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Adaptation of the Non-Human Great Ape Lower Limb in Response to Locomotor Behaviour

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Adaptation of the Non-Human Great Ape Lower Limb in Response to Locomotor Behaviour Adaptation of the non-human great ape lower limb in response to locomotor behaviour Thesis submitted in accordance with the requirements of the University of Liverpool for the degree of Doctor in Philosophy by Katy Ann Wareing June 2016 Adaptation of the non-human great ape lower limb in response to locomotor behaviour Katy Ann Wareing ABSTRACT Understanding the relationship between structure and function is crucial when trying to establish differences between closely related species; such as primates. Muscle architecture from the hindlimbs of great apes was compared, and indicated differences both within and across species. Asymmetry in the musculature of chimpanzees was found to be significant for certain muscle groups; indicating that leg preference for specific tasks may exist within this species. The comparison across the four species studied indicated subtle differences between the orangutan and the other great apes; with longer muscle fascicles, smaller physiological cross- sectional area and angles of pennation. This suggests an adaptation to slow and controlled, wider positional movements, as part of a complex arboreal environment. Muscle architectural variables did not consistently scale allometrically, however, using analysis of covariance to normalise for body mass showed significant differences at the species level. In all great apes, the lower limb tendons varied in their mechanical properties; with a hallucal flexor yielding a higher Young’s modulus than tendons associated with muscles of power and balance, suggesting an adaptation to a specific functional role. The plantar aponeurosis was morphologically different across all species studied, with results indicating an adaptation to shear, multi-directional forces in the orangutan foot, possibly reflecting the use of hand assisted bipedalism in an arboreal context, and linear, anteroposterior forces in the gorilla. Overall, this thesis outlines the subtle differences present between closely related species of primates, indicating that morphological adaptations occur in response to external loading during locomotor behaviour. I ACKNOWLEDGEMENTS I would like to acknowledge and thank my supervisor, Dr Iain S. Young, for his support and advice throughout my Ph.D. I would also like to thank my additional supervisors, Ms. Julie Bridson, Dr Nathan Jeffery and Professor Robin Crompton, and I would like to thank the University of Liverpool for supporting this research. I would like to thank those who have contributed to this work, particularly Dr Julia Myatt for providing excellent advice and assisting with data collection and Dr Carol Hercock for assistance with material testing. I would also like to thank Dr Andrew Kitchener and Mr Lee Moore for providing specimens, equipment and assistance throughout this thesis. There are many people whose support and friendship have helped me through difficulties, in particular Dr Emma Webster, Dr Jane Pulman, Ms Lisa Crimmins, and the School of Medicine staff, to name but a few. I would also like to acknowledge Dr Mary Blanchard for her helpful suggestions, endless support, laughter, belief and friendship, for which I cannot be thankful enough. Additionally I would like to thank Mr Matt Shillito for helpful suggestions and continued support. II I would like to thank my family, in particular my Grandparents and Dad for their love, kindness, friendship and never-ending support. I would also like to thank Ms Rebecca Lambert for never giving up on me. Finally, I would like to thank my best friend and fiancé Mr Kieran O’Mahony. My own words cannot express my gratitude, so I must borrow some from a great man: ‘I want to stand as close to the edge as I can without going over. Out on the edge you see all kinds of things you can't see from the centre’, thank you Kieran for keeping me on the edge. III TABLE OF CONTENTS ABSTRACT ...................................................................................................................... I ACKNOWLEDGEMENTS ................................................................................................ II TABLE OF CONTENTS ...................................................................................................IV TABLE OF FIGURES .................................................................................................... XIII TABLE OF TABLES .................................................................................................... XVII TABLE OF EQUATIONS ............................................................................................... XXI Chapter 1 ...................................................................................................................... 1 General Introduction .................................................................................................... 1 1.1 The field of anatomy ..................................................................................... 1 1.2 Anatomical terminology ................................................................................ 1 1.3 Components of the musculoskeletal system ................................................ 2 1.3.1 The lower limb in humans ...................................................................... 5 1.3.2 The lower limb in great apes .................................................................. 7 1.4 Primate locomotion ..................................................................................... 11 1.4.1 Locomotion in humans ......................................................................... 12 1.4.2 Locomotion in the orangutan .............................................................. 13 1.4.3 Locomotion in the chimpanzee ............................................................ 15 IV 1.4.4 Locomotion in the bonobo ................................................................... 17 1.4.5 Locomotion in the gorilla ..................................................................... 18 1.4.6 Problems with observing behaviour .................................................... 20 1.5 Methods of investigation ............................................................................ 21 1.5.1 Gait analysis; measured and modelled data ........................................ 21 1.6 Thesis outline ............................................................................................... 23 1.6.1 Chapter 2 .............................................................................................. 23 1.6.2 Chapter 3 .............................................................................................. 26 1.6.3 Chapter 4 .............................................................................................. 27 1.6.4 Chapter 5 .............................................................................................. 28 Chapter 2 .................................................................................................................... 30 Hindlimb descriptive anatomy and muscle architecture in great apes; comparing inter- and intra-species variation ............................................................................... 30 2.1 Introduction ................................................................................................. 30 2.1.1 Descriptive anatomy; qualitative research .......................................... 32 2.1.2 Muscle architecture data ..................................................................... 33 2.1.3 Primate morphology and behaviour .................................................... 35 2.1.4 Normalising data .................................................................................. 36 V 2.1.4.a Geometry vs. allometry in non-human primates....................................... 37 2.1.4.b Regression analysis .................................................................................... 38 2.2 Aims ............................................................................................................. 40 2.3 Objectives .................................................................................................... 41 2.4 Methods ...................................................................................................... 41 2.4.1 Specimens and preparation ................................................................. 41 2.4.2 Dissection and descriptive anatomy .................................................... 43 2.4.3 Recording muscle architecture data .................................................... 44 2.4.4 Data analysis ........................................................................................ 46 2.4.4.a Normalising data: current study ................................................................ 47 2.4.4.b Normalising data: including published studies .......................................... 48 2.4.4.c Interspecies effects .................................................................................... 50 2.5 Results ......................................................................................................... 52 2.5.1 Descriptive anatomy ............................................................................ 52 2.5.1.a Absent and extra muscles .......................................................................... 52 2.5.1.b Variations in the normal muscle arrangement .......................................... 53 2.5.2 Dissection data ..................................................................................... 54 2.5.2.a Muscle architecture
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