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Developments in Primatology: Progress and Prospects Series Editor: Russell H. Tuttle Department of Anthropology The University of Chicago, Il, USA For other titles published in this series, go to www.springer.com/series/5852 wwwwwwwwwwwwwww Kristiaan D’Août Evie E. Vereecke ● Editors Primate Locomotion Linking Field and Laboratory Research Editors Kristiaan D’Août Evie E. Vereecke Laboratory for Functional Morphology Anatomy Department of Biology Faculty of Medicine University of Antwerp Catholic University Leuven, KULAK Belgium Belgium [email protected] [email protected] ISBN 978-1-4419-1419-4 e-ISBN 978-1-4419-1420-0 DOI 10.1007/978-1-4419-1420-0 Springer New York Dordrecht Heidelberg London © Springer Science+Business Media, LLC 2011 All rights reserved. This work may not be translated or copied in whole or in part without the written permission of the publisher (Springer Science+Business Media, LLC, 233 Spring Street, New York, NY 10013, USA), except for brief excerpts in connection with reviews or scholarly analysis. Use in connection with any form of information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed is forbidden. The use in this publication of trade names, trademarks, service marks, and similar terms, even if they are not identified as such, is not to be taken as an expression of opinion as to whether or not they are subject to proprietary rights. Printed on acid-free paper Springer is part of Springer Science+Business Media (www.springer.com) Foreword Studies of primate locomotion in the field and in captivity spanned the entire 20th century and first decade of the current century, and, as highlighted in Primate Locomotion: Linking Field and Laboratory Research, they promise to continue for many more decades as newer generations of scientists devise and employ ever more refined tools and approaches. Major events in the evolutionary history of verte- brates such as the tetrapod shift from water to land, and befeathered reptiles taking to the air, have held special interest for scientists and laypersons alike. Standing prominently among these evolutionary puzzles, human bipedalism also generated great interest in how other primates are built and move and are motivated to do so, thereby stimulating research to test models of precedent positional behaviors and changes that might have occurred in the transition from quadruped to hominid biped. Although the anthropological bias has been strong, many scientists have also pursued topics on nonhuman primate species and a wide variety of other tetrapods simply for their own sake or to illuminate broad biomechanical principles that apply to them (Howell 1944; Young 1957; Hildebrand 1967; Alexander 1968, 2003; Biewener 2003). Sir Arthur Keith must be counted among the earliest scientists to employ behav- ioral observations and laboratory experiments, in addition to comparative morpho- logical studies on nonhuman primates to illuminate our peculiar mode of posture and locomotion. While a medical officer in Thailand (1889–1892), Keith set up a primitive dissection laboratory in the dense forest where he resided. His initial goal was to dissect gibbons (Hylobates lar) and sympatric colobine monkeys (Trachypithecus germaini: Groves 2001; Roos et al. 2008) to see whether they, like his patients, suffered from malaria (Keith 1940, 1950). Following earlier anato- mists, he noted marked differences between their internal and external structures, with gibbons more closely resembling humans. He further observed distinct differ- ences between how brachiating gibbons and quadrupedal monkeys negotiated the forest canopy. When he returned to the United Kingdom he continued to dissect a greater variety of apes and monkeys and conducted experiments to understand possible selective effects of gravity on the human body in relation to obligate orthograde v vi Foreword posture and locomotion. For instance, he inserted a mercury manometer into his stomach and rectum (one expects in that sequence) to measure pressures on the pelvic floor, abdominal wall, diaphragm, and viscera as he assumed a variety of postures (Keith 1923). Basic research slowed during World Wars I and II, but during the latter, Elftman and Manter (1935a,b; Elftman 1944) published much-cited informative compari- sons of human and chimpanzee footprints and feet as the subjects walked bipedally. Later researchers have supported many of their observations on the functional mor- phology of human and chimpanzee feet, but some of their generalizations from a single 5-year-old chimpanzee can be challenged. For instance, chimpanzees more commonly walk with extended lateral toes and an abducted hallux than with curled lateral toes and an adducted hallux (Tuttle 1970, 1987, 1990, 2008; Tuttle et al. 1990, 1991, 1992, 1998). I suspect the extent to which subjects are comfortable during experiments is a factor. Studies, research papers, symposia, and books on primate locomotion and post- cranial morphology in extant and fossil primates burgeoned from the 1960s onwards (Kinzey 1967; Kondo et al. 1975; Jenkins 1974; Morbeck et al 1979; Kondo 1985; Strasser et al. 1998; Ishida et al 2006; Stevens and Carlson 2008), and virtually all meetings of the American Association of Physical Anthropologists, International Primatological Society, and American Society of Primatologists have hosted symposia and podium and poster presentations on these topics. Clearly, although we have learned a good deal in comparison with the level of pre-20th century knowledge, there are many more puzzles remaining to be solved and envisioned. As a pioneer in the adaptation and application of fine-wire elec- trode electromyography to apes (Tuttle et al. 1972, 1979, 1983, 1992; Tuttle and Basmajian 1973, 1974a,bc, 1977, 1978a,b; Tuttle 1974, 1994; Tuttle, Basmajian, and Ishida 1975, 1978, 1979; Ishida, Tuttle et al. 1978; Tuttle and Watts 1985; Tuttle, Hallgrímsson, and Basmajian 1994, 1999), I must warn that the return of useful information about the adaptive complexes of subject species, and especially the application of it to interpret fossil primates, is very limited. The same holds for new and refined technologies employed by researchers who report and reflect on their projects in Primate Locomotion: Linking Field and Laboratory Research. As some of the authors remind us, the environments in which one must work are increasingly restricted by rules governing studies on primates, particularly great apes. The good news is that some researchers meet the challenge by creatively crafting protocols that limit or eliminate invasive techniques and physical restric- tion of their subjects. A further encouraging sign for future advances is that there are many more researchers, laboratories, field sites, and focal species than when I began collaborative research with John V. Basmajian in the United States and Hidemi Ishida, Tasuku Kimura, and Morihiko Okada in Japan. For instance, the 45 authors in Primate Locomotion: Linking Field and Laboratory Research are from 8 nations (Belgium, France, Germany, Greece, Japan, Madagascar, the United Kingdom, and the United States). Finally, I urge all laboratory workers, especially ones who have spent their lives in urban settings, to venture into the field and spend notable spans watching Foreword vii primates and other animals moving on natural substrates. Films are fine, but they really are not the same as one’s own direct observations to inform creative labora- tory experiments and to bound evolutionary models based on them. Russell H. Tuttle Department of Anthropology The University of Chicago, Il, USA References Alexander RMcN (1968) Animal Mechanics. Sidgwich & Jackson, London. ——— 2003. Principles of Animal Locomotion. Princeton University Press, Princeton, NJ. Biewener AA (2003) Oxford University Press, Oxford. Elftman H (1944) The bipedal walking of the chimpanzee. J Mammal 24:67–71. Elftman H, Manter J (1935a) Chimpanzee and human feet in bipedal walking. Am J Phys Anthropol 20:69–79. ——— (1935b) The evolution of the human foot, with especial reference to the joints. J Anat 70:56–67. Groves C (2001) Primate Taxonomy. Smithsonian Institution Press, Washington, DC. Hildebrand M (1967) Symmetrical gaits of primates. Am J Phys Anthropol 26:119–130. Howell AB (1944) Speed in Animals: Their Specialization for Running and Leaping. Hafner, New York. Ishida H, Tuttle RH, Okada M, Kimura T (1978) Activities of hindlimb muscles in a bipedal gib- bon. In: Chivers DJ, Joysey KA (eds), Recent Advances in Primatology, Vol. 3: Evolution. Academic Press, London, pp 459–462. Ishida H, Tuttle R, Pickford M, Ohihara N, Nakatsukasa M (2006) Human Origins and Environmental Backgrounds. Springer, New York. Jenkins FA Jr, ed (1974) Primate Locomotion. Academic Press, New York. Keith A (1923) Man’s posture: its evolution and disorders. Br Med J 1:451–454, 499–502, 545– 548, 587–590, 624–626, 669–672. ——— (1940) Fifty years ago. Am J Phys Anthropol 26:251–267. ——— (1950) An Autobiography. Watts, London. Kinzey WG, ed (1967) Symposium on primate locomotion. Am J Phys Anthropol 26:115–275. Kondo S (1985) Primate Morphophysiology, Locomotor Analyses and Human Bipedalism. University of Tokyo Press, Tokyo. Kondo S, Kawai M, Ehara A, Kawaura S (1975) Proceedings from the Symposia of the Fifth congress of the International Primatological Society. Japan Science Press, Tokyo. Morbeck ME, Preuschoft H, Gomberg N (1979) Environment, Behavior, and Morphology: Dynamic Interactions in Primates. Gustav Fischer, Stuttgart and New York. Roos C, Nadler T, Walter L (2008) Mitochondrial phylogeny, taxonomy and biogeography of the silvered langur species group (Trachypithecus cristatus). Mol Phylogenet Evol 47:629–636. Stevens NJ, Carlson KJ, eds (2008) Bridging gaps between experimental and naturalistic approaches in the study of primate behavior. Int J Primatol 29:1395–1480. Strasser E, Fleagle J, Rosenberger A, McHenry H (1998) Primate Locomotion: Recent Advances. Plenum Press, New York. Tuttle RH, Watts DP (1985) The positional behavior and adaptive complexes of Pan gorilla. In: Kondo S (ed), Primate Morphophysiology, Locomotor Analyses and Human Bipedalism, pp. University of Tokyo Press, Tokyo, pp 261–28. viii Foreword Tuttle RH (1970) Postural, propulsive, and prehensile capabilities in the cheiridia of chimpanzees and other great apes. In Bourne GH (ed), The Chimpanzee, Vol. 2. Karger, Basel, pp 167–253. ——— (1975) Electromyography of Pan gorilla: an experimental approach to hominization. In: Kondo S, Kawai M, Ehara A, Kawamura S (eds), Proceedings from the Symposia of the Fifth Congress of the International Primatological Society. Japan Science Press, Tokyo, pp 303–314. ——— (1987) Kinesiological inferences and evolutionary implications from Laetoli bipedal trails G-1, G-2/3, and A. In: Leakey MD, Harris JM (eds), Laetoli, a Pliocene Site in Northern Tanzania.Clarendon Press, Oxford, pp 503–523.. ——— (1990) The pitted pattern of Laetoli feet. Nat Hist 3/90:60–65. ——— (1994) Up from electromyography: primate energetics and the evolution of human bipedalism. In: Corruccini RS, Ciochon RL (eds), Integrative Paths to the Past: Paleoanthropological Advances in Honor of F. Clark Howell. Prentice Hall, Englewood Cliffs, NJ, pp 269–284. ——— (2008) Footprint clues in hominid evolution and forensics: lessons and limitations. Ichnos 15:158–165. Tuttle RH, Basmajian JV (1973) EMG of locomotion in gorilla and man. In: Stein R, Pearson KB, Smith RS, Redford JB (eds), Control of Posture and Locomotion. Plenum Press, London, pp 599–609. ——— (1974a) Electromyography of forearm musculature in gorilla and problems related to knuckle-walking. In: Jenkins FA Jr (ed), Primate Locomotion. Academic Press, New York, pp 293–347. ——— (1974b) Electromyography of the manual long digital flexor muscles in gorilla. In: Barnosell F (ed), Proceedings of the 6th Congreso Internacional de Medicina Fisica, Vol. II, 1972. Ministerio de Trabajo, Instituto Nacional de Prevision, Madrid, pp 311–315. ——— (1974c) Electromyography of brachial muscles in Pan gorilla and hominoid evolution. Am J Phys Anthropol 41:71–90. ——— (1977) Electromyography of pongid shoulder muscles and hominoid evolution I. Retractors of the humerus and “rotators” of the scapula. Yrbk Phys Anthropol 1976 20:491–497. ——— (1978a) Electromyography of pongid shoulder muscles. II. Deltoid, rhomboid and “rota- tor cuff.” Am J Phys Anthropol 49:47–56. ——— (1978b) Electromyography of pongid shoulder muscles. III. Quadrupedal positional behavior. Am J Phys Anthropol 49:57–70. Tuttle RH, Basmajian JV, Ishida H (1975) Electromyography of the gluteus maximus muscle in gorilla and the evolution of hominid bipedalism. In: Tuttle RH (ed), Primate Functional Morphology and Evolution. Mouton, The Hague, pp 253–269. ———(1978) Electromyography of pongid gluteal muscles and hominid evolution. In: Chivers DJ, Joysey KA (eds), Recent Advances in Primatology, Vol. 3, Evolution.Academic Press, London, pp 463–468. ——— (1979) Activities of pongid thigh muscles during bipedal behavior. Am J Phys Anthropol 50:123–136. Tuttle RH, Basmajian JV, Regenos E, Shine G (1972) Electromyography of knuckle-walking: results of four experiments on the forearm of Pan gorilla. Am J Phys Anthropol 37:255–266. Tuttle RH, Cortright G, Buxhoeveden D (1979) Anthropology on the move; progress in studies of non-human primate positional behavior. Yrbk Phys Anthropol 1979 22:187–214. Tuttle RH, Hallgrímsson B, Basmajian JV (1994) Electromyography and elastic mechanisms in kunckle-walking Pan gorilla and Pan troglodytes. In: Thierry B, Anderson JR, Roeder JJ, Herrenschmidt N (eds), Current Primatology, Vol. 1: Ecology and Evolution. Université Louis Pasteur, Strasbourg, pp 215–222. ——— (1999) Electromyography, elastic energy and knuckle-walking: a lesson in experimental anthropology. In: Lindburg D, Strum SC (eds), The New Physical Anthropology. Prentice- Hall, Englewood Cliffs, NJ, pp 32–41.. Tuttle RH, Hallgrìmsson B, Stein T (1998) Heel, squat, stand, stride: function and evolution of hominoid feet. In: Strasser E, Fleagle J, Rosenberger A, McHenry H (eds), Primate Locomotion: Recent Advances. New York: Plenum Press, New York, pp 435–448. Foreword ix Tuttle RH, Hollowed J, Basmajian JV (1992) Electromyography of pronators and supinators in great apes. Am J Phys Anthropol 87:215–226. Tuttle RH, Velte M, Basmajian JV (1983) Electromyography of brachial muscles in Pan troglo- dytes and Pongo pygmaeus. Am J Phys Anthropol 61:75–83. Tuttle RH, Webb DM, Baksh M (1991) Laetoli toes and Australopithecus afarensis. Hum Evol 6:193–100. Tuttle RH, Webb DM, Tuttle NI (1991) Laetoli footprint trails and the evolution of hominid bipedalism. In : Coppens Y, Senut B (eds), Origine(s) de la Bipédie chez les Hominidés. C.N.R.S, Paris, pp 203–218. Tuttle RH, Webb DM, Tuttle NI, Baksh M (1992) Footprints and gaits of bipedal apes, bears and barefoot people: perspectives on Pliocene tracks. In: Matano S, Tuttle RH, Ishida H, Goodman M (eds), Topics in Primatology, Vol. 3, Evolutionary Biology, Reproductive Endocrinology and Virology. University of Tokyo Press, Tokyo, pp 221–242. Young JZ (1957) The Life of Mammals. Oxford University Press, Oxford. wwwwwwwwwwwwwww

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