International Journal of Primatology

, Volume 32, Issue 2, pp 430–444 | Cite as

Interpreting the Role of Climbing in Primate Locomotor Evolution: Are the Biomechanics of Climbing Influenced by Habitual Substrate Use and Anatomy?



Vertical climbing is widely accepted to have played an important role in the origins of both primate locomotion and of human bipedalism. Yet, only a few researchers have compared climbing mechanics in quadrupedal primates that vary in their degree of arboreality. It is assumed that primates using vertical climbing with a relatively high frequency will have morphological and behavioral specializations that facilitate efficient climbing mechanics. We test this assumption by examining whether time spent habitually engaged in climbing influences locomotor parameters such as footfall sequence, peak forces, and joint excursions during vertical climbing. Previous studies have shown that during climbing, the pronograde and semiterrestrial Macaca fuscata differs in these parameters compared to the more arboreal and highly specialized, antipronograde Ateles geoffroyi. Here, we examine whether a fully arboreal, quadrupedal primate that does not regularly arm-swing will exhibit gait and force distribution patterns intermediate between those of Macaca fuscata and Ateles geoffroyi. We collected footfall sequence, limb peak vertical forces, and 3D hindlimb excursion data for Macaca fascicularis during climbing on a stationary pole instrumented with a force transducer. Results show that footfall sequences are similar between macaque species, whereas peak force distributions and hindlimb excursions for Macaca fascicularis are intermediate between values reported for M. fuscata and Ateles geoffroyi. These results support the notion that time spent climbing is reflected in climbing mechanics, even though morphology may not provide for efficient mechanics, and highlight the important role of arboreal locomotor activity in determining the pathways of primate locomotor evolution.


Biomechanics Climbing Macaque Primate evolution Spider monkey 



We thank 2 anonymous reviewers, Dr. Joanna Setchell, and several WVSOM faculty and students for providing helpful comments. We also thank Ms. Megan Wilson for assistance with data collection and Ms. Bobbi Hoover, Mr. Bobby Lee, and Mr. Ken Moon for assistance with data preparation. This project was supported by an NSF (BCS-0749314) and WVSOM Intramural grant. All procedures approved by the WVSOM and Duke IACUCs.


  1. Ashton, E. H., & Oxnard, C. E. (1963). The musculature of the primate shoulder. Transactions of the Zoological Society of London, 29, 553–650.CrossRefGoogle Scholar
  2. Begun, D. R. (2004). Knuckle-walking and the origin of human bipedalism. In D. J. Meldrum (Ed.), From biped to strider: The emergence of modern human walking (pp. 9–33). New York: Kluwer.Google Scholar
  3. Cant, J. G. H. (1988). Positional behavior of long-tailed macaques (Macaca fascicularis) in northern Sumatra. American Journal of Physical Anthropology, 76, 29–37.PubMedCrossRefGoogle Scholar
  4. Cartmill, M. (1985). Climbing. In M. Hildebrand, D. M. Bramble, K. F. Liem, & D. B. Wake (Eds.), Functional vertebrate morphology (pp. 73–88). Cambridge: Belknap.Google Scholar
  5. Cartmill, M., Lemelin, P., & Schmitt, D. (2002). Support polygons and symmetrical gaits in mammals. Zoological Journal of the Linnean Society London, 136, 401–420.CrossRefGoogle Scholar
  6. Chatani, K. (2003). Positional behavior of free-ranging Japanese macaques (Macaca fuscata). Primates, 44, 13–23.PubMedGoogle Scholar
  7. Crompton, R. H., Vereecke, E. E., & Thorpe, S. K. S. (2008). Locomotion and posture from the common hominoid ancestor to fully modern hominins, with special reference to the last common panin/hominin ancestor. Journal of Anatomy, 212, 501–543.PubMedCrossRefGoogle Scholar
  8. Darwin, C. R. (1871). The descent of man, and selection in relation to sex. London: John Murray.CrossRefGoogle Scholar
  9. Demes, B., Fleagle, J. G., & Jungers, W. L. (1999). Takeoff and landing forces of leaping strepsirhine primates. Journal of Human Evolution, 37, 279–292.PubMedCrossRefGoogle Scholar
  10. Fleagle, J. G. (1976). Locomotion and posture of the Malayan siamang and implications for hominid evolution. Folia Primatologica, 26, 245–269.CrossRefGoogle Scholar
  11. Fleagle, J. G. (1999). Primate adaptation and evolution (2nd ed.). San Diego: Academic.Google Scholar
  12. Fleagle, J. G., & Anapol, F. C. (1992). The indriid ischium and the hominid hip. Journal of Human Evolution, 22, 285–305.CrossRefGoogle Scholar
  13. Fleagle, J. G., & McGraw, W. S. (2002). Skeletal and dental morphology of African papionins: unmasking a cryptic clade. Journal of Human Evolution, 42, 267–292.PubMedCrossRefGoogle Scholar
  14. Fleagle, J. G., & Mittermeier, R. A. (1980). Locomotor behavior, body size, and comparative ecology of seven Surinam monkeys. American Journal of Physical Anthropology, 52, 301–322.CrossRefGoogle Scholar
  15. Fleagle, J. G., Stern, J. T. J., Jungers, W. L., Susman, R. L., Vangor, A. K., & Wells, J. P. (1981). Climbing: a biomechanical link with brachiation and bipedalism. Symposia of the Zoological Society of London, 48, 359–375.Google Scholar
  16. Gebo, D. L. (1996). Climbing, brachiation, and terrestrial quadrupedalism: historical precursors of hominid bipedalism. American Journal of Physical Anthropology, 101(1), 55–92.PubMedCrossRefGoogle Scholar
  17. Grand, T. I. (1977). Body weight: its relation to tissue composition, segment distribution, and motor function. I. Interspecific comparisons. American Journal of Physical Anthropology, 47, 211–248.PubMedCrossRefGoogle Scholar
  18. Hanna, J. B. (2006). Kinematics of vertical climbing in lorises and Cheirogaleus medius. Journal of Human Evolution, 50, 469–478.PubMedCrossRefGoogle Scholar
  19. Hanna, J. B., Everett, S., & Schmitt, D. (2010). Biomechanics of climbing in 4 species of prosimian, with special reference to lorises. American Journal of Physical Anthropology, 151(S50), 122.Google Scholar
  20. Hanna, J. B., Griffin, T. M., & Schmitt, D. (2008). The energetic cost of climbing in primates. Science, 320(5878), 898.PubMedCrossRefGoogle Scholar
  21. Hildebrand, M. (1967). Symmetrical gaits of primates. American Journal of Physical Anthropology, 26, 119–130.CrossRefGoogle Scholar
  22. Hirasaki, E., Kumakura, H., & Matano, S. (1993). Kinesiological characteristics of vertical climbing in Ateles geoffroyi and Macaca fuscata. Folia Primatologica, 61, 148–156.CrossRefGoogle Scholar
  23. Hirasaki, E., & Matano, S. (1996). Comparison of locomotor patterns and the cerebellar complex in Ateles and Macaca. Folia Primatologica, 66, 209–225.CrossRefGoogle Scholar
  24. Hirasaki, E., Matano, S., Nakano, Y., & Ishida, H. (1992). Vertical climbing in Ateles geoffroyi and Macaca fuscata and its comparative neurological background. In S. Matano, R. H. Tuttle, H. Ishida, & M. Goodman (Eds.), Evolutionary biology, reproductive endocrinology, and virology (pp. 156–165). Tokyo: University of Tokyo Press.Google Scholar
  25. Hoelzer, G. A., & Melnick, D. J. (1996). Evolutionary relationships of the macaques. In J. E. Lindberg (Ed.), Evolution and ecology of macaque societies (pp. 3–19). New York: Cambridge University Press.Google Scholar
  26. Isler, K. (2002). Characteristics of vertical climbing in gibbons. Evolutionary Anthropology, 11, 49–52.CrossRefGoogle Scholar
  27. Isler, K. (2004). Footfall patterns, stride length and speed of vertical climbing in spider monkeys (Ateles fusciceps robustus) and woolly monkeys (Lagothrix lagotricha). Folia Primatologica, 75(3), 133–149.CrossRefGoogle Scholar
  28. Isler, K. (2005). 3D-kinematics of vertical climbing in hominoids. American Journal of Physical Anthropology, 126, 66–81.PubMedCrossRefGoogle Scholar
  29. Isler, K., & Grueter, C. C. (2006). Arboreal locomotion in wild black-and-white snub-nosed monkeys (Rhinopithecus bieti). Folia Primatologica, 77, 195–211.CrossRefGoogle Scholar
  30. Isler, K., & Thorpe, S. K. S. (2003). Gait parameters in vertical climbing of captive, rehabilitant and wild Sumatran orang-utans (Pongo pygmaeus abelii). Journal of Experimental Biology, 206, 4081–4096.PubMedCrossRefGoogle Scholar
  31. Larson, S. G. (1993). Functional morphology of the shoulder in primates. In D. Gebo (Ed.), Postcranial adaptation in nonhuman primates (pp. 45–69). DeKalb: NIU.Google Scholar
  32. Larson, S. G. (1998a). Unique aspects of quadrupedal locomotion in nonhuman primates. In E. Strasser, J. G. Fleagle, A. Rosenberger, & H. McHenry (Eds.), Primate locomotion: Recent advances (pp. 157–173). New York: Plenum.Google Scholar
  33. Larson, S. G. (1998b). Parallel evolution in the hominoid trunk and forelimb. Evolutionary Anthropology, 6, 87–99.CrossRefGoogle Scholar
  34. Larson, S. G., Schmitt, D., Lemelin, P., & Hamrick, M. (2001). Limb excursion during quadrupedal walking: how do primates compare to other mammals? Journal of Zoology, 255, 353–365.CrossRefGoogle Scholar
  35. Larson, S. G., & Stern, J. T. (2006). Maintenance of above-branch balance during primate arboreal quadrupedalis: Coordinated use of forearm rotators and tail motion. American Journal of Physical Anthropology, 129, 71–81.PubMedCrossRefGoogle Scholar
  36. Lovejoy, C. O., Simpson, S. W., White, T. D., Asfaw, B., & Suwa, G. (2009). Careful climbing in the Miocene: the forelimbs of Ardipithecus ramidus and humans are primitive. Science, 326, 70–77.CrossRefGoogle Scholar
  37. Lovejoy, C. O., Suwa, G., Spurlock, L., Asfaw, B., & White, T. D. (2009). The pelvis and femur of Ardipithecus ramidus: the emergence of upright walking. Science, 326, 78–83.Google Scholar
  38. Nakatsukasa, M. (2004). Acquisition of bipedalism: the Miocene hominoid record and modern analogues for bipedal protohominids. Journal of Anatomy, 204, 385–402.PubMedCrossRefGoogle Scholar
  39. Plavcan, J. M., & van Schaik, C. P. (1997). Intrasexual competition and body weight dimorphism in anthropoid primates. American Journal of Physical Anthropology, 103, 37–68.PubMedCrossRefGoogle Scholar
  40. Preuschoft, H. (2004). Mechanisms for the acquisition of habitual bipedality: Are there biomechanical reasons for the acquisition of upright bipedal posture? Journal of Anatomy, 204, 363–384.PubMedCrossRefGoogle Scholar
  41. Richmond, B. G., Begun, D. R., & Strait, D. S. (2001). Origin of human bipedalism: the knuckle-walking hypothesis revisited. Yearbook of Physical Anthropology, 44, 70–105.CrossRefGoogle Scholar
  42. Rodman, P. S. (1979). Skeletal differentiation of Macaca fascicularis and Macaca nemestrina in relation to arboreal and terrestrial quadrupedalism. American Journal of Physical Anthropology, 51, 51–62.CrossRefGoogle Scholar
  43. Rose, M. D. (1989). New postcranial specimens of catarrhines from the middle Miocene Chinji formation, Pakistan: descriptions and a discussion of proximal humeral functional morphology in anthropoids. Journal of Human Evolution, 18, 131–162.CrossRefGoogle Scholar
  44. Rose, M. D. (1991). The process of bipedalization in hominoids. In Y. Coppens & B. Senut (Eds.), Origine(s) de la bipedie chez les hominides (pp. 37–49). Paris: CNRS.Google Scholar
  45. Schmitt, D. (2003). Insights into the evolution of human bipedalism from experimental studies of humans and other primates. Journal of Experimental Biology, 206(9), 1437–1448.PubMedCrossRefGoogle Scholar
  46. Schoonaert, K., D’Aout, K., & Aerts, P. (2006). A dynamic force analysis system for climbing of large primates. Folia Primatologica, 77, 246–254.CrossRefGoogle Scholar
  47. Shinoda, K. (1994). Allometry of the long bones of closely related macaques. Anthropological Science, 102(Supplement), 11–25.Google Scholar
  48. Stern, J. T. (1971). Functional morphology of the hip and thigh of cebid monkeys and its implications for the evolution of erect posture. Basel: Karger.Google Scholar
  49. Stern, J. T. (1975). Before bipedality. Yearbook of Physical Anthropology, 19, 59–68.Google Scholar
  50. Stern, J. T. (2000). Climbing to the top: a personal memoir of Australopithecus afarensis. Evolutionary Anthropology, 9, 113–133.CrossRefGoogle Scholar
  51. Stern, J. T., & Susman, R. L. (1981). Electromyography of the gluteal muscles in Hylobates, Pongo, and Pan—implications for the evolution of hominid bipedality. American Journal of Physical Anthropology, 55(2), 153–166.CrossRefGoogle Scholar
  52. Steudel, K. (1981). Functional aspects of primate pelvic structure: a multivariate approach. American Journal of Physical Anthropology, 55, 399–410.PubMedCrossRefGoogle Scholar
  53. Steudel, K. (1984). Patterns of allometry in the pelvis of higher primates. Journal of Human Evolution, 13, 545–554.CrossRefGoogle Scholar
  54. Thorpe, S. K. S., Holder, R. L., & Crompton, R. H. (2007). Origin of human bipedalism, as an adaptation for locomotion on flexible branches. Science, 316, 1328–1331.PubMedCrossRefGoogle Scholar
  55. Vangor, A. K. (1979). Electromyography of gait in non-human primates and its significance for the evolution of bipedality. Ph.D. thesis. State University of New York, Stony Brook.Google Scholar
  56. Vilensky, J. A., Moore, A. M., & Libii, J. N. (1994). Squirrel monkey locomotion on an inclined treadmill: implications for the evolution of gaits. Journal of Human Evolution, 26, 375–386.CrossRefGoogle Scholar
  57. Youlatos, D. (1996). Atelines, apes and wrist joints. Folia Primatologica, 67, 193–198.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  1. 1.Department of Biomedical SciencesWest Virginia School of Osteopathic MedicineLewisburgUSA
  2. 2.Department of Evolutionary AnthropologyDuke UniversityDurhamUSA

Personalised recommendations