. Ryan and R. A. Ketcham, “Angular orientation of trabecular bone in the femoral head and its relationship to hip joint loads in leaping primates,” Journal of Morphology, vol. 265, no. 3, pp. 249–263, 2005.
[60]
R. Susman, J. T. J. Stern, and W. L. Jungers, “Arboreality and bipedality in the hadar hominids,” Folia Primatologica, vol. 43, no. 2-3, pp. 113–156, 1984.
[61]
J. T. Stern, “Climbing to the top: a personal memoir of Australopithecus afarensis,” Evolutionary Anthropology, vol. 9, no. 3, pp. 113–133, 2000.
[62]
C. Owen Lovejoy, G. Suwa, L. Spurlock, B. Asfaw, and T. D. White, “The pelvis and femur of ardipithecus ramidus: the emergence of upright walking,” Science, vol. 326, no. 5949, pp. 71–76, 2009.
[63]
K. Kimura and S. Takai, “Comparative anatomical studies of the extremities of the crab-eating monkey based on the relative muscle weight,” The Anthropological Society of Nippon, vol. 45, no. 2, pp. 80–90, 1970.
[64]
J. T. Stern Jr., “Functional myology of the hip and thigh of cebid monkeys and its implications for the evolution of erect posture,” Bibliotecha Primatology, vol. 14, pp. 1–318, 1971.
[65]
A. K. Vangor, Electromyography of gait in non-human primates and its significance for the evolution of bipedality, Ph.D. thesis, State University of New York at Stony Brook, Stony Brook, NY, USA, 1980.
[66]
A. K. Vangor and J. P. Wells, “Muscle recruitment and the evolution of bipedality: evidence from telemetered electromyography of the spider, woolly, and patas monkeys,” Annales des Sciences Naturelles Zoologique Paris, vol. 5, pp. 125–135, 1983.
[67]
J. Kataoka, “Comparative studies on muscle structure of the m. triceps surae and m. plantaris in man and monkey,” Journal of the Anthropological Society of Nippon, vol. 47, no. 6, pp. 851–861, 1987.
[68]
E. Glaesmer, “Untersuchung ueber die flexorengruppe am unterschekel und fuβ der saeugetiere,” Morphologie Jahrbuch, vol. 38, pp. 36–90, 1908.
[69]
E. Glaesmer, “Die beugumuskeln am unterschenkel und fub bei insectivoran, marsupialiern, edentaten, prosimiae und simiae,” Morphologie Jahrbuch, vol. 41, pp. 147–336, 1910.
[70]
H. Frey, “Der musculus triceps surae in der primatenreihe,” Morphologie Jahrbuch, vol. 47, pp. 1–191, 1913.
[71]
J. H. Langdon, “Variations in cruropedal musculature,” International Journal of Primatology, vol. 11, no. 6, pp. 575–606, 1990.
[72]
S. J. Houtz and F. P. Walsh, “Electromyographic analysis of the functions of the muscles acting on the ankle during weightbearing with special reference to the triceps surae,” The Journal of Bone and Joint Surgery, vol. 41, pp. 1469–1481, 1959.
[73]
A. Zihlman and L. Brunker, “Hominid bipedalism: then and now,” Yearbook of Physical Anthropology, vol. 22, pp. 132–162, 1979.
[74]
F. C. Anderson and M. G. Pandy, “Storage and utilization of elastic strain energy during jumping,” Journal of Biomechanics, vol. 26, no. 12, pp. 1413–1427, 1993.
[75]
F. E. Zajac, R. R. Neptune, and S. A. Kautz, “Biomechanics and muscle coordination of human walking: part II: lessons from dynamical simulations and clinical implications,” Gait and Posture, vol. 17, no. 1, pp. 1–17, 2003.
[76]
R. R. Neptune, F. E. Zajac, and S. A. Kautz, “Muscle force redistributes segmental power for body progression during walking,” Gait and Posture, vol. 19, no. 2, pp. 194–205, 2004.
[77]
B. Walmsley, J. A. Hodgson, and R. E. Burke, “Forces produced by medial gastrocnemius and soleus muscles during locomotion in freely moving cats,” Journal of Neurophysiology, vol. 41, no. 5, pp. 1203–1216, 1978.
[78]
W. Herzog and T. R. Leonard, “Soleus forces and soleus force potential during unrestrained cat locomotion,” Journal of Biomechanics, vol. 29, no. 3, pp. 271–279, 1996.
[79]
B. I. Prilutsky, W. Herzog, and T. L. Allinger, “Mechanical power and work of cat soleus, gastrocnemius and plantaris muscles during locomotion: possible functional significance of muscle design and force patterns,” The Journal of Experimental Biology, vol. 199, pp. 801–814, 1996.
[80]
C. G. Hartman and W. L. Straus Jr., The Anatomy of the Rhesus Monkey, Hafner Publishing Company, New York, NY, USA, 1933.
[81]
M. A. Sch？n, The Musculature System of the Red Howling Monkey, Smithsonian Institution Press, Washington, DC, USA, 1968.
[82]
B. A. Sigmon and D. L. Farslow, “The primate hindlimb,” in Comparative Primate Biology, Vol. 1: Systematics, Evolution, and Anatomy, D. R. Swindler and J. Erwin, Eds., vol. 1, pp. 671–718, Alan R. Liss, New York, NY, USA, 1986.
[83]
S. Standring, Gray's Anatomy, Elsevier, New York, NY, USA, 39th edition, 2005.
[84]
R. A. Bergman, S. A. Thomspon, A. K. Afifi, and F. A. Saadeh, Compendium if Human Anatomic Variation, Urban & Schwarzenberg, Baltimore, Md, USA, 1988.
[85]
O. J. Lewis, “The phylogeny of the crural and pedal flexor musculature,” Proceedings of the Zoological Society of London, vol. 138, pp. 77–109, 1962.
[86]
O. J. Lewis, “The monotreme cruro-pedal flexor musculature,” Journal of Anatomy London, vol. 97, no. 1, pp. 55–63, 1963.
[87]
O. J. Lewis, “The evolution of the long flexor muscle of the leg and foot,” Review of General and Experimental Zoology, vol. 1, pp. 165–185, 1964.
[88]
E. Loth, “Die aponeurosis plantaris in der primatenreihe,” Gegenbaurs Morphologisches Jahrbuch, vol. 38, pp. 194–321, 1908.
[89]
C. Argot, “Functional, adaptive analysis of the hindlimb anatomy of extant marsupials and the paleobiology of the Paleocene marsupials Mayulestes ferox and Pucadelphys andinus,” Journal of Morphology, vol. 253, no. 1, pp. 76–108, 2002.
[90]
R. E. Fisher, B. Adrian, C. Elrod, and M. Hicks, “The phylogeny of the red panda (Ailurus fulgens): evidence from the hindlimb,” Journal of Anatomy, vol. 213, no. 5, pp. 607–628, 2008.
[91]
R. E. Fisher, K. M. Scott, and B. Adrian, “Hind limb myology of the common hippopotamus, Hippopotamus amphibius (Artiodactyla: Hippopotamidae),” Zoological Journal of the Linnean Society, vol. 158, no. 3, pp. 661–682, 2010.
[92]
C. F. Sonntag, “On the myology and classification of the wombat, koala, and phalangers,” Proceedings of the Zoological Society of London, pp. 863–896, 1922.
[93]
A. Prejzner-Morawska and M. Urbanowicz, “Morphology of some of the lower limb muscles in primates,” in Primate Evolutionary Biology, A. B. Chiarelli and R. S. Corruccini, Eds., pp. 60–67, Springer, New York, NY, USA, 1981.
[94]
H. H. Woollard, “The anatomy of Tarsius spectrum,” Proceedings of the Zoological Society, vol. 70, pp. 1071–1184, 1925.
[95]
J. Murie and S. G. Mivart, “On the anatomy of the Lemuroidea,” Transactions of the Zoological Society, vol. 7, no. 1, pp. 1–113, 1866.
[96]
E. L. Patterson, “The myology of Rhinopithecus roxellanae and Cynopithecus niger,” Proceedings of the Zoological Society of London, pp. 31–104, 1942.
[97]
D. R. Swindler and C. D. Wood, An Atlas of Primate Gross Anatomy: Baboon, Chimpanzee, and Man, University of Washington Press, Seattle, Wash, 1973.
[98]
J. L. Stevens, V. R. Edgerton, and S. Mitton, “Gross anatomy of the hindlimb skeletal system of the Galago senegalensis,” Primates, vol. 12, no. 3-4, pp. 313–321, 1972.
[99]
S. Babcock, Hindlimb Muscle Morphology and Mechanical Adaptation in Galagos: An Analysis of Scale, Function, and Phylogeny, Ph.D. thesis, Duke University, Durham, NC, USA, 1993.
[100]
C. Gans and W. J. Bock, “The functional significance of muscle architecture: a theoretical analysis,” Ergebn Anat Entwickl-Gesch, vol. 38, pp. 115–142, 1965.
[101]
C. Gans, “Fiber architecture and muscle function,” Exercise and Sport Sciences Reviews, vol. 10, pp. 160–207, 1982.
[102]
R. D. Sacks and R. R. Roy, “Architecture of the hind limb muscles of cats: functional significance,” Journal of Morphology, vol. 173, no. 2, pp. 185–195, 1982.
[103]
F. Anapol and K. Barry, “Fiber architecture of the extensors of the hindlimb in semiterrestrial and arboreal guenons,” American Journal of Physical Anthropology, vol. 99, no. 3, pp. 429–447, 1996.
[104]
M. H. Brooke and K. K. Kaiser, “Muscle fiber types: how many and what kind?” Archives of Neurology, vol. 23, no. 4, pp. 369–379, 1970.
[105]
D. F. Goldspink, “Growth of muscle,” in Developmental and Specialization of Skeletal Muscle, D. F. Goldspink, Ed., pp. 19–36, Cambridge University Press, Cambridge, UK, 1980.
[106]
K. G. Braund, K. A. Amling, J. R. Mehta, J. E. Steiss, and C. Scholz, “Histochemical and morphometric study of fiber types in ten skeletal muscles of healthy young adult cats,” American Journal of Veterinary Research, vol. 56, no. 3, pp. 349–357, 1995.
[107]
F. K. Jouffroy, J. T. Stern Jr., M. F. Medina, and S. G. Larson, “Function and cytochemical characteristics of postural limb muscles of the rhesus monkey: a telemetered EMG and immunofluorescence study,” Folia Primatologica, vol. 70, no. 5, pp. 235–253, 1999.
[108]
C. Cordonnier, L. Stevens, F. Picquet, and Y. Mounier, “Structure-function relationship of soleus muscle fibres from the rhesus monkey,” Pflügers Archiv European Journal of Physiology, vol. 430, pp. 19–25, 1995.
[109]
M. A. Ariano, R. B. Armstrong, and V. R. Edgerton, “Hindlimb muscle fiber populations of five mammals,” Journal of Histochemistry and Cytochemistry, vol. 21, no. 1, pp. 51–55, 1973.
[110]
S. E. Peters, R. Mulkey, S. A. Rasmussen, and G. E. Goslow Jr, “Motor units of the primary ankle extensor muscles of the opossum (Didelphis virginiana): functional properties and fiber types,” Journal of Morphology, vol. 181, no. 3, pp. 305–317, 1984.
[111]
L. Acosta and R. R. Roy, “Fiber-type composition of selected hindlimb muscles of a primate (Cynomolgus monkey),” Anatomical Record, vol. 218, no. 2, pp. 136–141, 1987.
[112]
V. R. Edgerton, R. J. Barnard, J. B. Peter, A. Maier, and D. R. Simpson, “Properties of immobilized hind-limb muscles of the Galago senegalensis,” Experimental Neurology, vol. 46, pp. 115–131, 1975.
[113]
K. M. Van De Graaff, E. C. Frederick, R. G. Williamson, and G. E. Goslow Jr, “Motor units and fiber types of primary ankle extensors of the skunk (Mephitis mephitis),” Journal of Neurophysiology, vol. 40, no. 6, pp. 1424–1431, 1977.
[114]
T. J. Burkholder, B. Fingado, S. Baron, and R. L. Lieber, “Relationship between muscle fiber types and sizes and muscle architectural properties in the mouse hindlimb,” Journal of Morphology, vol. 221, no. 2, pp. 177–190, 1994.
[115]
R. B. Armstrong, “Properties and distributions of the fibre types in the locomotory muscles of mammals,” in Comparative Physiology: Primitive Mammals, k. Schmidt-Nielsen,, L. Bolis, and C. R. Taylor, Eds., pp. 243–254, Cambridge University Press, Cambridge, UK, 1980.
[116]
R. B. Armstrong, C. W. Saubert, H. J. Seeherman, and C. R. Taylor, “Distribution of fiber types in locomotory muscles of dogs,” American Journal of Anatomy, vol. 163, no. 1, pp. 87–98, 1982.
[117]
D. Kernall, “Muscle regionalization,” Canadian Journal of Applied Physiology, vol. 23, pp. 1–22, 1998.
[118]
L. C. Wang and D. Kernall, “Fibre type regionalization in lower hindlimb muscles of rabbit, rat and mouse: a comparative study,” Journal of Anatomy, vol. 199, pp. 631–643, 2001.
[119]
J. Joseph, Man’s Posture: Electromyographic Studies, Charles C Thomas, Springfield, Mass, USA, 1960.
[120]
R. M. Alexander, A. S. Jayes, M. O. Maloiy, and E. M. Wathuta, “Allometry of the leg muscles of mammals,” Journal of Zoology London, vol. 194, pp. 539–552, 1981.
[121]
C. M. Pollock and R. E. Shadwick, “Allometry of muscle, tendon, and elastic energy storage capacity in mammals,” American Journal of Physiology, vol. 266, no. 3, pp. R1022–R1031, 1994.
[122]
R. C. Payne, R. H. Crompton, K. Isler et al., “Morphological analysis of the hindlimb in apes and humans. I. Muscle architecture,” Journal of Anatomy, vol. 208, no. 6, pp. 709–724, 2006.
[123]
E. E. Vereecke, K. D'Ao？t, R. Payne, and P. Aerts, “Functional analysis of the foot and ankle myology of gibbons and bonobos,” Journal of Anatomy, vol. 206, no. 5, pp. 453–476, 2005.
[124]
S. K. S. Thorpe, R. H. Crompton, M. M. Guenther, R. F. Ker, and R. M. Alexander, “Dimensions and moment arms of the hind- and forelimb muscles of common chimpanzees (Pan troglodytes),” American Journal of Physical Anthropology, vol. 110, pp. 179–199, 1999.
[125]
K. J. Carlson, “Muscle architecture of the common chimpanzee (Pan troglodytes): perspectives for investigating chimpanzee behavior,” Primates, vol. 47, no. 3, pp. 218–229, 2006.
[126]
N. C. Tappen, “Relative weights of some functionally important muscles of the thigh, hip and leg in a gibbon and in man,” American Journal of Physical Anthropology, vol. 13, no. 3, pp. 415–420, 1955.
[127]
J. Ito, N. Shiraishi, M. Umino, T. Kimura, and H. Akita, “Morphological evaluation of the baboon hind limb muscles based on relative weight,” Okajimas Folia Anatomica Japonica, vol. 77, no. 5, pp. 161–166, 2000.
[128]
T. I. Grand, “The functional anatomy of the lower limb of the howler monkey (Alouatta caraya),” American Journal of Physical Anthropology, vol. 28, pp. 163–182, 1968.
[129]
B. Demes, J. G. Fleagle, and P. Lemelin, “Myological correlates of prosimian leaping,” Journal of Human Evolution, vol. 34, no. 4, pp. 385–399, 1998.
[130]
T. I. Grand, “The functional anatomy of the ankle and foot of the slow loris (Nycticebus coucang),” American Journal of Physical Anthropology, vol. 26, pp. 207–218, 1967.
[131]
R. B. Armstrong and R. O. Phelps, “Muscle fiber type composition of the rat hindlimb,” American Journal of Anatomy, vol. 171, no. 3, pp. 259–272, 1984.
[132]
S. B. Williams, R. C. Payne, and A. M. Wilson, “Functional specialisation of the pelvic limb of the hare (Lepus europeus),” Journal of Anatomy, vol. 210, no. 4, pp. 472–490, 2007.
[133]
R. C. Payne, J. R. Hutchinson, J. J. Robilliard, N. C. Smith, and A. M. Wilson, “Functional specialisation of pelvic limb anatomy in horses (Equus caballus),” Journal of Anatomy, vol. 206, no. 6, pp. 557–574, 2005.
[134]
C. E. Miller, The anatomy and biomechanics of elephant limbs and feet, Ph.D. thesis, The Veterinary College, University of London, London, UK, 2009.
[135]
C. F. Sonntag, “On the anatomy, physiology, and pathology of the orang-outan,” Proceedings of the Zoological Society of London, vol. 24, no. 24, pp. 349–450, 1924.
[136]
F. J. Shepherd, “Short notes on the myology of the American black bear,” Proceedings of the Royal Society London, pp. 103–117, 1895.
[137]
E. A. Kelley, “Notes on the myology of Ursus maritimus,” Proceedings of the Academy of Natural Sciences of Philadelphia, vol. 40, pp. 141–154, 1888.
[138]
L. J. Ray, “The myology of the inferior extremity of the Malay bear, Ursus malayanus,” Proceedings of the Zoological Society of London, vol. 119, pp. 121–132, 1949.
[139]
G. E. Weissengruber and G. Forstenpointner, “Musculature of the crus and pes of the African elephant (Loxodonta africana): insight into semiplantigrade limb architecture,” Anatomy and Embryology, vol. 208, no. 6, pp. 451–461, 2004.
[140]
B. Campbell, The comparative myology of the hippopotamus, pig, tapir, Ph.D. thesis, Johns Hopkins Unversity Medical School, Baltimore, Md, USA, 1935.
[141]
D. M. Doran, “The ontogeny of chimpanzee and pygmy chimpanzee locomotor behavior: a case study of paedomorphism and its behavioral correlates,” Journal of Human Evolution, vol. 23, no. 2, pp. 139–157, 1992.
[142]
J. E. Turnquist and J. P. Wells, “Ontogeny of locomotion in rhesus macaques (Macaca mulatta): I. Early postnatal ontogeny of the musculoskeletal system,” Journal of Human Evolution, vol. 26, no. 5-6, pp. 487–499, 1994.
[143]
D. M. Doran, “Ontogeny of locomotion in mountain gorillas and chimpanzees,” Journal of Human Evolution, vol. 32, no. 4, pp. 323–344, 1997.
[144]
J. P. Wells and J. E. Turnquist, “Ontogeny of locomotion in rhesus macaques (macaca mulatta): II. Postural and locomotor behavior and habitat use in a free-ranging colony,” American Journal of Physical Anthropology, vol. 115, no. 1, pp. 80–94, 2001.
[145]
W. C. O. Hill, Primates: Comparative Anatomy and Taxonomy. Cebidae Part B, John Wiley and Sons, New York, NY, USA, 1962.
[146]
B. C. A. Windle, “Notes on the mycology of Midas rosalia with remarks on the muscular system in apes,” Proceedings of the Birmingham Philosophical Society, vol. 5, pp. 152–166, 1886.
[147]
I. Engberg and A. Lundgren, “An electromyographic analysis of muscular activity in the hindlimb of the cat during unrestrained locomotion,” Acta Physiologica Scandinavica, vol. 75, pp. 614–630, 1969.
[148]
M. Tokuriki, “Electromyographic and joint-mechanical studies in quadrupedal locomotion. I. Walk,” The Japanese Journal of Veterinary Science, vol. 35, no. 5, pp. 433–446, 1973.
[149]
S. Rasmussen, A. K. Chan, and G. E. Goslow Jr., “The cat step cycle: electromyographic patterns for hindlimb muscles during posture and unrestrained locomotion,” Journal of Morphology, vol. 155, no. 3, pp. 253–269, 1978.
[150]
G. E. Goslow Jr., H. J. Seeherman, C. R. Taylor, M. N. McCutchin, and N. C. Heglund, “Electrical activity and relative length changes of dog limb muscles as a function of speed and gait,” Journal of Experimental Biology, vol. 94, pp. 15–42, 1981.
[151]
L. D. Abraham and G. E. Loeb, “The distal hindlimb musculature of the cat,” Experimental Brain Research, vol. 58, no. 3, pp. 580–593, 1985.
[152]
P. F. Gardiner and A. E. Olha, “Contractile and electromyographic characteristics of rat plantaris motor unit types during fatigue in situ,” Journal of Physiology, vol. 385, pp. 13–34, 1987.
[153]
K. R. Gardiner, P. F. Gardiner, and V. R. Edgerton, “Guinea pig soleus and gastrocnemius electromyograms at varying speeds, grades, and loads,” Journal of Applied Physiology, vol. 52, no. 2, pp. 451–457, 1982.
[154]
J. A. Hodgson, S. Wichayanuparp, M. R. Recktenwald et al., “Circadian force and EMG activity in hindlimb muscles of rhesus monkeys,” Journal of Neurophysiology, vol. 86, no. 3, pp. 1430–1444, 2001.
[155]
A. L. O'Connell, “Electromyographic study of certain leg muscles during movements of the free foot and during standing,” American Journal of Physical Medicine, vol. 37, no. 6, pp. 289–301, 1958.
[156]
C. K. Battye and J. Joseph, “An investigation by telementering of the activity of some muscles in walking,” Medical & Biological Engineering, vol. 4, no. 2, pp. 125–135, 1966.
[157]
J. V. Basmajian, Muscles Alive: Their Functions Revealed By Electromyography, The Williams and Wilkins Company, Baltimore, Md, USA, 2nd edition, 1967.
[158]
D. H. Sutherland, “An electromyographic study of the plantar flexors of the ankle in normal walking on the level,” Journal of Bone and Joint Surgery, vol. 48, no. 1, pp. 66–71, 1966.
[159]
W. L. Hylander and K. R. Johnson, “The relationship between masseter force and masseter electromyogram during mastication in the monkey Macaca fascicularis,” Archives of Oral Biology, vol. 34, no. 9, pp. 713–722, 1989.
[160]
W. L. Hylander and K. R. Johnson, “Modelling relative masseter force from surface electromyograms during mastication in non-human primates,” Archives of Oral Biology, vol. 38, no. 3, pp. 233–240, 1993.
[161]
R. R. Neptune, S. A. Kautz, and F. E. Zajac, “Contributions of the individual ankle plantar flexors to support, forward progression and swing initiation during walking,” Journal of Biomechanics, vol. 34, no. 11, pp. 1387–1398, 2001.
[162]
M. Q. Liu, F. C. Anderson, M. G. Pandy, and S. L. Delp, “Muscles that support the body also modulate forward progression during walking,” Journal of Biomechanics, vol. 39, no. 14, pp. 2623–2630, 2006.
[163]
W. T. Liberson, “Biomechanics of gait: a method of study,” Archives of Physical Medicine and Rehabilitation, vol. 46, pp. 37–48, 1965.
[164]
R. A. Mann and J. Hagy, “Biomechanics of walking, running, and sprinting,” American Journal of Sports Medicine, vol. 8, no. 5, pp. 345–350, 1980.
[165]
J. Nilsson, A. Thorstensson, and J. Halbertsma, “Changes in leg movements and muscle activity with speed of locomotion and mode of progression in humans,” Acta Physiologica Scandinavica, vol. 123, pp. 457–475, 1985.
[166]
P. R. Cavanagh and M. A. Lafortune, “Ground reaction forces in distance running,” Journal of Biomechanics, vol. 13, no. 5, pp. 397–406, 1980.
[167]
D. I. Miller, “Ground reaction forces in distance running,” in Biomechanics of Distance Running, P. Cavanagh, Ed., pp. 203–224, Human Kinetics Books, Champaign, Ill, USA, 1990.
[168]
G. A. Valiant, “Transmission and attenuation of heel-strike accelerations,” in Biomechanics of Distance Running, P. Cavanagh, Ed., pp. 225–248, Human Kinetics Books, Champaign, Ill, USA, 1990.
[169]
D. E. Lieberman, M. Venkadesan, W. A. Werbel et al., “Foot strike patterns and collision forces in habitually barefoot versus shod runners,” Nature, vol. 463, no. 7280, pp. 531–535, 2010.
[170]
H. Ishida, T. Kimura, and M. Okada, “Patterns of bipedal walking in anthropoid primates,” in Proceedings of the Fifth Congress of the International Primatological Society, S. Kondo, M. Kawai, A. Ehara, and S. Kawamura, Eds., pp. 287–301, Japan Science Press, Tokyo, Japan, 1974.
[171]
H. Ishida, M. Okada, R. H. Tuttle, and T. Kimura, “Activities of hindlimb muscles in bipedal gibbons,” in Recent Advances in Primatology, D. J. Chivers and K. A. Joysey, Eds., vol. 3 of Evolution, pp. 459–462, Academic Press, London, UK, 1978.
[172]
D. Schmitt and S. G. Larson, “Heel contact as a function of substrate type and speed in primates,” American Journal of Physical Anthropology, vol. 96, no. 1, pp. 39–50, 1995.
[173]
H. Ishida, T. Kimura, M. Okada, and N. Yamazaki, “Kinesiological aspects of bipedal walking in gibbons,” in The Lesser Apes: Evolution and Behavioral Biology, H. Preuschoft, D. J. Chivers, W. Y. Bruckelman, and N. Creel, Eds., pp. 135–145, Edinburgh University Press, Edinburgh, UK, 1984.
[174]
M. Okada, “Primate bipedal walking: comparative kinematics,” in Primate Morphophysiology, Locomotor Analyses, and Human Bipedalism, S. Kondo, H. Ishida, and T. Kimura, Eds., pp. 47–58, University of Tokyo Press, Tokyo, Japan, 1985.
[175]
E. Hirasaki, H. Kumakura, and S. Matano, “Electromyography of 15 limb muscles in Japanese macaques (Macaca fuscata) during vertical climbing,” Folia primatologica, vol. 64, no. 4, pp. 218–224, 1995.
[176]
E. Hirasaki, H. Kumarkura, and S. Matano, “Biomechanical analysis of vertical climbing in the spider monkey and the Japanese macaque,” American Journal of Physical Anthropology, vol. 113, pp. 455–472, 2000.
[177]
D. Meglan and F. Todd, “Kinetics of human walking,” in Human Walking, J. Rose and J. G. Gamble, Eds., pp. 73–99, Williams and Wilkins, Baltimore, Md, USA, 2nd edition, 1994.
[178]
D. Schmitt, “Mediolateral reaction forces and forelimb anatomy in quadrupedal primates: Implications for interpreting locomotor behavior in fossil primates,” Journal of Human Evolution, vol. 44, no. 1, pp. 47–58, 2003.
[179]
K. J. Carlson, B. Demes, and T. M. Franz, “Mediolateral forces associated with quadrupedal gaits of lemurids,” Journal of Zoology, vol. 266, no. 3, pp. 261–273, 2005.
[180]
R. Wunderlich, Pedal form and plantar pressure distribution in anthropoid primates, Ph.D. thesis, State University of New York at Stony Brook, Stony Brook, NY, USA, 1999.
[181]
Y. Li, R. H. Crompton, R. M. Alexander, M. M. Guenther, and W. J. Wang, “Characteristics of ground reaction forces in normal and chimpanzee-like bipedal walking by humans,” Folia Primatologica, vol. 66, pp. 137–159, 1996.
[182]
J. B. Hanna, S. Everett, and D. Schmitt, “Biomechanics of climbing in 4 species of prosimian, with special reference to lorises,” American Journal of Physical Anthropology, vol. 141, no. 50, p. 122, 2010.
[183]
N. Yamazaki and H. Ishida, “A biomechanical study of vertical climbing and bipedal walking in gibbons,” Journal of Human Evolution, vol. 13, no. 7, pp. 563–571, 1984.
[184]
D. Schmitt and P. Lemelin, “Locomotor mechanics of the slender loris (Loris tardigradus),” Journal of Human Evolution, vol. 47, no. 1-2, pp. 85–94, 2004.
[185]
E. E. Vereecke, K. D'Ao？t, and P. Aerts, “Speed modulation in hylobatid bipedalism: a kinematic analysis,” Journal of Human Evolution, vol. 51, no. 5, pp. 513–526, 2006.
[186]
K. Isler, “Arboreal locomotion in wild black-and-white snub-nosed monkeys (Rhinopithecus bieti),” Folia Primatologica, vol. 77, no. 3, pp. 195–211, 2006.
[187]
k. Isler, “Characteristics of vertical climbing in gibbons,” Evolutionary Anthropology, vol. 11, 1, pp. 49–52, 2002.
[188]
K. Isler, “3D-kinematics of vertical climbing in hominoids,” American Journal of Physical Anthropology, vol. 126, no. 1, pp. 66–81, 2005.
[189]
J. M. DeSilva, Vertical climbing adaptations in the anthropoid ankle and midfoot: implications for locomotion in Miocene catarrhines and Plio-pleistocene hominins, Ph.D. thesis, University of Michigan, Ann Arbor, Mich, USA, 2008.
[190]
J. M. DeSilva, “Functional morphology of the ankle and the likelihood of climbing in early hominins,” Proceedings of the National Academy of Sciences, vol. 106, pp. 6567–6572, 2009.
[191]
J. B. Hanna, “Kinematics of vertical climbing in lorises and Cheirogaleus medius,” Journal of Human Evolution, vol. 50, no. 4, pp. 469–478, 2006.
[192]
G. P. Rauwerdink, “Muscle fibre and tendon lengths in primate extremities,” in Hands of Primates, H. Preuschoft and D. J. Chivers, Eds., pp. 207–223, Springer, New York, NY, USA, 1993.
[193]
W. K. Gregory, The Anatomy of the Gorilla, Columbia University Press, New York, NY, USA, 1950.
[194]
K. L. Rafferty and C. B. Ruff, “Articular structure and function in Hylobates, Colobus, and Papio,” American Journal of Physical Anthropology, vol. 94, no. 3, pp. 395–408, 1994.
[195]
B. Demes and M. M. Günther, “Biomechanics and allometric scaling in primate locomotion and morphology,” Folia Primatologica, vol. 53, no. 1–4, pp. 125–141, 1989.
[196]
S. L. Washburn, “The analysis of primate evolution with particular reference to the origin of man,” in Origin and Evolution of Man: Cold Spring Harbor Symposia on Quantitative Biology, vol. 15, pp. 67–78, Cold Spring Harbor, New York, NY, USA, 1950.
[197]
R. H. Tuttle, “Parallelism, brachiation and hominid phylogeny,” in Phylogeny of the Primates. A Multidisciplinary Approach, W. P. Luckett and F. S. Szalay, Eds., pp. 447–480, Plenum Press, New York, NY, USA, 1975.
[198]
M. Cartmill and K. Milton, “The lorisiform wrist joint and the evolution of 'brachiating' adaptations in the Hominoidea,” American Journal of Physical Anthropology, vol. 47, no. 2, pp. 249–272, 1977.
[199]
J. H. Prost, “Origin of bipedalism,” American Journal of Physical Anthropology, vol. 52, no. 2, pp. 175–189, 1980.
[200]
J. G. Fleagle, J. T. Stern Jr, W. L. Jungers, and R. L. Susman, “Climbing: a biomechanical link with brachiation and with bipedalism,” Symposium of the Zoological Society of London, vol. 48, pp. 359–375, 1981.
[201]
R. H. Tuttle, “Evolution of hominid bipedalism and prehensile capabilities,” Philosophical Transactions of the Royal Society of London, vol. 292, pp. 89–94, 1981.
[202]
B. Senut, “Climbing as a crucial preadaptation for human bipedalism,” International Journal of Skeletal Research, vol. 14, pp. 35–44, 1988.
