Animal Locomotion

236 Pages·2018·8.596 MB·English

by  Andrew Biewener, Sheila Patek

Animal Locomotion

Animal Locomotion
Second Edition
Andrew A. Biewener
Charles P. Lyman Professor of Biology
Director, Concord Field Station, Harvard University
Sheila N. Patek
Associate Professor of Biology, Duke University
1
1
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© Andrew A. Biewener & Sheila N. Patek 2018
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First Edition published in 2003
Second Edition published in 2018
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Library of Congress Control Number: 2018933083
ISBN 978–0–19–874315–6 (hbk.)
ISBN 978–0–19–874316–3 (pbk.)
DOI: 10.1093/oso/9780198743156.001.0001
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Table of Contents
Preface ix
List of Variables xi
1 Physical and Biological Properties and Principles: Related to Animal Locomotion 1
1.1 Environmental media 1
1.2 Physics and energetics of movement 2
1.3 Biomechanics of locomotor support 3
1.4 Scaling: the importance of size 7
1.5 Dimensions and units 9
1.6 Summary 11
2 Muscles and Skeletons: The Building Blocks of Animal Movement 12
2.1 Muscles 12
2.2 Molecular organization: mechanism of force generation and shortening 12
2.3 Levels of force generation and the isometric force-length relationship 14
2.4 Power, efficiency and the isotonic force-velocity relationship 16
2.5 “Work loops”: time varying force-length behavior of muscles 18
2.6 Excitation–contraction coupling and motor units 20
2.7 Muscle fiber types 22
2.8 Fiber architecture and its effects on muscle volume and energy use 25
2.9 Skeletons 27
2.10 The connection between muscle and skeleton 27
2.11 Vertebrate endoskeletons 28
2.12 Invertebrate exoskeletons 30
2.13 Hydrostatic skeletons 30
2.14 Skeletons as jointed lever systems 31
2.15 Summary 33
3 Energetics of Locomotion 34
3.1 Linking cellular metabolism to locomotor energetics 34
3.2 Sources and time course of energy usage during exercise 35
3.3 Endurance and fatigue 40
3.4 Energy costs across terrestrial locomotor speeds 40
3.5 Energy cost relative to body size 47
3.6 Energy cost of incline running 52
vi TABLE OF CONTENTS
3.7 Cost of swimming 53
3.8 Cost of flight 54
3.9 Locomotion costs compared 56
3.10 Intermittent exercise 58
3.11 Other adaptations for increased aerobic capacity 59
3.12 Summary 59
4 Movement on Land 61
4.1 Biological wheels: why so few? 61
4.2 Limbs as propulsors: support and swing phases 62
4.3 Limb mechanical advantage and joint torques: interaction
of limb posture and ground reaction force 64
4.4 Locomotor gaits 67
4.5 Stride frequency and stride length relative to speed and size 69
4.6 Spring-mass properties of running 71
4.7 Maneuverability versus stability 73
4.8 Froude number and dynamic similarity 76
4.9 Inferring gait and speed of fossil animals 77
4.10 Mechanical work: potential and kinetic energy changes
during terrestrial locomotion 77
4.11 Collisional mechanics of legged locomotion 80
4.12 Legged robotics 82
4.13 Limbless locomotion 82
4.14 Muscle work versus force economy 84
4.15 Tendon springs and muscle dampers 85
4.16 Summary 88
5 Movement in Water 90
5.1 Thrust and drag 90
5.2 Inertia, viscosity and Reynolds number 91
5.3 Steady flow: drag and streamlines 93
5.4 Swimming fish, mammals and cephalopods: movement at high Re 95
5.5 Jet-based fluid propulsion 103
5.6 Movement at low Re: the reversibility of flow 104
5.7 Movement at intermediate Re: switching between paddles and rakes 108
5.8 Air-water interface: surface swimming, striding and sailing 108
5.9 Biological robotics in and on water 112
5.10 Summary 112
6 Movement in Air 114
6.1 Flight forces: lift, drag and thrust 115
6.2 Power requirements for steady flight 119
6.3 Gliding flight 121
6.4 Flapping flight 125
6.5 Flight motors and wing anatomy 132
6.6 Flight maneuvering and stability 139
TABLE OF CONTENTS vii
6.7 Unsteady aerodynamic mechanisms 143
6.8 Summary 146
7 Jumping, Climbing and Suspensory Locomotion 147
7.1 Jumping 147
7.2 Jump take-offs and trajectories 148
7.3 Scaling of jumps 149
7.4 Power enhancements to jump performance 152
7.5 Interactions with the substrate during jumping 156
7.6 Climbing and attachment mechanisms 158
7.7 Suspensory locomotion 162
7.8 Inspiration for synthetic systems 163
7.9 Summary 163
8 Neuromuscular Control of Movement 165
8.1 Sensory elements 165
8.2 Sensorimotor integration via local reflex pathways 169
8.3 Muscle recruitment in relation to functional demand:
force, speed and endurance 174
8.4 Reciprocal inhibition: a basic feature of sensorimotor neural circuits 182
8.5 Distributed control: the role of central pattern generators 183
8.6 Case examples of motor control 185
8.7 Summary 187
9 Evolution of Locomotion 190
9.1 Large-scale trends in animal locomotion 190
9.2 From genes to locomotion 197
9.3 Comparative methods and animal locomotion 198
9.4 The relevance of evolution to robotics and bio-inspired design 200
9.5 Summary 202
References 205
Index 219

Preface
The goal of this book is to provide a synthesis of the ment, we can understand the common principles that
physical, physiological, evolutionary, and biomech- underlie each mode of locomotion. A second is that
anical principles that underlie animal locomotion. size matters. One of the most amazing aspects of biol-
An understanding and full appreciation of animal ogy is the enormous spatial and temporal scale over
locomotion requires the integration of these prin- which organisms and biological processes operate.
ciples. Throughout this book, we present, as broadly Within each mode of locomotion, animals have evolved
as possible and within a reasonable amount of space, designs and mechanisms that effectively contend with
a discussion of animal locomotion that is accessible the physical properties and forces imposed on them
to undergraduates, yet also of value to more advanced by their environment. Understanding the cons traints
graduate students and professionals. Toward this of scale that underlie locomotor mechanisms is
end, we provide the necessary introductory founda- essential to appreciating how these mechanisms have
tion that will allow a more in-depth understanding evolved and how they operate. A third theme is the
of the physical biology and physiology of animal importance of taking an integrative and compara-
movement. In so doing, we hope that this book will tive evolutionary approach in the study of biology.
illuminate the fundamentals and breadth of these Organisms share much in common. Much of their
systems, while inspiring our readers to look more molecular and cellular machinery is the same. They
deeply into the scientific literature and investigate also must navigate similar physical properties of their
new features of animal movement. environment. Consequently, an integrative approach
Animal locomotion is so rich and diverse that it is to organismal function that spans multiple levels of
daunting to try to write an introductory book, even biological organization provides a strong under-
at an upper-level undergraduate or graduate level. standing of animal locomotion. By comparing across
The scales of locomoting animals range from micro- species, common principles of design emerge. Such
scopic to house-sized and the habitats extend from comparisons also highlight how certain organisms
the moist surface of delicate leaves to the depths of may differ and point to strategies that have evolved
the open ocean. The study of animal locomotion itself for movement in diverse environments. Finally,
extends back thousands of years as humans have per- because convergence upon common designs and
formed observational and experimental studies of the generation of new designs result from historical
animal capabilities, whether due to simple fascination processes governed by natural selection, it is also
or with the desire to emulate nature’s capabilities. This important that we ask how and why these systems
is a big, historic field offering a wealth of inspiration, have evolved.
yet the field is grounded in a set of physical rules When we decided to write the second edition of
that unites much of the diversity and allows us to this book, which was first published more than a dec-
write a concise book about the core principles of ade ago, our goal was to bring the first edition up to
animal locomotion. date, increase the diversity of animals covered in the
Several themes run through this book. The first is book, and to address the burgeoning fields of evolu-
that by comparing the modes and mechanisms by tionary analysis of locomotion and the application of
which animals have evolved the capacity for move- animal locomotor mechanisms to the development