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Unique Aspects of Quadrupedal Locomotion in Nonhuman Primates

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Primate Locomotion

Abstract

Quadrupedal walking and running are certainly not the first things that come to mind when one considers unique aspects of primate locomotion. However, there is a growing body of information about how the form of quadrupedalism displayed by primates differs from that of nonprimate mammals (see Vilensky, 1987, 1989). One of the most distinctive characteristics of primate quadrupedalism is that they typically utilize a diagonal sequence/diagonal couplets walking gait pattern (i.e., foot falls in sequence: left hind, right fore, right hind, left fore, with diagonal limbs moving as a pair), in contrast to the almost universally employed lateral sequence walking gait (left hind, left fore, right hind, right fore) of nonprimate mammals (Howell, 1944; Prost, 1965, 1969; Hildebrand, 1967; Rollinson and Martin, 1981; Vilensky, 1989; Vilensky and Larson, 1989). This difference in gait pattern is not trivial, since a diagonal sequence/diagonal couplet walking gait creates a strong potential for interference between the ipsilateral hind and forelimbs (Figure 1). The potential for hind/forelimb interference is exacerbated in primates by their long limbs (due to their relatively longer limb bones, Alexander et al., 1979), and by their propensity to use relatively longer stride lengths than nonprimate quadrupeds (Vilensky, 1980; Alexander and Maloiy, 1984; Reynolds, 1987). As a result, many primate quadrupeds must regularly “overstride” during walking, that is, touch down with their hind foot ahead of their ipsilateral hand by passing it either “inside” or “outside” of the forelimb (Hildebrand, 1967; Reynolds, 1985b; Larson and Stern, 1987; see Figure 1). Another distinctive aspect of primate gait utilization is the infrequent use of a running trot (defined as diagonal limbs moving synchronously with relative stance duration of each limb less than 50%; see Hildebrand, 1967).

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References

  • Alexander R McN (1991) Elastic mechanisms in primate locomotion. Z. Morph. Anthrop. 78:315–320.

    CAS  Google Scholar 

  • Alexander R McN, Jayes AS, Maloiy GMO, and Wathuta EM (1979) Allometry of the limb bones of mammals from shrews (Sorex) to elephant (Loxodonta). J. Zool., Lond. 189:305–314.

    Article  Google Scholar 

  • Alexander R McN, and Maloiy GMO (1984) Stride lengths and stride frequencies of primates. J. Zool., Lond. 202:577–582.

    Article  Google Scholar 

  • Biewener AA (1983) Allometry of quadrupedal locomotion: The scaling of duty factor, bone curvature and limb orientation to body size. J. exp. Biol. 105:147–171.

    PubMed  CAS  Google Scholar 

  • Biewener AA (1989) Scaling body support in mammals: Limb posture and muscle mechanics. Science 245:45–48.

    Article  PubMed  CAS  Google Scholar 

  • Biewener AA(1990) Biomechanics of mammalian terrestrial locomotion. Science 250:1097–1103.

    Google Scholar 

  • Blickhan R (1989) The spring-mass model for running and hopping. J. Biomech. 22:1217–1227.

    Article  PubMed  CAS  Google Scholar 

  • Cartmill M (1974) Pads and claws in arboreal locomotion. In FA Jenkins Jr. (ed.): Primate Locomotion. New York: Academic Press, pp. 45–83.

    Google Scholar 

  • Cartmill M (1985) Climbing. In M Hildebrand, DM Bramble, KF Liem, and DB Wake (eds.): Functional Vertebrate Morphology. Cambridge: Belknap Press, pp. 73–88.

    Google Scholar 

  • Dagg AI (1974) Running, Walking and Jumping. London: Wykeham.

    Google Scholar 

  • Demes B, Jungers WL, and Nieschalk U (1990) Size-and speed-related aspects of quadrupedal walking in slender and slow lorises. In FK Jouffroy, MH Stack, and C Niemitz (eds.): Gravity, Posture and Locomotion in Primates. Firenze: II Sedicesimo, pp. 175–197.

    Google Scholar 

  • Demes B, Larson SG, Stern JT Jr., and Jungers WL (1992) The hindlimb drive of primates — theoretical reconsideration and empirical examination of a widely held concept. Am. J. Phys. Anthropol. Suppl. 14:69.

    Google Scholar 

  • Demes B, Larson SG, Stern JT Jr., Jungers WL, Biknevicius AR, and Schmitt D (1994) The kinetics of “hind limb drive” reconsidered. J. Hum. Evol. 26:353–374.

    Article  Google Scholar 

  • Dial KP, Goslow GE Jr., and Jenkins FA Jr. (1991) The functional anatomy of the shoulder in the European starling (Stunus vulgaris). J. Morph. 207:327–344.

    Article  Google Scholar 

  • Dial KP, Kaplan SR, Goslow GE Jr., and Jenkins FA Jr. (1987) Structure and neural control of the pectoralis in pigeons: implications for flight mechanics. Anat. Rec. 218:284–287.

    Article  PubMed  CAS  Google Scholar 

  • Dunbar RIM, and Dunbar EP (1974) Ecological relations and niche separation between sympatric terrestrial primates in Ethiopia. Folia Primatol. 21:36–60.

    Article  PubMed  CAS  Google Scholar 

  • Dykyj D (1980) Locomotion of the slow loris in a designed substrate context. Am. J. Phys. Anthropol. 52:577–586.

    Article  Google Scholar 

  • Eaton TH Jr. (1944) Modification of the shoulder girdle related to reach and stride in mammals. J. Morph. 75:167–171.

    Article  Google Scholar 

  • Eidelberg E, Waiden JG, and Nguyen LH (1981) Locomotor control in macaque monkeys. Brain 104:647–663.

    Article  PubMed  CAS  Google Scholar 

  • English AW (1978a) Functional analysis of the shoulder girdle of cats during locomotion. J. Morph. 156:279–292.

    Article  PubMed  CAS  Google Scholar 

  • English AW (1978b) An electromyographic analysis of forelimb muscles during overground stepping in the cat. J. exp. Biol. 76:105–122.

    PubMed  CAS  Google Scholar 

  • Farley CT, Glasheen J, and McMahon TA (1993) Running springs: Speed and animal size. J. exp. Biol. 185:71–86.

    PubMed  CAS  Google Scholar 

  • Fedigan L, and Fedigan LM (1988) Cercopithecus aethiops: A review of field studies. In A Gautier-Hion, F Bourliere, J Gautier (eds.): A Primate Radiation: Evolutionary Biology of the African Guenons. Cambridge: Cambridge Univ. Press, pp. 389–411.

    Google Scholar 

  • Fischer MS (1994) Crouched posture and high fulcrum, a principle in the locomotion of small mammals: The example of the rock hyrax (Procavia capensis) (Mammalia: Hyracoidea). J. Hum. Evol. 26:510–524.

    Article  Google Scholar 

  • Fleagle JG (1978) Locomotion, posture and habitat use of two sympatric leaf-monkeys in West Malaysia. In DJ Chivers and J Herbert (eds.): Recent Advances in Primatology, Vol. 1, behavior. New York: Academic Press, pp. 331–336.

    Google Scholar 

  • Georgopoulos AP, and Grillner S (1989) Visuomotor coordination in reaching and locomotion. Science 245:1209–1210.

    Article  PubMed  CAS  Google Scholar 

  • Goslow GE Jr., Dial KP, and Jenkins FA Jr. (1989) The avian shoulder: An experimental approach. Amer. Zool. 29:287–301.

    Google Scholar 

  • Grand T (1968a) Functional anatomy of the lower limb of the howler monkey (Alouatta caraya). Am. J. Phys. Anthropol. 28:163–181.

    Article  PubMed  CAS  Google Scholar 

  • Grand T (1968b) Functional anatomy of the upper limb. In: Biology of the Howler Monkey (Alouatta caraya). Bibl. Primat., No. 7, Basel: Karger, pp. 104–125.

    Google Scholar 

  • Grand T (1984) Motion economy within the canopy: Four strategies for mobility. In P Rodman and JGH Cant (eds.): Adaptations for Foraging in Nonhuman Primates: Contributions to an Organismal Biology of Prosimians, Monkeys and Apes. New York: Columbia Univ. Press, pp. 54–72.

    Google Scholar 

  • Heglund NC, Taylor CR, and McMahon TA (1974) Scaling stride frequency and gait to animal size: Mice to horses. Science 186:1112–1113.

    Article  PubMed  CAS  Google Scholar 

  • Hildebrand M (1967). Symmetrical gaits of primates. Am. J. Phys. Anthropol. 26:119–130.

    Article  Google Scholar 

  • Hildebrand M (1988) Analysis of Vertebrate Structure, 3rd Ed. New York: John Wiley and Sons.

    Google Scholar 

  • Howell AB (1944) Speed in Animals. Chicago: Univ. Chicago Press.

    Google Scholar 

  • Ishida H, Jouffroy FK, and Nakano Y (1990) Comparative dynamics of pronograde and upside down horizontal quadrupedalism in the slow loris (Nycticebus coucang). In FK Jouffroy, MH Stack, and C Niemitz (eds.): Gravity, Posture and Locomotion in Primates. Firenze: II Sedicesimo, pp. 209–220.

    Google Scholar 

  • Iwamoto M, and Tomita M (1966) On the movement order of four limbs while walking and the body weight distribution to fore and hind limbs while standing on all fours in monkeys. J. Anthropol. Soc. Nippon 74:228–231.

    Article  Google Scholar 

  • Jenkins FA Jr. (1971) Limb posture and locomotion in the Virginia opossum (Didelphis marsupialis) and in other non-cursorial mammals. J. Zool., Lond. 165:303–315.

    Article  Google Scholar 

  • Jenkins FA Jr. (1974) The movement of the shoulder in claviculate and aclaviculate mammals. J. Morph. 144:71–83.

    Article  Google Scholar 

  • Jenkins FA Jr., and Goslow GE Jr. (1983) The functional anatomy of the shoulder of the savanna monitor lizard (Varanus exanthematicus). J. Morph. 175:195–216.

    Article  Google Scholar 

  • Jenkins FA Jr., and Weijs WA (1979) The functional anatomy of the shoulder in the Virginia opossum (Didelphis virginiana). J. Zool., Lond. 188:379–410.

    Article  Google Scholar 

  • Jouffroy FK, and Petter A (1990) Gravity-related kinematic changes in lorisine horizontal locomotion in relation to position of the body. In FK Jouffroy, MH Stack, and C Niemitz (eds.): Gravity, Posture and Locomotion in Primates. Firenze: II Sedicesimo, pp. 199–208.

    Google Scholar 

  • Jouffroy FK, Renous S, and Gasc JP (1983) Etude cinéradiographique des déplacements du membre antérieur du Potto de Bosman (Perodicticus potto) au cours de la marche quadrupède sur une branche horizontale. Ann. Sc. Nat. Zool. 13ème sér. 5:75–87.

    Google Scholar 

  • Jungers WL (1985) Body size and scaling of limb proportions in primates. In WL Jungers (ed.): Size and Scaling in Primate Biology. New York: Plenum Press, pp. 345–381.

    Google Scholar 

  • Jungers WL, Jouffroy FK, and Stern JT Jr. (1980) Gross structure and function of the quadriceps femoris in Lemur fulvus: An analysis based on telemetered electromyography. J. Morph. 164:287–299.

    Article  PubMed  CAS  Google Scholar 

  • Kimura T(1985) Bipedal and quadrupedal walking of primates: Comparative dynamics. In S Kondo (ed.): Primate Morphophysiology, Locomotor bAnalyses and Human Bipedalism. Tokyo: Univ. of Tokyo Press, pp. 81–104.

    Google Scholar 

  • Kimura T, Okada M, and Ishida H (1979) Kinesiological characteristics of primate walking: Its significance in human walking. In ME Morbeck, H Preuschoft, and N Gomberg (eds.): Environment, Behavior, and Morphology: Dynamic Interactions in Primates. New York: Gustav Fischer, pp. 297–311.

    Google Scholar 

  • Kram R, and Taylor CR (1990) Energetics of running: A new perspective. Nature 346:265–267.

    Article  PubMed  CAS  Google Scholar 

  • Larson SG, and Stern JT Jr. (1987) EMG of chimpanzee shoulder muscles during knuckle-walking: Problems of terrestrial locomotion in a suspensory adapted primate. J. Zool. Lond. 212:629–655.

    Article  Google Scholar 

  • Larson SG, and Stern JT Jr. (1989a) The role of supraspinatus in the quadrupedal locomotion of vervets (Cercopithecus aethiops): Implications for interpretation of humeral morphology. Am. J. Phys. Anthropol. 79:369–377.

    Article  PubMed  CAS  Google Scholar 

  • Larson SG, and Stern JT Jr. (1989b) The role of propulsive muscles of the shoulder during quadrupedal ism in vervet monkeys (Cercopithecus aethiops): Implications for neural control of locomotion in primates. J. Motor behavior 21:457–472.

    CAS  Google Scholar 

  • Lemelin P (1996) The evolution of manual prehensility in primates: A comparative and functional analysis in prosimian primates and didelphid marsupials. Ph.D. Dissertation, State University of New York at Stony Brook.

    Google Scholar 

  • McMahon TA (1975) Using body size to understand the structural design of animals: Quadrupedal locomotion. J. Appl. Physiol. 39:619–627.

    PubMed  CAS  Google Scholar 

  • McMahon TA (1984) Muscles, Reflexes and Locomotion. Princeton: Princeton Univ. Press.

    Google Scholar 

  • McMahon TA (1985) The role of compliance in mammalian running gaits. J. exp. Biol. 115:263–282.

    PubMed  CAS  Google Scholar 

  • McMahon TA, Valiant G, and Frederick EC (1987) Groucho running. J. Appl. Physiol. 62:2326–2337.

    PubMed  CAS  Google Scholar 

  • Meldrum DJ (1991) Kinematics of the cercopithecine foot on arboreal and terrestrial substrates with implications for the interpretation of hominid terrestrial adaptations. Am. J. Phys. Anthropol. 84:273–290.

    Article  PubMed  CAS  Google Scholar 

  • Miller S, and Van der Meché FGA (1975) Movements of the forelimbs of the cat during stepping on a treadmill. Brain Res. 91:255–269.

    Article  PubMed  CAS  Google Scholar 

  • Morbeck ME (1979) Forelimb use and positional adaptation in Colobus guereza: Integration of behavioral, ecological and anatomical data. In M Morbeck, H Preuschoft, and N Gomberg (eds.): Environment, Behavior, and Morphology: Dynamic Interactions in Primates. New York: Gustav Fisher, pp. 95–118.

    Google Scholar 

  • Muybridge E (1957) Animals in Motion. In LS Brown (ed.): Animals in Motion. New York: Dover. (Originally published by Chapman and Hall, London, 1899)

    Google Scholar 

  • Napier JR (1967) Evolutionary aspects of primate locomotion. Am. J. Phys. Anthropol. 27:333–342.

    Article  PubMed  CAS  Google Scholar 

  • Nomura S, Sawazake H, and Ibaraki T (1966) Co-operated muscular action in postural adjustment and motion in dog, from the viewpoint of electromyographic kinesiology and joint mechanics. IV. About muscular activity in walking and trot. Jap. J. Zootech. Sci. 37:221–229.

    Google Scholar 

  • Okada M, Kimura T, Ishida H, and Kondo S (1978) Biomechanical aspects of primate quadrupedal ism. In E Asmussen and K Jørgensen (eds.): Biomechanics 6A. Baltimore: Univ. Part Press, pp. 119–124.

    Google Scholar 

  • Pandy MG, Kumar V, Berme N, Waldron KJ (1988) The dynamics of quadrupedal locomotion. J. Biomech. Engr. 110:230–237.

    Article  CAS  Google Scholar 

  • Peters SE, and Goslow GE Jr. (1983) From salamanders to mammals: Continuity in musculoskeletal function during locomotion. Brain Behav. Evol. 22:191–197.

    Article  PubMed  CAS  Google Scholar 

  • Preuschoft H, and Gunther MM (1994) Biomechanics and body shape in primates compared to horses. Z. Morph. Anthropol. 80:149–165.

    Google Scholar 

  • Preuschoft H, Witte H, Christian A, and Fischer M (1996) Size influences on primate locomotion and body shape, with special emphasis on the locomotion of’ small mammals.’ Folia Primatol. 66:93–112.

    Article  PubMed  CAS  Google Scholar 

  • Prost JH (1965) The methodology of gait analysis and gaits of monkeys. Am. J. Phys. Anthropol. 23:215–240.

    Article  PubMed  CAS  Google Scholar 

  • Prost JH (1969) A replication study on monkey gaits. Am. J. Phys. Anthropol. 30:203–208.

    Article  Google Scholar 

  • Reynolds TR (1985a) Mechanics of increased support of weight by the hindlimbs in primates. Am. J. Phys. Anthropol. 67:335–349.

    Article  PubMed  CAS  Google Scholar 

  • Reynolds TR (1985b) Stresses on the limbs of quadrupedal primates. Am. J. Phys. Anthropol. 67:351–362.

    Article  PubMed  CAS  Google Scholar 

  • Reynolds TR (1987) Stride length and its determinants in humans, early hominids, primates, and mammals. Am. J. Phys. Anthropol. 72:101–116.

    Article  PubMed  CAS  Google Scholar 

  • Rollinson J. and Martin RD (1981) Comparative aspects of primate locomotion, with special reference to arboreal cercopithecines. In MH Day (ed.): Vertebrate Locomotion. Symposia of the Zoological Society of London, No. 48. London: Academic Press, pp. 377–427.

    Google Scholar 

  • Rose MD (1979) Positional behavior of natural populations: Some quantitative results of a field study of Colobus guereza and Cercopithecus aethiops. In ME Morbeck, H Preuschoft, and N Gomberg (eds.): Environment, Behavior, and Morphology: Dynamic Interactions in Primates. New York: Gustav Fischer, pp. 74–93.

    Google Scholar 

  • Schmitt D (1994) Forelimb mechanics as a function of substrate type during quadrupedal ism in two anthropoid primates. J. Hum. Evol. 26:441–457.

    Article  Google Scholar 

  • Schmitt D (1995) A kinematic and kinetic analysis of forelimb use during arboreal and terrestrial quadrupedalism in Old World monkeys. Ph.D. Dissertation, State University of New York at Stony Brook.

    Google Scholar 

  • Schmitt D, and Larson SG (1994) Heel contact as a function of substrate type and speed in primates. Am. J. Phys. Anthropol. 96:39–50.

    Article  Google Scholar 

  • Smith JM, and Savage RJG (1956) Some locomotor adaptations in mammals. J. Linn. Soc. (Zool.) 42:603–622.

    Article  Google Scholar 

  • Stern JT Jr., Wells JP, Vangor AK, and Fleagle JG (1977) Electromyography of some muscles of the upper limb in Ateles and Lagothrix. Yrbk. Phys. Anthropol. 20:98–507.

    Google Scholar 

  • Steudel K (1994) Locomotor energetics and hominid evolution. Evol. Anthropol. 3:42–48.

    Article  Google Scholar 

  • Struhsaker TT (1967) Ecology of vervet monkeys (Cercopithecus aethiops) in the Masai-Ambesoli Game Reserve, Kenya. Ecology 48:891–094.

    Article  Google Scholar 

  • Tokuriki M (1973) Electromyographic and joint-mechanical studies in quadrupedal locomotion. I. Walk. Jap. J. Vet. Sci. 35:433–448.

    Article  CAS  Google Scholar 

  • Tomita M (1967) A study on the movement patterns of four limbs in walking. 1. Observation and discussion on the two types of the movement order of four limbs seen in mammals while walking. J. Anthropol. Soc. Nippon 75:120–146.

    Article  Google Scholar 

  • Vangor A, and Wells JP (1983) Muscle recruitment and the evolution of bipedality: Evidence from telemetered electromyography of spider, woolly, and patas monkeys. Ann. Sci. Nat., Zool., Paris, Ser. 13 5:125–136.

    Google Scholar 

  • Viala D, and Vidal C (1978) Evidence for distinct spinal locomotion generators supplying respectively fore-and hindlimbs in the rabbit. Brain Res. 155:182–186.

    Article  PubMed  CAS  Google Scholar 

  • Vilensky JA (1980) Trot-gallop transition in a macaque. Am. J. Phys. Anthropol. 53:347–348.

    Article  Google Scholar 

  • Vilensky JA (1987) Locomotor behavior and control in human and nonhuman primates: comparisons with cats and dogs. Neurosci. Biobehav. Rev. 11:263–274.

    Article  PubMed  CAS  Google Scholar 

  • Vilensky JA (1989) Primate quadrupedalism: How and why does it differ from that of typical quadrupeds. Brain Behav. Evol. 34:357–364.

    Article  PubMed  CAS  Google Scholar 

  • Vilensky JA, Gankiewicz E, and Townsend DW (1988) Effects of size on vervet (Cercopithecus aethiops) gait parameters: A cross-sectional approach. Am. J. Phys. Anthropol. 76:463–480.

    Article  Google Scholar 

  • Vilensky JA, Gankiewicz E, and Townsend DW (1990) Effects of size on vervet (Cercopithecus aethiops) gait parameters: A longitudinal approach. Am. J. Phys. Anthropol. 81:429–439.

    Article  PubMed  CAS  Google Scholar 

  • Vilensky JA, and Larson SG (1989) Primate locomotion: Utilization and control of symmetrical gaits. Ann. Rev. Anthropol. 18:17–35.

    Article  Google Scholar 

  • Vilensky JA, Moore AM, and Libii JN (1994) Squirrel monkey locomotion on an inclined treadmill: Implications for the evolution of gaits. J. Hum. Evol. 26:375–386.

    Article  Google Scholar 

  • Whitehead PF, and Larson SG (1994) Shoulder motion during quadrupedal walking in Cercopithecus aethiops: Integration of cineradiographic and electromyographic data. J. Hum. Evol. 26:525–544.

    Article  Google Scholar 

  • Wood Johns F (1926) The Arboreal Man. New York: Hafner.

    Google Scholar 

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Larson, S.G. (1998). Unique Aspects of Quadrupedal Locomotion in Nonhuman Primates. In: Strasser, E., Fleagle, J.G., Rosenberger, A.L., McHenry, H.M. (eds) Primate Locomotion. Springer, Boston, MA. https://doi.org/10.1007/978-1-4899-0092-0_10

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