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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
Great Clarendon Street, Oxford, OX2 6DP,
United Kingdom
Oxford University Press is a department of the University of Oxford.
It furthers the University’s objective of excellence in research, scholarship,
and education by publishing worldwide. Oxford is a registered trade mark of
Oxford University Press in the UK and in certain other countries
© Andrew A. Biewener & Sheila N. Patek 2018
The moral rights of the authors have been asserted
First Edition published in 2003
Second Edition published in 2018
Impression: 1
All rights reserved. No part of this publication may be reproduced, stored in
a retrieval system, or transmitted, in any form or by any means, without the
prior permission in writing of Oxford University Press, or as expressly permitted
by law, by licence or under terms agreed with the appropriate reprographics
rights organization. Enquiries concerning reproduction outside the scope of the
above should be sent to the Rights Department, Oxford University Press, at the
address above
You must not circulate this work in any other form
and you must impose this same condition on any acquirer
Published in the United States of America by Oxford University Press
198 Madison Avenue, New York, NY 10016, United States of America
British Library Cataloguing in Publication Data
Data available
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
Printed and bound by
CPI Group (UK) Ltd, Croydon, CR0 4YY
Links to third party websites are provided by Oxford in good faith and
for information only. Oxford disclaims any responsibility for the materials
contained in any third party website referenced in this work.
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 TA B L E O F C O N T E N T S

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
 TA B L E O F C O N T E N T S 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

References205
Index219
 Preface
The goal of this book is to provide a synthesis of the
physical, physiological, evolutionary, and biomech-
anical principles that underlie animal locomotion.
An understanding and full appreciation of animal
locomotion requires the integration of these prin-
ciples. Throughout this book, we present, as broadly
as possible and within a reasonable amount of space,
a discussion of animal locomotion that is accessible
to undergraduates, yet also of value to more advanced
graduate students and professionals. Toward this
end, we provide the necessary introductory founda-
tion that will allow a more in-depth understanding
of the physical biology and physiology of animal
movement. In so doing, we hope that this book will
illuminate the fundamentals and breadth of these
systems, while inspiring our readers to look more
deeply into the scientific literature and investigate
new features of animal movement.
Animal locomotion is so rich and diverse that it is
daunting to try to write an introductory book, even
at an upper-level undergraduate or graduate level.
The scales of locomoting animals range from micro-
scopic to house-sized and the habitats extend from
the moist surface of delicate leaves to the depths of
the open ocean. The study of animal locomotion itself
extends back thousands of years as humans have per-
formed observational and experimental studies of
animal capabilities, whether due to simple fascination
or with the desire to emulate nature’s capabilities. This
is a big, historic field offering a wealth of inspiration,
yet the field is grounded in a set of physical rules
that unites much of the diversity and allows us to
write a concise book about the core principles of
animal locomotion.
Several themes run through this book. The first is
that by comparing the modes and mechanisms by
which animals have evolved the capacity for move-
ment, we can understand the common principles that
underlie each mode of locomotion. A second is that
size matters. One of the most amazing aspects of biol-
ogy is the enormous spatial and temporal scale over
which organisms and biological processes operate.
Within each mode of locomotion, animals have evolved
designs and mechanisms that effectively contend with
the physical properties and forces imposed on them
by their environment. Understanding the con­straints
of scale that underlie locomotor mechanisms is
essential to appreciating how these mechanisms have
evolved and how they operate. A third theme is the
importance of taking an integrative and compara-
tive evolutionary approach in the study of biology.
Organisms share much in common. Much of their
molecular and cellular machinery is the same. They
also must navigate similar physical properties of their
environment. Consequently, an integrative approach
to organismal function that spans multiple levels of
biological organization provides a strong under-
standing of animal locomotion. By comparing across
species, common principles of design emerge. Such
comparisons also highlight how certain organisms
may differ and point to strategies that have evolved
for movement in diverse environments. Finally,
because convergence upon common designs and
the generation of new designs result from historical
processes governed by natural selection, it is also
important that we ask how and why these systems
have evolved.
When we decided to write the second edition of
this book, which was first published more than a dec-
ade ago, our goal was to bring the first edition up to
date, increase the diversity of animals covered in the
book, and to address the burgeoning fields of evolu-
tionary analysis of locomotion and the application of
animal locomotor mechanisms to the development
x P R E FA C E
of novel engineering devices. Naturally, the funda-
mental rules of physics have not changed, yet the
depth of knowledge and development of impressive
technical approaches to the study of these systems
have moved quickly in particular areas. Some areas
covered in the first edition could be written in the
span of a few paragraphs, and now an entire chapter
of new discoveries could be devoted to the topic.
Without a doubt, the biggest challenge of writing
and synthesizing this new edition was keeping the
book straightforward and focused on guiding, fun-
damental principles, while trying to figure out how
to navigate all of the fabulous discoveries that we
simply could not fit in this short volume. As in the
first edition, our foremost goal was to capture the
fundamentals underling the study of animal loco-
motion, even if it meant leaving out much of the
research and history of this vibrant field.
We have re-organized the book in multiple ways,
both in terms of the coverage of the chapters and the
topics of the chapters. The book begins with a chap-
ter on the fundamentals of motion, and quickly
moves to a chapter focused on muscles, a source of
motion unique to animals, and how muscles interact
with animal skeletons to transmit force for move-
ment and support. We next consider the energetics
of locomotion, focusing on how the metabolic cost
of terrestrial movement varies with animal size and
speed, and compares with the cost of flying and
swimming. We then examine the principles of loco-
motion through a series of chapters that explore
three major habitats - land, water, and air. The sev-
enth chapter probes a suite of locomotor modes
that transcend particular habitats and these modes
include jumping, suspensory locomotion and adhe-
sion. The eighth chapter examines the neuromuscu-
lar control of movement, providing an overview of
sensory-motor pathways and motor recruitment that
are central to the dynamic nature of complex loco-
motor systems. We wrap up the book with a chapter
on the evolution of locomotion that examines the
broad trends in the evolution of locomotion, as well
as the methods and levels of analysis for examining
locomotor diversity. It is clear that between the first
and second edition of this book, there has been
exceptional growth in the comparative biomechanics
and physiology of animal locomotion.
We have many people to thank for helping with
both the first and second editions of this book. We
are grateful to our students and colleagues with
whom we have shared the fascination and love of
animal movement, physiology and biomechanics.
These interactions that have come from our work
and discussions are the best part of science. For
their insights on the first edition of the book, we
thank George Lauder, Bob Shadwick, Gary Gillis,
Ty Hedrick, Jim Usherwood, Bob Full, Tom Roberts,
and Peter Weyand. Michael Dickinson and Bret
Tobalske provided feedback on both editions. We
thank Walter Federle for his assistance with synthe-
sizing the field of adhesion in this second edition.
We thank the students of Duke University’s “How
Organisms Move” course and Brown University’s
“Animal Locomotion” course taught by Sharon
Swartz for their feedback on the second edition, espe-
cially Sarah Beaverson, Aakash Jain and Suzanne
Ou. We are grateful to Rachel Crane and Grace Farley
for their editorial assistance. We thank our editors
for their assistance with the process of writing the
first and second editions. Most of all, we are grate-
ful to our families for their support and patience.
This book is dedicated to Dick Taylor, Beth Brainerd,
Farish Jenkins, Jr. and Karel Liem, whose unbounded
enthusiasm for comparative physiology and love of
animal locomotion are an inspiration to so many
students and scientists.
 List of Variables

A area, m2 EMA effective mechanical advantage or lever arm

A wavelength amplitude, m ratio, dimensionless
Am muscle cross-sectional area, or ‘physiological’ ε strain, dimensionless
cross-sectional area (PCSA) of a pinnate ε0 maximum operating strain, dimensionless
muscle, m2
Af fiber cross-sectional area, m2 F force, N
AR aspect ratio, dimensionless F0 isometric muscle force, N
a acceleration, m s−2 Fadd adductor force, N
α incline slope or angle of support (o, degree) Far acceleration reaction force, N
Ffrict static frictional grip, N
b (wing) span, m and scaling exponent, Flat laterally directed force, N
dimensionless Fm force of muscle fibers, N
β duty factor, dimensionless Fr Froude number, dimensionless
BL body length, m f frequency, Hz
BM body mass, kg fnat natural frequency, Hz
BW body weight, N fs stride frequency, s−1 or Hz
Ft tendon force, N
Ca added mass coefficient, dimensionless Ftan tangent force, N
Cd coefficient of drag, dimensionless
Cl lift coefficient, dimensionless G ground reaction force, N
CM center of mass, kg GH horizontal fore-aft ground reaction force, N
Cnet net cost of transport, J m−1 GML medio-lateral ground reaction force, N
Ctot total cost of transport, J m−1 g acceleration due to gravity, m s−2
c cost coefficient, J N−1 GV vertical ground reaction force, N
c' (wing) chord, m Γ circulation (line integral of velocity flow), m2 s−1
cs slipping coefficient, dimensionless
h height, m
D diameter, m η coefficient of friction, dimensionless
D drag, N η’ wave efficiency, dimensionless
d local drag, N
dL limb displacement, m I' moment of inertia, kg m2
ΔL muscle shortening, m
ds muscle shortening, m k spring stiffness, N m−1
d(θ) change in joint angle, rad or deg KE kinetic energy, J
kleg leg spring stiffness, N m−1
E Young’s modulus or elastic modulus, Pa
E* total energy, J l or L length, m
Ėmetab metabolic energy rate, J s−1 L lift force, N
Eff energetic efficiency, % (dimensionless) Lc step length, m
xii L I S T O F VA R I A B L E S

LCM distance that center of mass is accelerated, m T thrust, N

lf muscle fiber length, m T' torque, N m
Ll limb length traveled during landing, m Ts stride duration or time, s
Lpect lift force produced by pectoral fins, N t time, s
Ls sarcomere length or stride length, m tair time airborne during a jump, s
Lt limb length traveled during takeoff, m tc time of limb ground contact or time required
Ltot maximum jump length, m to take off, s
λ wavelength (body undulation), m θ various angles (joint, limb, heading, glide,
grip), rad or deg
m, M mass, kg
μ viscosity, Pa s U* amount of strain energy absorbed per unit
volume of material, J m−3
P power, W or J s−1
P* mass-specific power output, W kg−1 V̇O2max rate of oxygen consumption, ml O2 s−1
PE potential energy, J V volume of accelerated fluid, m3
PPE potential energy power, W or J s−1 v velocity, m s-1
ϕ collision angle, rad or deg vflap velocity of flapping wing, m s−1
vg glide velocity, m s−1
r and R moment arm, m vh horizontal velocity or component of take-off
R resultant propulsive force, N velocity, m s−1
Re Reynolds number, dimensionless vmax maximum velocity, m s−1
ρ density of fluid, kg m−3 vr resultant velocity (of a wing), m s−1
RQ respiratory quotient, dimensionless vs sinking speed (of a glider), m s−1
vt take-off velocity, m s−1
S surface area, m2 vv vertical component of take-off velocity, m s-1
S strength or maximum stress, N m−2 vw water velocity, m s−1
s position of moving object or v* muscle’s intrinsic shortening velocity,
projectile, m lengths s−1
σ force per unit area or stress, N m−2
σ0 maximum operating stress, N m−2 W work, J
σf failure stress, N m−2 Wf work of fracture, J m−2
 C H A PT ER 1
Physical and Biological Properties
and Principles
Related to Animal Locomotion
Observations of the beauty, grace and sheer athleti-
cism of locomoting animals inspire human fascination
with movement. Which aspects of flight do darting
hummingbirds and bumblebees share in common?
How do they differ from a soaring petrel? Which
principles of design are shared by a racing antelope,
a scurrying lizard or a running cockroach, and in
what ways do they differ? The grand scale of bio-
logical sizes and evolutionary diversity yields an
impressive range of locomotor mechanisms. Yet,
underlying this amazing diversity are fundamen-
tal principles of biological organization that can
explain most of these locomotor systems. Studies of
animal locomotion depend on an understanding of
the physical principles that govern how animals
move and properties of the media through which
they move. These studies, in turn, explain why cer-
tain biological devices, such as a wing or a fin, share
features that have evolved for movement within
their particular fluid environments.
This book is about how animals move. It addresses
basic physical principles and properties of the
media in which animals move, seeking to explain
the mechanical design and locomotor function of
animals within these media. It also attempts to
capture the amazing diversity of animal design
and movement. Much of this diversity arises from
the enormous range of sizes—from microscopic
swimmers to the largest whales (1015 orders of mag-
nitude in mass)—and the breadth of environments
that animals inhabit. In this first chapter, we lay the
groundwork for the more focused subsequent
chapters. We examine the role of the environment
Animal Locomotion. Second Edition. Andrew A. Biewener & Sheila N. Patek, Oxford University Press (2018).
© Andrew A. Biewener & Sheila N. Patek 2018. DOI: 10.1093/oso/9780198743156.001.0001
and the fundamentals of loading and forces in ani-
mal mechanics. We offer a quick review of scaling
analyses as well as the key dimensions and units
used in this book.
1.1 Environmental media
Land, air and water constitute the physical world of
organisms. To a large extent, the properties of these
media dictate the locomotor mechanisms that ani-
mals have evolved. For animals that move on land
and fly, the properties of the air and gravity dominate
their physical world. For most aquatic animals,
however, gravity is of little concern. In addition, air
and water play an important role as respiratory
media and therefore affect locomotor design in
terms of how energy is supplied for powering
and sustaining movement. The capacity to move
between physical environments is also important to
many animals. This is the case for flying animals
that must also be capable of movement on land or
through water, as well as for terrestrial animals that
live near the shore where locomotion in air and
water are both required.
1.1.1 Physical properties of media
A few, key physical properties of air and water
impact nearly any animal movement and locomotor
mechanism (Table 1.1). Air and water are both ­fluids:
fluid movement past the body of organisms is fun-
damental to nearly all forms of animal locomo-
tion—even burrowing. Recent studies of burrowing
2 A N I M A L L O C O M OT I O N
Table 1.1 The physical properties of air and water that influence the mechanisms of locomotion.
Physical property Air
Density (g/cm3) @ 25°C 0.0012
Dynamic viscosity 18 x 10−6
(Pa s = Ns/m) @ 20oC
Oxygen content (ml O2/L) 209
Heat capacity (cal/L°C) 0.31
in granular media, such as sand, demonstrate an
intriguing mix of fluid and solid properties and
associated locomotor strategies. Of all the fluid
properties, however, density varies the most: water
density exceeds that of air by more than 800-fold.
The difference in viscosity, though smaller in mag-
nitude, also has an important influence on how
fluid moves past an organism in motion.
Even though aerial flight and aquatic locomo-
tion depend on the same fluid dynamic principles,
the difference in density of these two media has
significant implications for respiratory design and
the capacity for flight, swimming and terrestrial
locomotion of land animals. Oxygen content and
the heat capacity of air versus water indirectly
influence locomotor systems by affecting their
thermal and respiratory function. As we will see,
the locomotor capacity and strategy of animals
depends on the delivery of oxygen to their tissues,
especially the muscles, in order to generate meta-
bolic energy in the form of adenosine triphosphate
(ATP). Temperature and the availability of oxygen
supply from the environment are critical to loco-
motor design.
1.1.2 Impact of physical media on locomotor
function
Because of its much lower density and viscosity,
air imposes proportionately smaller resistive (drag)
forces for flying and terrestrial animals than for
aquatic animals. The main problem for terrestrial
­animals therefore lies in overcoming mass-related
gravi­tational forces as they move. The low density
of air also means that flying animals must generate
sufficient aerodynamic force (lift) to support their
Water Proportional difference
1.000 830
1.02 (seawater)
1 x 10−3 55
7 30
1000 3200
weight, in addition to aerodynamic thrust to over-
come drag associated with moving in a forward dir-
ection. Aquatic animals, on the other hand, need
not worry much about supporting their weight,
because the density of their bodies nearly matches
that of water. Most aquatic animals therefore are
neutrally, or slightly negatively, buoyant in water.
The higher density and viscosity of water, however,
means that drag poses a formidable obstacle to their
movement. Consequently, drag reduction is crit-
ical, particularly at moderate to large size.
Differences in the oxygen content and heat capacity
of the two media also affect the activity levels and
locomotor strategies of animals. The greater oxygen
content of air generally affords higher levels and
broader strategies of activity for flying and running
animals versus swimming animals. The higher heat
capacity of water further constrains the locomotor
capacities of swimming animals by making it more
difficult for them to maintain a warmer body
­temperature than their surrounding environment.
However, there are many exceptions to these g ­ eneral
rules. Aquatic and cold-acclimated animals have
evolved, and can adaptively express, metabolic
en­zymes that work well at low temperatures, enab­
ling them to compensate for a colder environment.
In addition, differing metabolic pathways for energy
production afford animals varied locomotor strat-
egies for daily activity that enable equally success-
ful performance compared with that achieved by
warmer animals.
1.2 Physics and energetics of movement
Animals move by exerting forces (F, measured in S.I.1
units of Newtons, N) on their external environment,
 P H YS I C A L A N D B I O L O G I C A L P R O P E RT I E S A N D P R I N C I P L E S
whether it is a solid substrate, air, or water. By
Newton’s First Law:
F = ma (1.1)
where m is the mass (in kilograms, kg) of the body
moved and a is its acceleration (m/sec2). Therefore,
an animal’s weight is a force produced by the accel-
eration of Earth’s gravity acting on its mass (m g).
To move its body, an animal must do work (W):
W = Fd (1.2)
where d is the distance (in meters, m) that the ani-
mal’s body moves as a result of the net force acting
on it, in reaction to the forces that the animal trans-
mits to the environment. Work (in Joules, J) repre-
sents the mechanical energy required to move the
animal’s body. The amount of mechanical energy
required to move per unit time,
= =
P W /t Fd/t = Fv (1.3)
represents the mechanical power (P, in Watts) of
locomotion, and thus can be related to the forces
that an animal exerts as it moves a given distance
per unit time, or the velocity (v) of its movement.
The energetic efficiency (Eff) of an animal’s move-
ment can be calculated by comparing the metabolic
energy consumed (energy input) to the mechanical
work (energy output) performed over a given
period of time:
Eff = Energy Out / Energy In (1.4)
= Work/Metabolic Energy
(1.5)
or equivalently, the mechanical power output ver-
sus the metabolic power input (Pout / Pin ) . Typically,
locomotor efficiencies are determined by compar-
ing the oxygen consumption of an animal with the
mechanical work performed over an integral num-
ber of strides. Because all animals must ultimately
balance their energy needs by means of aerobic
(oxygen-dependent) metabolism, measurements of
oxygen consumption are commonly used to assess
the energy supply of ATP needed for sustainable
locomotor activity. Typically, a value of 20.1 kJ/liter
O2 is used. This value assumes that ATP is produced
by means of aerobic glycolysis (the breakdown of
glycogen into glucose and its transformation via
glycolysis and the Kreb’s cycle into ATP production
3
within the mitochondria by electron transport and
oxidative phosphorylation).
1.3 Biomechanics of locomotor support
The forces required for locomotion are typically gen-
erated by the motor proteins within muscles, which
are transmitted to the external environment by means
of a skeleton. These forces cause deformations in the
structures that transmit them. The ability of a struc-
ture to resist deformation when subjected to a given
force is a measure of its stiffness and is the slope of a
structure’s force-length relationship (Fig. 1.1a). Linearly
elastic structures are defined as having a linear force-
length relationship, typical of a simple spring that
is stretched. Although linear elasticity is easier to
analyze, many biological structures exhibit non-
­
linear elasticity. Because larger structures can support
larger forces, engineers commonly normalize for dif-
ferences in the size of structures by dividing the force
acting on a structure by the structure’s cross-sec-
tional area (A, Fig. 1.1b). When normalized in this
way, a force is defined as a stress (Greek sigma, σ):
σ = F/A (1.6)
Common units of stress relevant to the musculo-
skeletal systems of animals during locomotion are
=
N/mm 2
=
( 10 6
N/m 2 1 MN/m 2 , or 1 MPa), or
N/cm ( = 10 kN/m 2 , or 10 kPa). Because these
2
units of stress may be new to many readers, and also
counterintuitive, a useful example is that the weight
of an apple (about 1 N, certainly an apropos ­definition
of a Newton!) balanced on the end of a toothpick (of
1 mm2 cross-sectional area) exerts a stress of 1 MPa.
Whereas forces act on structures, stresses can be
thought of as being transmitted through the struc-
ture. Large structures also undergo larger deform­
ations than smaller structures. Once again, in order
to account for differences in size, deformations or
changes in length are normalized by dividing by
the structure’s resting (unloaded) length (Fig. 1.1b,c),
and are defined as a strain (Greek epsilon, ε):
ε = ∆L / L (1.7)
As engineering terms, therefore, stress and strain
have quite distinct meanings. However, whereas strain
represents the real physical deformation of a struc-
ture in response to being loaded, the stress acting
within the material represents a conceptualization
4 A N I M A L L O C O M OT I O N

(a) Structural properties (b)

F F
Linear spring F
4F A A
F A
k L

Force
= L 4A
Slope ΔL ΔL
ΔL 4L
=k
F
F F
x
Deformation (ΔL) 4F 4 × ΔL

Material properties
F
(c) F Force and length change not equivalent
σ Stress and strain equivalent
Stress (F/A)

Slope
=E

Strain (ΔL/L)
ε

Figure 1.1 The mechanical properties of structures can be defined by how they deform in relation to different applied loads. (a) When a force (F)
is applied to a structure with cross-sectional area (A), it deforms a given length (∆L). In linearly elastic structures, such as this spring which is
lengthened linearly with the application of a force, the slope of force versus deformation represents the spring stiffness (k). (b) The response of a
structure to a load varies in relation to its size. Size can be measured in terms of length or cross-sectional area. Structural properties, such as
stiffness, k, in (a), do not account for size and thus vary across these examples. In contrast, material properties account for size by incorporating
relative length or cross-sectional area; these examples are equivalent in terms of stress and strain. (c) Stress and strain are normalized for
differences in size and thus reflect the material properties of a structure. The slope of stress versus strain represents the elastic modulus (E) of a
material.

of the intensity of force transmission. Finally, by
considering the size-independent properties of a
material, stress and strain have an equivalent rela-
tionship to that of force and length (Fig. 1.1c), in
which the stiffness of the material is the slope of the
stress-strain relation, and is defined as the elastic
modulus (also known as “Young’s modulus,” E):
E = σ /ε
The force that causes a structure to break (Fig. 1.1a)
corresponds to the strength, or maximum stress
(Fig. 1.1c) that a structure can bear before failing.
This also defines the strain at failure. The area under
the force-length curve represents the amount of
energy ( 1/2 F × d , for linearly elastic elements) that
is absorbed by a structure when it is loaded (Fig. 1.2a).
Similarly, the area under the stress-strain curve rep-
resents the amount of strain energy absorbed per
unit volume of material ( U* = 1/2σ ε ; Fig. 1.2b). If a
structure is unloaded before breaking, this energy
can be recovered elastically (much like a rubber
ball or an elastic band) and may be used to do
work. Elastic structures exist within animals that
can be used to store and recover elastic strain energy
and thus reduce the work and metabolic cost of
locomotion.
The elastic modulus and the energy absorbed
before failure defines whether a material is “rigid”
or “compliant” and “brittle” versus “tough.” Rigid
(1.8)
materials deform little when loaded and have a
high elastic modulus, whereas compliant materials
undergo considerable strain for a given load and
have a low modulus. Tough materials absorb
considerable elastic strain energy before failing,
whereas brittle materials, such as glass, absorb very
little (Fig. 1.2c). Generally, tough materials are not
as rigid—i.e. they have a lower elastic modulus—as
brittle materials. On the other hand, although brittle
materials may have a high failure strength and elas-
tic modulus, they often fail relatively easily, especially
when subjected to impact loads. Consequently, the
amount of energy absorbed to failure is a measure
 P H YS I C A L A N D B I O L O G I C A L P R O P E RT I E S A N D P R I N C I P L E S 5

(a) (b)

Ff σf

Stress
Force
Lf
σo U*

εo εf
Deformation Strain

(c) ‘Brittle’ ‘Rigid’

‘Tough’
U*1
U*2 U*2 >> U*1
Stress

‘Compliant’

Strain

Figure 1.2 The response of materials and structures to force and deformation yields information about stored energy, failure, and overall
behavior during loading. (a) The energy absorbed by a structure when loaded is equal to the area under its force-deformation curve (for linearly
elastic structures this is 1 / 2F × ∆1). The structure will break if force (Ff ) or deformation (Lf ) reach the threshold for failure. (b) The area under a
material’s stress-strain curve also represents the energy absorbed per unit volume (U*; hatched area represents energy absorbed to failure and gray
area represents energy absorbed at a maximum operating stress (σo) and strain (εo)). Typically, σo and εo of a material are much less than its
failure stress (σf) and failure strain (εf). The ratio of a material’s failure stress relative to its operating stress (σf /σo) is often used to define the
safety factor of a material or a structure. (c) The slopes of stress-strain curves can be used to compare the response of a material to loading. When
stress increases rapidly with a small amount of strain, the material is “brittle”. In contrast, slow accumulation of stress with increasing strain
indicates a compliant material. Tough materials store a much larger amount of energy (U*2) compared to brittle materials (U1* ).

of the material’s “toughness.” Because biological
structures are often subjected to dynamic loads,
their ability to absorb strain energy is often the crit-
ical factor determining whether they break. In gen-
eral, most biomaterials have evolved designs that
enable them to be tough, so that they can absorb a
considerable amount of energy before breaking. As a
result, rigid biomaterials, such as bone or insect c­ uticle,
exhibit a stress-strain relationship intermediate to
brittle and compliant materials (Fig. 1.2c).
1.3.1 Modes of loading
The mechanical loading of support structures con-
sists of four types of loads: 1) axial tension, 2) axial
compression, 3) bending, and 4) torsion (Fig. 1.3).
When subjected to axial loads, the stress developed
depends only on the structure’s cross-sectional area
relative to the magnitude of the applied load.
Tension is defined as an axial load that elongates a
structure, whereas compression is defined as a load
that shortens the structure along a given axis. When
subjected to bending, both tensile and compressive
stresses act within a structure (Fig. 1.3b). Compression
occurs on the concave surface and tension on the
convex surface, with the greatest stress acting at the
surfaces in the plane of bending. Consequently, there
is a gradient of stress (and strain) from ­maximum
compression on one surface to maximum tension
on the opposite surface (Fig. 1.3c). This means that
midway through the structure’s cross-section a neu-
tral plane exists where stress and strain are zero. If a
structure is subjected to bending and axial compres-
sion or tension, this will cause a shift in the neutral
plane, displacing it from the midpoint of the sec-
tion. Unlike axial compression or tension, stresses
due to bending depend on the shape of the cross-
section as well as its size. This is because material
located near the neutral plane of bending experi-
ences lower stresses.
Beam-like elements with hollow, rather than solid,
cross-sections therefore provide much better resistance
6 A N I M A L L O C O M OT I O N

(a) such as the long bones of a vertebrate limb, are more

+ΔL L
F likely to experience large bending-induced stresses
F Tension
−ΔL A
−F −F Compression
(b) Bending
−M +M
L /2
Cantilever bending
L
−M
(c)
Compression −ε
Strain
Tension ε=0 +ε
(d)
Torsion
Figure 1.3 Biological (and synthetic) structures are subjected to a
variety of loading modes. Whereas (a) long-axis (axial) tension and
compression result in uniform stress or strain distributions across the
cross-section of a beam, (b) bending and torsion produce non-uniform
gradients of stress and strain. (c) In the case of bending, maximum
tension and compression occur on opposing surfaces with a plane of
zero strain across the beam’s midsection (neutral plane of bending).
(d) In torsion, the location of zero strain is an axis running through the
center of the beam. Typically, bending and torsion produce much
greater strains, with the possibility of failure, than when a structure is
loaded in tension or compression.
to bending for a given weight (Fig. 1.3c). This is why
bicycle frames and many other structures (tent
poles) are constructed with a tubular design. For the
more ambitious reader, the mechanical basis of this
shape factor, termed the second moment of area,
is provided in engineering texts (e.g. Beer and
Johnston, 1981; Wainwright et al., 1976). A symmet-
ric tubular shape is favored when a range of bending
loads in various directions are likely to act on the
structure. Finally, the stresses developed in bending
depend not only on the magnitude of the bending
force (Fb), but the bending moment ( Fb × L / 2 , in the
case of bending stresses developed at a midpoint of
a beam, Fig. 1.3b left; and Fb × L , in the case of stresses
at the base of a beam subjected to cantilever bend-
ing, Fig. 1.3b right). This means that longer beams,
than short elements, such as the vertebrae.
In addition to axial loading and bending, struc-
tures may also be loaded in torsion, which involves
a rotational moment applied about the long axis of
a beam-like structure (Fig. 1.3d). As with bending,
cross-sectional shape also influences how well tor-
sion is resisted. In this case, shape depends on the
distribution of material away from the neutral axis
of torsion (for a circular beam this is the midpoint of
the cross-section). In general, biological structures
that effectively resist bending also provide effective
resistance to torsional loads. Strong twisting of the
body about a structural member is not common in
the natural movements of most animals, but there
are contexts when enabling twisting can reduce fail-
ure, such as in coral arms that twist in response to
flow, or accommodate failure, such as in long insect
legs that twist slightly or buckle when launching
rapidly (Bayley et al., 2012; Etnier, 2003; Vogel, 2007).
When twisting happens suddenly and without mech-
anisms to reduce stresses, such as when a ski’s bind-
ing fails to release in response to a twisting motion
of the skier’s body, unfortunate consequences often
result!
1.3.2 Safety factors
Like human-engineered devices, biological struc-
tures are designed (by means of natural selection) to
have a “factor of safety” in order to reduce their risk
of failure. Safety factors are often defined in terms of
the ratio of a structure’s strength relative to the max-
imum stress that it is likely to experience over its
lifetime of use ( σ f / σ o , Fig. 1.2b). Engineered struc-
tures are typically built to have safety factors as high
as ten. This means that the maximum anticipated
load would not exceed one-tenth of the structure’s
maximum load capacity. With a safety factor of ten,
the chance of failure is quite low; a comforting fact
when using an elevator to move up several floors of
a tall building! With more stringent performance
requirements (such as aircraft, which must minimize
weight) or a lower cost for failure, the safety of a
structure may be less. Safety factors might also be
defined in terms of toughness and strain energy.
However, because these are often much more diffi-
 P H YS I C A L A N D B I O L O G I C A L P R O P E RT I E S A N D P R I N C I P L E S
cult to measure, stress is most often used to define a
structure’s safety factor.
Biological safety factors are generally less than
the safety factors of engineered buildings and
mechanical devices; more often ranging between
two and eight. For example, in order for the tibia of
a gazelle, which has failure strength of 200 MPa, to
maintain a safety factor of four during fast gallop-
ing or jumping, the size of its tibia and its manner
of loading must ensure that the maximal stresses
developed within the bone do not exceed 50 MPa
during these activities. The lower safety factors of
biological structures are likely due, in part, to the
fact that animals must also pay a price for main-
taining and transporting the mass of their tissues
when they move. This cost is likely balanced against
the benefit of a reduced risk of failure (Alexander,
1981). Finally, it is likely that the failure of struc-
tures that would most reduce an animal’s fitness,
such as a primary limb bone versus a distal phal­
anx or a feather shaft, would favor a higher safety
factor. The relative incidence of bone fracture
within thoroughbred race-horses appears to pro-
vide evidence of this: fracture is highest in the dis-
tal limb bones, lower in the proximal femur and
humerus, and lowest in the vertebral column and
skull (Currey, 1981).
l
a d
l∝L∝d∝D
a ∝ l 2∝ d 2
a∝A
Figure 1.4 Geometric scaling strongly influences the relative dimensions of differently sized animals. For example, while length dimensions scale
linearly across different animals, area (A) scales with the square of length.
7
1.4 Scaling: the importance of size
Size is arguably one of the most important variables
affecting the function and form of organisms. This
is because changes in size during growth and over
evolutionary time impose changes in the relative
dimensions of organisms that have important func-
tional consequences. Many physiological processes
and mechanical properties depend on key struc-
tural dimensions, such as surface area or thickness,
which change dramatically with changes in size.
When differently sized structures retain the same
shape, they are considered to scale isometrically,
or to be “geometrically similar.” For geometrically
similar structures (Fig. 1.4), all linear dimensions scale
in proportion to one another. That is, Lengths (L) are
proportional to diameters (D); areas (A) are propor-
tional to L2 or D2, and to volume (V)2/3.
As a result, area-dependent processes change at
a different rate with respect to processes that are lin-
ear- or volume-dependent. This is important for
both the physiological and mechanical functions of
organisms. For example, the capacity of animals to
sustain activity depends on their ability to transport
oxygen and fuel substrates to the mitochondria inside
their muscle fibers. Ultimately, this depends on the
rate of diffusion across cellular and mitochondrial
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