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The Evolution of Hominoid Ecomorphology Studies Of THE EVOLUTION OF HOMINOID ECOMORPHOLOGY STUDIES OF LOCOMOTOR BEHAVIOUR AND ANATOMY IN HUMAN AND NONHUMAN APES Emily Louisa Rose Saunders A thesis submitted to the University of Birmingham for the degree of DOCTOR OF PHILOSOPHY School of Biosciences College of Life and Environmental Sciences University of Birmingham September 2016 University of Birmingham Research Archive e-theses repository This unpublished thesis/dissertation is copyright of the author and/or third parties. The intellectual property rights of the author or third parties in respect of this work are as defined by The Copyright Designs and Patents Act 1988 or as modified by any successor legislation. Any use made of information contained in this thesis/dissertation must be in accordance with that legislation and must be properly acknowledged. Further distribution or reproduction in any format is prohibited without the permission of the copyright holder. ABSTRACT Locomotor behaviour is the interface between an animal and the surrounding environment, dictating its ability to access food, escape predators and compete for mates. Extant apes have evolved a diverse range of locomotor strategies which allows them to exploit terrestrial and arboreal environments despite their large body size. However, hominins (modern humans and their ancestors) are traditionally defined by their restriction to upright, bipedal posture and locomotion. Reconstructions of locomotor capacity in fossil hominoids allow investigation of the evolution of extant ape locomotor behaviours, including our own bipedal gait. However, these reconstructions rely on a detailed understanding of the relationships between morphology, locomotor behaviour and the environment in extant apes. This thesis explores variation in locomotor behaviour and skeletal morphology among extant apes in order to shed light on these relationships. The effects of environmental variation on bipedal and knuckle-walking kinematics were investigated in captive chimpanzees (Pan troglodytes) and lowland gorillas (Gorilla gorilla gorilla). Analysis of video footage of individuals moving through their enclosures shows that locomotor kinematics are sensitive to arboreal support properties in both species, and forelimb kinematics during knuckle-walking contrast with previously suggested differences used to advocate independent evolution of knuckle-walking in Pan and Gorilla. The results emphasise the influence of environmental context on hominoid locomotion. The arboreal locomotor behaviour of modern human tree climbers from the UK was explored in the light of claims that adaptations to habitual terrestrial bipedality restrict arboreal capacity. The climbers completed an ecological task of activating four buzzers situated in the peripheral branches of an oak tree. Their behaviour demonstrated that substantial arboreal capabilities are accommodated by modern human morphology, and that humans use similar locomotor strategies to other extant great apes in order to overcome the challenges of the arboreal environment. This provides strong evidence against the presence of a rapid and absolute arboreal-terrestrial transition in hominin evolution. The variation in five skeletal indicators of habitual bipedality among extant apes was quantified in order to test the reliability of inferring habitual bipedality from skeletal morphology in fossil hominoids. Expression of the anterior inferior iliac spine, obturator externus groove, twisting of the femoral head, angle of the distal tibia articular surface and high lateral lip of the patellar groove of the femur was measured from skeletal specimens of extant apes. There was considerable variation in the expression of these features, particularly within modern humans, suggesting that the absence of any one feature may not reliably indicate a lack of bipedality. Joint ranges of motion (ROM) predicted from skeletal material have also been used to infer locomotor behaviour in fossil hominoids. Flexion/extension ROMs at the hip, knee and ankle were measured from skeletal specimens of extant great apes using digitised photographs. These skeletal measures of ROM varied considerably within extant ape species, and were not strongly related to interspecific differences in passive ROM (maximum ROM in a living animal) and active ROM (the ROM used during positional behaviour). This suggests that interpretations of locomotor capacity in fossil hominoids based on relationships between skeletal measures of ROM and locomotor behaviour in extant apes are unreliable. These studies highlight the importance of behavioural flexibility in determining locomotor capacity in hominoids, and suggest that fossil hominoids were less restricted in their locomotor repertoires than previous reconstructions suggest. Crown hominoids may share a morphological propensity for considerable behavioural flexibility, rather than phylogenetically constrained sets of locomotor behaviours. For my Dad, who taught me to question. ACKNOWLEDGEMENTS I would like to thank Susannah Thorpe and Alice Roberts, who have been friends and mentors throughout my PhD as well as brilliant academic supervisors. Thank you Susannah for your constant support, for teaching me how to write, and for giving me so many wonderful opportunities; and thank you Alice for inspiring me with your infectious enthusiasm for anthropology, and for teaching me to never, ever stop thinking about spandrels! I would also like to thank Jackie, Julia, Lucy, Elise, Maria and everybody else in the lab for their help and for a fantastic four years at Birmingham. A very special thank you to Nardie – I feel incredibly lucky to have been able to share this experience with you. Thank you for your true friendship, for inspiring me with your love of nature, and for staying up to help me to fix electrodes at 3am when we had to start the experiment at 5am. Thanks also to the team at Liverpool University: Robin Crompton for valuable input into study design and writing, Kris D’Août and Russ Savage for their technical expertise and support during the climbing study, and Colleen Goh for her constant collaboration and for sharing much-needed laughs in the strangest rental accommodation ever. Thank you to Jo Newbolt and the primate keepers at Paignton Zoo for all their valuable help during data collection, and to the gorillas who ensured the nine months I spent there were entertaining. Thank you also to the staff at Twycross Zoo, The Natural History Museum, The Museum of London, The Powell-Cotton Museum, The Museum für Naturkunde in Berlin, The Anthropological Institute at Zurich University, The National Museum of Scotland, The Royal Museum of Central Africa in Tervuren, The Lapworth Museum and The National Trust, for their friendly welcomes and assistance with my research. Special thanks go to Professor Pasuk, Doi and Neu at the Forensic Osteology Research Center, Chiang Mai University for making my time in Thailand so enjoyable. Thank you also to Jane, Scott, Ruby and Katie in Zurich for your generous hospitality and welcome, and to Auntie Daphne, Uncle Den, Louise and Laura for putting me up several times during data collection! Thank you to Waldo Etherington, James Aldred and Ian Geddes from Canopy Access Ltd., and all the tree climbers and helpers who put up with the wind and rain to help us produce a fantastic study! Thank you also to James Ashley for his keen dedication to the chimpanzee project and for all the hours spent filming them at the zoo, and to Fran Childs and Naomi Mountford for their valuable help with data collection. I would also like to thank Sam Lucas and Rebecca Lucas for their physiology expertise and insightful discussions on tree climbing, and Tim Collins for his valuable signal processing help. Thank you also to Colin Shaw, Nick Owen, Tom Rein, Kate Robson Brown and Dr Nok for their assistance with anatomical studies. Thank you to my family for their constant encouragement. Thank you Luce for the never- failing friendship, laughter and calm support that you give. Thank you Mum and Dad for always believing in me, for helping to build bone-clamping devices and spreadsheets, and for the hours spent driving me around to find a study tree! Lastly, thank you Pete for always being beside me, always understanding and always cheering me up. Finally, I would like to thank the University of Birmingham for funding this research, and the George Parkes Fund for enabling me to present my work at conferences. THESIS CONTENTS Page CHAPTER ONE GENERAL INTRODUCTION Positional behaviour, ecomorphology and evolution 1 Environmental challenges to primate positional behaviour 10 Solutions in positional behaviour 11 Behavioural and morphological flexibility 24 Thesis aims 28 CHAPTER TWO KINEMATIC VARIATION IN THE BIPEDAL AND KNUCKLE- WALKING GAITS OF CHIMPANZEES (PAN TROGLODYTES) AND WESTERN LOWLAND GORILLAS (GORILLA GORILLA GORILLA): THE IMPORTANCE OF ENVIRONMENTAL INFLUENCES AND BEHAVIOURAL FLEXIBILITY Abstract 30 Introduction 31 Materials and Methods 40 Study subjects and experimental setup 40 Sequence digitisation 42 Statistical analysis 44 Results 45 Bipedal kinematics 45 Knuckle-walking kinematics 49 Discussion 51 Conclusions 58 CHAPTER THREE MODERN HUMAN ARBOREAL CAPACITY CASTS DOUBT ON EARLY HUMAN ARBOREAL-TERRESTRIAL TRANSITION (a manuscript for Science) Abstract 61 Introduction 62 Results and Discussion 65 Conclusions 69 Materials and Methods 70 Experimental Design 70 Locomotion and Support Use 72 Kinematic Analysis 72 Statistical Analysis 73 CHAPTER FOUR MODERN HUMAN LOCOMOTOR
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