Journal of Mammalian Evolution

, Volume 22, Issue 3, pp 435–450 | Cite as

Adjustments of Limb Mechanics in Cotton-top Tamarins to Moderate and Steep Support Orientations: Significance for the Understanding of Early Primate Evolution

  • Bettina Hesse
  • John A. Nyakatura
  • Martin S. Fischer
  • Manuela Schmidt
Original Paper


Early primate evolution is connected to the efficient exploitation of the terminal branch habitat. Mammals that forage in this habitat constantly encounter flexible thin branches that bend under the weight of the animals and thus form steeply inclined and declined supports. This study was aimed to gain insight into how cotton-top tamarins – a previously proposed modern analogue for a hypothetical stage in early primate evolution with prehensile autopodia – meet the specific functional demands when navigating thin, branch-like supports of different orientation. X-ray motion analysis was combined with synchronous single limb substrate reaction force measurements to discern limb mechanical adjustments. Previously reported gait parameter adjustments were confirmed for moderate support orientations, but on the steepest inclines and declines kinematic discontinuities were observed. These are interpreted to emphasize the functional roles of the forelimbs (net-braking role) and hind limbs (net-propulsive role) already established for level and moderately inclined supports. Tensile forces were exerted by the forelimbs on the steepest inclines and by the hind limbs on the steepest declines (head-first descents). Even though non-specialized small mammals have also been shown to successfully negotiate similar supports, prehensility offers advantages for foraging on thin, steeply inclined and declined terminal branches. Thus, the evolution of prehensile autopodia in small early primates likely has enhanced the exploitation of the terminal branch habitat.


X-ray motion analysis Force measurement Saguinus oedipus Primate Locomotion 



The experimental setup was developed by André Schmidt, Jörg Mämpel, and Sebastian Köring and was used in previous studies. We thank Rommy Petersohn for technical assistance and Sandra Clemens, Marlen Hinz, Johanna Neufuß, and Gabriele Unterhitzenberger for help with animal keeping. We also thank the reviewers and John Wible for their help to improve the manuscript. This study was funded by the Federal Ministry of Education and Research (BMBF, Fkz 01RI0633).


  1. Andrada E, Mämpel J, Schmidt A, Fischer MS, Karguth A, Witte H (2013) From biomechanics of rats’ inclined locomotion to a climbing robot. Int J Des Nat Ecodyn 8:191–212Google Scholar
  2. Arms A, Voges D, Fischer MS, Preuschoft H (2002) Arboreal locomotion in small New-World monkeys. Z Morphol Anthropol 83:243–263PubMedGoogle Scholar
  3. Birn-Jeffery AV, Higham TE (2014) The scaling of uphill and downhill locomotion in legged animals. Integr Comp Biol doi:  10.1093/icb/icu015 PubMedGoogle Scholar
  4. Bloch JI, Boyer DM (2002) Grasping primate origins. Science 298:1606–1610PubMedCrossRefGoogle Scholar
  5. Carlson-Kuhta P, Trank TV, Smith JL (1998) Forms of forward quadrupedal locomotion. II. A comparison of posture, hindlimb kinematics, and motor patterns for upslope and level walking. J Neurophysiol 79:1687–1701PubMedGoogle Scholar
  6. Cartmill M (1974) Rethinking primate origins. Science 184:436–443PubMedCrossRefGoogle Scholar
  7. Cartmill M (1985) Climbing. In: Hildebrand M, Bramble DM, Liem KF, Wake DB (eds) Functional Vertebrate Morphology. Harvard University Press, Cambridge, pp 73–88Google Scholar
  8. Cartmill M, Lemelin P, Schmitt D (2002) Support polygons and symmetrical gaits in mammals. Zool J Linn Soc 136:401–420CrossRefGoogle Scholar
  9. Delciellos AC, Vieira MV (2006) Arboreal walking performance in seven didelphid marsupials as an aspect of their fundamental niche. Austral Ecol 31:449–457CrossRefGoogle Scholar
  10. Demes B, Larson SG, Stern JT Jr, Jungers WL, Biknevicius AR, Schmitt D (1994) The kinetics of primate quadrupedalism: “hindlimb drive” reconsidered. J Hum Evol 26:353–374CrossRefGoogle Scholar
  11. Dunbar DC, Badam GL (2000) Locomotion and posture during terminal branch feeding. Int J Primatol 21:649–669CrossRefGoogle Scholar
  12. Fischer MS, Krause C, Lilje KE (2010). Evolution of chameleon locomotion, or how to become arboreal as a reptile. Zoology 113:67–74PubMedCrossRefGoogle Scholar
  13. Fischer MS, Schilling N, Schmidt M, Haarhaus D, Witte H (2002) Basic limb kinematics of small therian mammals. J Exp Biol 205:1315–1338PubMedGoogle Scholar
  14. Garber PA (1980) Locomotor behavior and feeding ecology of the Panamanian tamarin (Saguinus oedipus geoffroyi, Callitrichidae, Primates). Int J Primatol 1:185–201CrossRefGoogle Scholar
  15. Gebo DL (2004) A shrew‐sized origin for primates. Am J Phys Anthropol 125:40–62CrossRefGoogle Scholar
  16. Hershkovitz P (1977) Living New World Monkeys (Platyrrhini). University of Chicago Press, ChicagoGoogle Scholar
  17. Hildebrand M (1966) Analysis of the symmetrical gaits of tetrapods. Folio Biotheor 6:9–22Google Scholar
  18. Jenkins FA Jr (1974) Tree shrew locomotion and the origins of primate arborealism. In: Jenkins FA Jr (ed) Primate Locomotion. Academic Press, New York, pp 85–115Google Scholar
  19. Jenkins FA Jr, McClearn D (1984) Mechanisms of hind foot reversal in climbing mammals. J Morphol 182:197–219Google Scholar
  20. Kimura T, Okada M, Ishida H (1979) Kinesiological characteristics of primate walking: its significance in human walking. In: Morbeck ME, Preuschoft H, Gomberg N (eds) Environment, Behavior, and Morphology: Dynamic Interactions in Primates. Gustav Fischer, Stuttgart, pp 73–88Google Scholar
  21. Lammers AR (2007) Locomotor kinetics on sloped arboreal and terrestrial substrates in a small quadrupedal mammal. Zoology 110:93–103PubMedCrossRefGoogle Scholar
  22. Lammers AR, Biknevicius AR (2004) The biodynamics of arboreal locomotion: the effects of substrate diameter on locomotor kinetics in the gray short-tailed opossum (Monodelphis domestica). J Exp Biol 207:4325–4336PubMedCrossRefGoogle Scholar
  23. Lammers AR, Earls KD, Biknevicius AR (2006) Locomotor kinetics and kinematics on inclines and declines in the gray short-tailed opossum Monodelphis domestica. J Exp Biol 209:4154–4166PubMedCrossRefGoogle Scholar
  24. Lammers AR, Gauntner T (2008) Mechanics of torque generation during quadrupedal arboreal locomotion. J Biomech 41:2388–2395PubMedCrossRefGoogle Scholar
  25. Lemelin P, Cartmill M (2010) The effect of substrate size on the locomotion and gait patterns of the kinkajou (Potos flavus). J Exp Zool A Comp Exp Biol 313:157–168Google Scholar
  26. Lemelin P, Grafton BW (1998) Grasping performance in Saguinus midas and the evolution of hand prehensility in primates. In: Strasser E, Fleagle JG, Rosenberger AL, McHenry HM (eds) Primate Locomotion—Recent Advances. Springer Science and Business Media, New York, pp 131–144CrossRefGoogle Scholar
  27. Nyakatura JA, Fischer MS, Schmidt M (2008) Gait parameter adjustments of cotton-top tamarins (Saguinus oedipus, Callitrichidae) to locomotion on inclined arboreal substrates. Am J Phys Anthropol 135:13–26PubMedCrossRefGoogle Scholar
  28. Nyakatura JA, Heymann EW (2010) Effects of support size and orientation on symmetric gaits in free-ranging tamarins of Amazonian Peru: implications for the functional significance of primate gait sequence patterns. J Hum Evol 58:242–251PubMedCrossRefGoogle Scholar
  29. Preuschoft H (2002) What does “arboreal locomotion” mean exactly and what are the relationships between “climbing”, environment and morphology? Z Morphol Anthropol 83:171–188PubMedGoogle Scholar
  30. Preuschoft H, Günther MM, Christian A (1998) Size dependence in prosimian locomotion and its implications for the distribution of body mass. Folia Primatol 69:60–81PubMedCrossRefGoogle Scholar
  31. Prost J, Sussman R (1969) Monkey locomotion on inclined surfaces. Am J Phys Anthropol 31:53–58CrossRefGoogle Scholar
  32. Ravosa MJ, Dagosto M (2007) Primate Origins. Adaptations and Evolution. Springer Science and Business Media, New YorkCrossRefGoogle Scholar
  33. Reynolds TR (1985) Mechanics of increased support of weight by the hindlimbs in primates. Am J Phys Anthropol 67:335–349PubMedCrossRefGoogle Scholar
  34. Rollinson J, Martin R (1981) Comparative aspects of primate locomotion, with special reference to arboreal cercopithecines. Symp Zool Soc Lond 48:377–427Google Scholar
  35. Rose MD (1974) Postural adaptations in New and Old World monkeys. In: Jenkins FA Jr (ed) Primate Locomotion. Academic Press, New York, pp 201–222Google Scholar
  36. Sargis EJ (2001) The grasping behaviour, locomotion and substrate use of the tree shrews Tupaia minor and T. tana (Mammalia, Scandentia). J Zool 253:485–490CrossRefGoogle Scholar
  37. Sargis EJ (2002) Primate origins nailed. Science 298:1564–1565PubMedCrossRefGoogle Scholar
  38. Sargis EJ, Boyer DM, Bloch JI, Silcox MT (2007) Evolution of pedal grasping in Primates. J Hum Evol 53:103–107PubMedCrossRefGoogle Scholar
  39. Schmidt A (2014) Locomotion in degus on terrestrial substrates varying in orientation—implications for biomechanical constraints and gait selection. Zoology 117:146–159PubMedCrossRefGoogle Scholar
  40. Schmidt A, Fischer MS (2010) Arboreal locomotion in rats—the challenge of maintaining stability. J Exp Biol 213:3615–3624PubMedCrossRefGoogle Scholar
  41. Schmidt A, Fischer MS (2011) The kinematic consequences of locomotion on sloped arboreal substrates in a generalized (Rattus norvegicus) and a specialized (Sciurus vulgaris) rodent. J Exp Biol 214:2544–2559CrossRefGoogle Scholar
  42. Schmidt M (2005) Hind limb proportions and kinematics: are small primates different from other small mammals? J Exp Biol 208:3367–3383PubMedCrossRefGoogle Scholar
  43. Schmidt M (2008) Forelimb proportions and kinematics: how are small primates different from other small mammals? J Exp Biol 211:3775–3789PubMedCrossRefGoogle Scholar
  44. Schmidt M (2010) Die arboreal quadrupede Fortbewegung der Primaten. Das Grundmuster der Bewegungsprinzipien und die Konsequenzen für die Evolution des Bewegungssystems der Primaten. Habilitation Thesis. Jena: Friedrich Schiller University. (published online at
  45. Schmidt M, Krause C (2011) Scapula movements and their contribution to three-dimensional forelimb excursions in quadrupedal primates. In: D’Août K, Vereecke EE (eds) Primate Locomotion—Linking Field and Laboratory Research. Springer Science and Business Media, New York, pp 83–108Google Scholar
  46. Schmitt D (2003a) Evolutionary implications of the unusual walking mechanics of the common marmoset (C. jacchus). Am J Phys Anthropol 122:28–37PubMedCrossRefGoogle Scholar
  47. Schmitt D (2003b) Insights into the evolution of human bipedalism from experimental studies of humans and other primates. J Exp Biol 206:1437–1448PubMedCrossRefGoogle Scholar
  48. Schmitt D, Cartmill M, Griffin TM, Hanna JB, Lemelin P (2006) Adaptive value of ambling gaits in primates and other mammals. J Exp Biol 209:2042–2049PubMedCrossRefGoogle Scholar
  49. Schmitt D, Gruss LT, Lemelin P (2010) Brief communication: forelimb compliance in arboreal and terrestrial opossums. Am J Phys Anthropol 141:142–146Google Scholar
  50. Shapiro LJ, Young JW (2010) Is primate-like quadrupedalism necessary for fine-branch locomotion? A test using sugar gliders (Petaurus breviceps). J Hum Evol 58:309–319PubMedCrossRefGoogle Scholar
  51. Shapiro LJ, Young JW, Suther A (2011) Quadrupedal locomotion of Saimiri boliviensis: a comparison of field and laboratory-based kinematic data. In: D’Août K, Vereecke EE (eds) Primate Locomotion—Linking Field and Laboratory Research. Springer Science and Business Media, New York, pp 335–356Google Scholar
  52. Shapiro LJ, Young JW, VandeBerg JL (2014) Body size and the small branch niche: using marsupial ontogeny to model primate locomotor evolution. J Hum Evol 68:14–31PubMedCrossRefGoogle Scholar
  53. Smith JL, Carlson-Kuhta P, Trank TV (1998) Forms of forward quadrupedal locomotion. III. A comparison of posture, hindlimb kinematics, and motor patterns for downslope and level walking. J Neurophysiol 79:1702–1716PubMedGoogle Scholar
  54. Soligo C, Martin RD (2007) The first primates: a reply to Silcox et al. (2007). J Hum Evol 53:325–328CrossRefGoogle Scholar
  55. Soligo C, Martin RD (2006) Adaptive origins of primates revisited. J Hum Evol 50:414–430PubMedCrossRefGoogle Scholar
  56. Stevens NJ (2006) Stability, limb coordination and substrate type: the ecorelevance of gait sequence pattern in primates. J Exp Zool A Comp Exp Biol 305:953–963PubMedCrossRefGoogle Scholar
  57. Stevens NJ (2008) The effect of branch diameter on primate gait sequence pattern. Am J Primatol 70:356–362PubMedCrossRefGoogle Scholar
  58. Stevens NJ, Ratsimbazafy JH, Ralainasolo F (2011) Linking field and laboratory approaches for studying primate locomotor responses to support orientation. In: D’Août K, Vereecke EE (eds) Primate Locomotion—Linking Field and Laboratory Research. Springer Science and Business Media, New York, pp 311–333Google Scholar
  59. Sussman RW (1991) Primate origins and the evolution of angiosperms. Am J Primatol 23:209–223CrossRefGoogle Scholar
  60. Vilensky JA, Moore AM, Libii JN (1994) Squirrel monkey locomotion on an inclined treadmill: implications for the evolution of gaits. J Hum Evol 26:375–386CrossRefGoogle Scholar
  61. Wallace IJ, Demes B (2008) Symmetrical gaits of Cebus apella: implications for the functional significance of diagonal sequence gait in primates. J Hum Evol 54:783–794PubMedCrossRefGoogle Scholar
  62. Whitehead P, Larson S (1994) Shoulder motion during quadrupedal walking in Cercopithecus aethiops: integration of cineradiographic and electromyographic data. J Hum Evol 26:525–544CrossRefGoogle Scholar
  63. Witte H, Biltzinger J, Hackert R, Schilling N, Schmidt M, Reich C, Fischer MS (2002) Torque patterns of the limbs of small therian mammals during locomotion on flat ground. J Exp Biol 205:1339–1353PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Bettina Hesse
    • 1
  • John A. Nyakatura
    • 1
    • 2
  • Martin S. Fischer
    • 1
  • Manuela Schmidt
    • 1
  1. 1.Institut für Spezielle Zoologie und Evolutionsbiologie mit Phyletischem MuseumFriedrich-Schiller-Universität JenaJenaGermany
  2. 2.AG Morphologie und Formengeschichte. Bild Wissen Gestaltung - ein Interdisziplinäres Labor & Institut für BiologieHumboldt Universität zu BerlinBerlinGermany

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