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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
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Second Edition published in 2018
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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 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
8 A N I M A L L O C O M OT I O N

membranes, which in turn depends on the surface-
area of exchange surfaces. However, if the energy
demand or work required to move the animal
depends on its mass (or volume), this poses a scale-
dependent constraint of energy supply relative to
energy demand that is proportional to A/V or
V −1/3 (equivalent to M −1/3 ) for geometrically simi-
lar animals. In other words, a 100-fold increase in
size can be expected to impose nearly a five-fold
reduction in an animal’s capacity to fuel its activity.
This would mean that an animal’s mass-specific
metabolism, defined as the amount of energy that
each gram of its tissue requires to meet its metabolic
needs, would decrease five-fold due to the decrease
in surface area relative to volume at a larger size.
The effect of size on energy metabolism associated
with fueling locomotor activity is discussed at length
in Chapter 3.
A similar area versus volume constraint operates
with respect to mechanical support. This is because
stress depends on force per unit area, which means
that stresses are likely to increase with size (again,
for a 100-fold increase in mass, weight-related stresses
can be expected to increase nearly five-fold). Unless
the tissue strength of the skeleton increases in a
similar fashion, the risk of failure may become
exceedingly high. For animals built of similar
mater­ials, this means that they must either evolve
mechanisms for reducing the weight-related forces
gen­erated within their musculoskeletal systems or
drastically restrict their performance.
To a certain extent, animals may deviate from
geometric similarity, in order to compensate for
the scale effects of size. When this happens distor-
tions of shape, or allometric changes in structural and
functional properties, occur with size. Allometric

(a) 14

12

10 area vs volume0.75

8
Area

(b) 3.5
6 3 isometric
isometric 2.5
Length

4 2
1.5
2 1 length vs volume0.25
0.5
0 0
0 10 20 30 0 10 20 30
Volume Volume
(c) (d)
Positive
allometry
Log Y

Log area
Negative
Log length allometry a

Log volume (or log mass) Log X

Figure 1.5 Scaling of morphological and physiological features can be compared on arithmetic or logarithmic coordinates. The shape and
variation in scaling relationships are illustrated in terms of (a) area versus volume and (b) length versus volume on arithmetic coordinates and (c)
on logarithmic coordinates. The isometric scaling pattern is depicted as a grey line in each graph and the allometric relationship is shown as dark
line. Scaling of area vs volume is positively allometric and length vs volume is negatively allometric. (d) Given the typical scatter of biological data,
a least-squares linear regression fit of the logarithmically-transformed data is used to determine the scaling exponent (slope, b) and coefficient
(y-intercept, a) of the exponential relationship: Y = aX b.
 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
scaling might reflect, for example, either a relative
shortening or lengthening of an element or its rela-
tive thickening or thinning for a given mass or
area. When the scaling change is greater than that
expected for isometry, it is defined as positive
allometry; when less than the isometric expectation,
it is defined as negative allometry. Even m ­ oderate
allometric scaling requires substantial distortions
in shape when size changes over ­several orders of
magnitude (Fig. 1.5). A good example of positive
allometry is the scaling of mammalian lung sur-
face area (Fig. 1.6a), in which lung surface area
was found to scale with a slope of 0.92 when plot-
ted on logarithmic axes. This indicates that the
lungs of larger mammals are much more finely
partitioned than would be expected if geometric-
ally similar to the lungs of small mammals. The
observed scaling of lung surface area also suggests
a greater aerobic capacity for locomotion than if
the lungs of larger animals remained isometric in
design (see Chapter 3). In a more recent re-analysis
of morphometric data for respiratory surface area
of both ectothermic and endothermic air and water
breathers that incorporated phylogenetic effects
(Gillooly et al., 2016), similar positive allometric
scaling was found for endothermic respiratory
surface area ( slope = 0.89 ) , which exceeded the
scaling of respiratory surface area in ectotherms
( slope = 0.78 ; Fig. 1.6b). This provides an example
in which the scaling of a key structural feature of
the lungs, important to diffusive gas exchange, can
be related to the metabolic demand for gas
exchange. If, on the other hand, differently sized
animals retain a similar shape (i.e. scale close to
geometric similarity) alternative mechanisms must
evolve to compensate for functional constraints of
size. We will see how size affects locomotor mech-
anisms. Indeed, much of the locomotor diversity
of animals reflects this fundamental aspect of their
biology.
1.4.1 Allometric equation
Geometric or allometric scaling of physiological
functions and structural dimensions can be related
to changes in size by the exponential equation,
Y = a Xb (1.9)
9
where b is termed the “scaling exponent” and a is
the “scaling coefficient” relating changes in variable
Y to changes in variable X. This equation can be lin-
earized by means of logarithmic transformation:
log Y = log a + b log X (1.10)
in which case, the scaling exponent becomes the
slope, b, and log a is the Y-intercept of the line relat-
ing log Y to log X (Fig. 1.5d). Frequently, base-10
logarithms are used to linearize the exponential
relationships describing the structural and physio-
logical scaling of organisms (as in Fig. 1.6a).
However, natural logarithms (ln, base e) are some-
times also used (as in Fig. 1.6b). The linear relation-
ship described by Eq. 1.10 has the benefit of allowing
data to be graphed over several orders of magni-
tude and the use of regression methods for statistical
evaluation of empirically determined relationships
between two variables. Such “bivariate plots” com-
monly have scatter around the predicted scaling
line, which provides a measure of how strongly cor-
related the two variables are with respect to each
other. Deviations from the observed scaling pattern
may also provide important insight into how a par-
ticular species has evolved a distinctive functional
design. Chapter 9 (Evolution) discusses in greater
detail how scaling analyses are performed across
the phylogenetic relationships of animals.
1.5 Dimensions and units
It is important (and of practical use) to distinguish
between dimensions and units in describing and
analyzing the design of organisms. Dimensions rep-
resent the fundamental physical features of a variable.
Variables such as force (F) are defined in terms of
mass (M) and the mass’ acceleration (a). Similarly,
velocity is defined in terms of the dimensions length
(L) per unit time (T). The quantitative measure of
dimensions is expressed in terms of units. Conse­
quently, depending on the set of units used to meas-
ure them, variables will have different values. Units
for force may be a dyne, a Newton, or pound. Units
of length may be inches, centimeters, or meters. The
Standard International (SI) system of units has been
adopted throughout the scientific community and
is the system that will be used in this book. Because
it is a metric system, forces are measured in Newtons,
10 A N I M A L L O C O M OT I O N

(a)
1000
Giraffe
Slope = 0.92 Eland
Wildebeest Camel
(isometry predicts 0.67) Zebu cattle
Alveolar surface area (m2) 100
Gazelle
Sheep
Goat

Dik-dik
10 Suni

Genet cat

1 Dwart mongoose

0.1 1 10 100 1000

Body mass (kg)

(b)

15
ln(respiratory surface area)

Slope = 0.89

10

Slope = 0.78

0 4 8 12
In(Body Mass)
Ectotherms Endotherms

Figure 1.6 The scaling of respiratory surface area with body mass in vertebrates exhibits positively allometric slopes, indicating strong selection
for pulmonary diffusion capacity so that oxygen uptake meets the increased metabolic demand for oxygen delivery at larger size. (a) For terrestrial
mammals, lung alveolar surface area scales with as slope of 0.92. Adapted from Gehr et al. (1981). (b) When accounting for phylogeny and considered
more broadly across endothermic birds and mammals, respiratory surface area scales similarly to the non-phylogenetic analysis shown in (a). The
slope for endotherms (0.89) exceeds the slope for ectothermic vertebrates (0.78). Isometric or geometrically similar scaling would predict a slope
of 2/3 (or 0.67). Adapted from Gillooly et al. (2016).
 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
lengths in meters, and ­velocities in meters per sec-
ond (m/s).
All biological and physical variables can be defined
in terms of three fundamental dimensions: length,
mass and time. Several variables with their com-
monly used dimensions and fundamental dimen-
sions are shown in Table 1.2. These dimensions
provide a means for ensuring that equations are
dimensionally correct (which is of equal, if not greater,
importance than being quantitatively c­orrect; as
quantitative accuracy depends on dimensional
accuracy). This, in turn, can often help to identify a
key variable that may be missing from the equa-
tion, if the equation is found to be dimensionally
incorrect.
1.6 Summary
In this first, foundational chapter of Animal Loco­
motion, we launched a series of key ideas that will
reappear throughout the book. The media in which
animals locomote are important not only to the gen-
eration of locomotor forces, but also to the ability
to acquire enough oxygen to power the motion.
Table 1.2 The dimensions of key biological variables used for
dimensional analysis.
Variable Common dimensions Fundamental dimensions
Force Mass and acceleration MLT −2
Velocity Distance and time LT−1 (equivalent in this case)
Work Force and distance ML2T−2
Stress Force and area ML−1T−2
11
The contrast in density between water and air has
major consequences for the large drag forces that
must be overcome in water, as well as for heat
transfer and oxygen access. In order to generate
forces, animal structures must resist and accom-
modate loads. The characterization of load on bio-
logical structures therefore revolves around force,
length changes, cross-sectional area and the mode
of loading, such as bending. In addition, biological
structures and materials must accommodate energy
without failure, which is measured in terms of
compliance, toughness, rigidity and ­brittleness, and
also in terms of safety factors, which represent the
factor above normal loads that an animal can with-
stand without breaking. Scaling is fundamental to
locomotion—not just in terms of the size and forces
of locomotion, but also the access to oxygen across
sizes given the substantial differences in the way
that surface area and volume scale relative to length.
These basic principles will appear throughout the
book as we explore the media through which ani-
mals locomote as well as the scaling, biomechanics
and energetics that accompany the diversity of loco-
motor mechanisms and environments.
Additional reading
Alexander, R. M. (1983). Animal Mechanics, 2nd ed. London:
Blackwell Scientific.
Vogel, S. (2013). Comparative Biomechanics: Life’s Physical
World. Princeton, Princeton University Press.
Wainwright, S. A., Biggs, W. D., Currey, J. D. and Gosline,
J. M. (1976). Mechanical Design in Organisms London:
Arnold.
 CH A PT ER 2
Muscles and Skeletons
The Building Blocks of
Animal Movement
Animal locomotion depends on the organization,
physiology and biomechanical properties of mus-
cles and skeletons. Musculoskeletal systems encom-
pass the mechanical interactions of muscles and
skeletal elements that ultimately transmit force for
movement and support. Muscles not only perform
work by contracting and shortening to generate
force, they can also operate as brakes to slow the
whole body or a single appendage. Muscles can
also function as struts (rod-like) to maintain the
position of a joint and facilitate elastic energy
storage and recovery. Skeletal muscles share a
­ ric. Ideal isometric contractions result in zero work
basic organization and all rely on the same protein
machinery for generating force and movement.
Variation in muscle function, therefore, depends
on the underlying mechanical and energetic com-
ponents, enzymatic properties and activation by the
nervous system. Muscles require an internal, exter-
nal or hydrostatic skeletal system to transmit force
for movement and support. In the vertebrates and
arthropods, muscle force transmission occurs through
jointed skeletal segments and levers. The variation
and mechanics of musculoskeletal systems enable
animals to support themselves and move through
their diverse environments.
2.1 Muscles
In order to function as biological motors, muscles
generate movement by doing work. Muscles do this
by exerting force (F) while shortening (change in
length, ΔL). Hence, the term “muscle contraction.”
The product of force and length change equals work
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
(W = F∆L) , which is measured in terms of joules
( N m ) . Muscles most commonly change length
over distances of millimeters, so that the work they
perform is given in millijoules (mJ). Work per unit
time, in turn, equals the power ( P = F∆L / ∆t ,
1 Watt = 1 J/s ) produced by a muscle. By definition,
muscles produce positive power when they shorten
(decreases in length are defined as being positive).
However, as we will see, muscles can also function
to generate force with little or no change in length,
in which case the contraction is referred to as isomet-
and power. Muscles can also maintain a constant
force while changing length (isotonic contraction).
Other muscles may lengthen as they generate force
(e.g. lowering a barbell during a biceps workout),
thereby absorbing energy and doing negative work
(ΔL is defined as negative in this case).
2.2 Molecular organization: mechanism
of force generation and shortening
In skeletal muscles, overlapping sets of actin and
myosin filaments are arranged in repeating units
called sarcomeres along a muscle fiber’s length
(Fig. 2.1). Each sarcomere is comprised of two sets
of actin filaments extending from either end (z-disc)
of the sarcomere. The actin filaments overlap by
interdigitating with the myosin filaments that extend
from the sarcomere midline. The sarcomeres are
organized in series (joined together at neighboring
z-discs) and form a myofibril that runs end to end
within the muscle fiber. This regular patterning and
 M U S C L E S A N D S K E L E TO N S 13

(a) (b) (c)

Filament
t
Mitochondria

Z-disk mc

I-band Transverse M
tubules
sr
Sarcoplasmic
Sarcomere

reticulum
A-band
d
(d) (e)
Motorneuron
Z-disk

Sarcolemma

Fibrils

Figure 2.1 Cross-striated and obliquely-striated muscles are formed by hierarchical structuring and organization of actin and myosin filaments
into sarcomeres. (a) Striated muscle is made of muscle fibrils within which the filaments [thin (actin) and thick (myosin)] form sarcomeres. The actin
thin filaments connect to the Z-disks and form a characteristic banding pattern with the lighter I band around each Z-disk, where the actin
filaments attach, and the darker A band which extends the length of the myosin filaments. Muscles are powered by ATP produced by the mitochon-
dria that are spread throughout muscle cells. The transverse tubules (T-tubules) conduct an arriving stimulus from a motorneuron to stimulate Ca2+
ion release from the sarcoplasmic reticulum and trigger cross-bridge cycling and muscle contraction. Reprinted from Loeb and Gans (1986) with
permission from Elsevier. (b) In these transmission electron micrographs (TEM) of squid (Loligo pealei) the tentacle fibers exhibit a cross-striated
appearance (right image) whereas the arm muscles have obliquely-striated fiber arrangements (left image). Scale bar 1 μm. Image from Kier and
Curtin (2002) with permission of the Company of Biologists Ltd. (c–e) The hexagonal organization of myosin and actin filaments can be seen in
cross-section with insets (d–e) showing higher magnification images of the myofilament arrays. Synchronous insect flight muscle, large scale
bar = 1 μm, small scale bar = 0.1 μm; reproduced from Josephson et al. (2000) with permission of the Company of Biologists Ltd. Abbreviations: SR,
sarcoplasmic reticulum; M, myofilaments; t, tracheole; d, dyad (connection between SR and t-tubule).

organization of sarcomeres within the ­ myofibrils
creates a striped appearance when viewed under a
microscope. Therefore, these skeletal muscles are
often referred to as striated muscle (in contrast to
smooth muscles found in arteries, the gut and else-
where, which lack sarcomeric organization). In add-
ition to the cross-striated vertebrate and invertebrate
muscles, obliquely striated muscles are found in
annelids and cephalopods.
During a muscle contraction, myosin cyclically
attaches to and detaches from actin (cross-bridge
cycling) so that the actin and myosin filaments move
past each other in opposite directions. The flexible
heads of the myosin molecules, projecting from the
myosin filament, form the cross-bridges that attach
and detach in a cyclical fashion at binding sites
along the actin filaments. Myosin filaments are made
of a polymeric chain of myosin protein ­elements,
each consisting of a heavy chain and two light chains
that form a pair of globular domains at the myosin’s
“head” end. Each myosin head is flexible and cap-
able of undergoing conformational rotation in the
presence of ATP. ATP binds to each cross-bridge and
allows the myosin to release from the actin binding
site and re-attach to another binding site along the
actin filament. The actin filaments are comprised of
actin monomers organized into an extended double
helical chain. A recent study indicates that the num-
ber of myosin heads binding during contraction can
be modulated based on the load; high loads stretch
the thick filament increasing the number of add­
itional myosin heads that may form cross-bridges
(Linari et al., 2015).
Each cross-bridge cycle involves the hydrolysis
(splitting) of one ATP molecule. Chemical energy
released from ATP is converted into the force and
rotational movement of the myosin head. As a
result, myosin is both a machine that transforms
chemical energy into mechanical work and an
enzyme (myosin-ATPase) that hydrolyzes ATP. ATP
hydrolysis occurs at the final step of the cross-
bridge cycle when the myosin head detaches from
actin and is then free to seek another binding site.
ATP binding energizes the actin-myosin complex,
enabling the subsequent conformational rotation of
the myosin head. Rates of cross-bridge cycling (and
ATP hydrolysis) that underlie the speed of muscle
shortening and force development, therefore, can
14 A N I M A L L O C O M OT I O N
be assayed based on the myosin-ATPase activity of
a muscle’s fibers. Across muscle systems and spe-
cies, myosin occurs in different isoforms that yield a
large array of outputs in terms of myosin head rota-
tion rate, release, force and stroke distance.
Cross-bridge cycling begins when Ca 2+ is released
into the muscle cell and stops when Ca 2+ is removed.
Motorneurons transmit action potentials to the
­muscle fiber, causing a depolarization that spreads to
the sarcoplasmic reticulum (SR), which then releases
Ca 2+ from the SR into the ­muscle cell. The presence
of Ca 2+ allows myosin heads to bind to actin and ini-
tiates cross-bridge cycling. When the muscle con-
traction ends, Ca 2+ is actively pumped back into
the SR and the myosin heads can no longer bind to
actin. Release of Ca 2+ depends on the number of
motor-endplate potentials transmitted to the muscle
cell’s SR: with increasing ­depolarization frequency
of the muscle’s fiber, more Ca 2+ is released. An
increase in the number of Ca 2+ ions allows muscles
to generate force over shorter time periods. For
most muscles, the energetic cost of Ca 2+ release and
uptake by the SR is ~25 percent of the cost associ-
ated with force generation.
Force is generated only during one direction of
the rotational movement of the myosin head: the
bending of the myosin head toward the sarcomere
midline. Consequently, as force develops, the sarco­
mere becomes shorter, resulting in an increased
overlap between the thick and thin filaments. When
the contraction is completed, large elastic protein
molecules (titin) that extend from the thick fila-
ments to the z-discs, restore the sarcomere back to
its resting position while also mediating the overall
stiffness of the sarcomere. The multiple cycles of
myosin attachment, force generation and shorten-
ing, detachment, and subsequent re-attachment are
summed across the sarcomere and along the length
of the myofibrils, yielding an overall shortening of
the muscle fiber and, ultimately, force generated at
the ends of the muscle.
2.3 Levels of force generation and the
isometric force-length relationship
The force generated by a muscle arises at multiple
structural scales and results from the activation
dynamics of sarcomeres and the muscle fibers they
populate. This section examines force generation
ranging from the level of myofilament overlap up
to the number of cross-bridges formed during a
muscle contraction. Whereas skeletal muscle force
per unit area of activated fibers is fairly constant
across vertebrates, ranging from 18–30 N/cm2; as a
result of differing actin-myosin filament lengths,
invertebrate muscles can generate specific forces as
high as 200 N/cm2 (Taylor, 2000).
The force of an actively contracting sarcomere
depends on the changing amount of overlap be­tween
the actin and myosin filaments during a contraction.
Within an actively contracting sarcomere, the chan-
ging effect of force development across varying
amounts of actin-myosin filament overlap is called
the force-length relationship (Fig. 2.2a) and constitutes
one of the fundamental properties of striated skel-
etal muscle. To examine the force-length relation-
ship, the force generated by a muscle at a sequence
of fixed lengths (isometric contractions) is meas-
ured experimentally. The initial discovery of the
force-length relationship was based on X-ray dif-
fraction images of myofilament overlap in sarcomeres,
combined with force measurements of isomet­ric con-
tractions in which the muscle was held at these dif-
ferent amounts of myofilament overlap (Gordon
et al., 1966).
This classic study revealed that as actin and
­myosin filaments increasingly overlap in shortened
sarcomeres, active force increases, but only up to a
maximal level of force. Once maximal force is achieved,
the force plateaus and then decreases as actin and
myosin filaments overlap further in shortened
sarcomeres. Excessive overlap of the actin filaments
causes disrupted spacing within the myofilament
lattice. With increasing overlap, the actin filaments
increasingly interfere with one another, block effect-
ive myosin cross-bridge binding, and ultimately
reduce contraction force. At extremely short sarco-
mere lengths, the myosin filaments push against the
z-discs. Force-length relationships suggest that
muscle fibers (and by implication, muscles) should
operate at an ­ intermediate range of sarcomere
lengths (typically ±5 percent to ±15 percent of the
optimal s­ arcomere length) to enable maximal force
development. The dependence of force on the
length of the contracting sarcomere is further influ-
enced by the change in position and orientation of
 M U S C L E S A N D S K E L E TO N S 15

(a)

Isometric force
40% 100% 160%
Percent resting length of sarcomere

(b) Ls
Rest 10 Ls Net
–20% 8 Ls 2 Ls

Rest 5 Ls Net
–20% 4 Ls 1 Ls

Figure 2.2 Muscle force can be modified at several levels of organization of a sarcomere. (a) The amount of overlap between thin (actin) and
thick (myosin) filaments defines the isometric force-length curve for striated muscle exposed to a series of isometric contractions at different
lengths. Maximum isometric force occurs when thick and thin filaments overlap such that the maximum number of cross-bridges can be formed
(Gordon et al., 1966). To the right along the force-length curve, force is lower when the sarcomere length (Ls) is long and the thick and thin
filaments have reduced overlap. On the left-hand side of the curve, force is lower because the excess overlap disrupts the actin-myosin spacing.
(b) The number of sarcomeres in series determines how the fractional shortening of individual sarcomeres sums to determine changes in fiber (and
whole muscle) length. As the number of sarcomeres increases, their summed change in length increases. Invertebrates can vary the length of the
sarcomere (Ls) in addition to varying the number of sarcomeres in series (not shown here). A longer sarcomere increases the amount of force
produced by the sarcomere, due to the increased number of cross bridges formed at a given instant, but decreases the speed of fiber shortening.

the myosin heads relative to actin filaments: in
order to maintain a constant volume in the muscle
fiber, the fibers bulge radially during contraction,
increasing the spacing between myosin and actin fila-
ments. This change in spacing steepens the slope of
the ascending and descending limbs of the force-
length relationship for insect flight muscle (Williams
et al., 2013).
Moving up in scale from the changing overlap
of actin and myosin that primarily defines a
­sarcomere’s force-length relationship, the force gen-
erated by a muscle fiber is also determined by the
total number of possible actin-myosin cross-bridges
within a sarcomere. The number of possible cross-
bridges is proportional to a sarcomere's length. The
sarcomere lengths of vertebrate skeletal muscles
are surprisingly uniform, typically falling in the
range of 2.0 to 2.8 μm, whereas invertebrate skel-
etal muscles exhibit a great diversity of sarcomere
lengths, 1.9 to 17.8 μm among arthropods and up
to 40 μm in annelid worms (Smith et al., 1973;
Taylor, 2000). Longer ­sarcomeres have longer myosin
and actin filaments, which means that more cross-
bridges can be formed with neighboring actin fila-
ments. As a result, longer sarcomeres are able to
generate greater force than shorter sarcomeres.
Differences in sarcomere length also affect the speed
of shortening of a fiber, with longer sarcomeres gen-
erally contracting at slower speeds.
The number of sarcomeres within a fiber affects
the absolute change in length for a given fractional
shortening of individual sarcomeres. Longer fibers
allow a muscle to achieve a greater overall length
change for a given fractional length change of its
sarcomeres (Fig. 2.2b); muscles that undergo greater
length change (i.e. produce greater displacement)
are likely to have longer fibers (with more s­ arcomeres
in series) than muscles that function over shorter
displacements. Both vertebrates and invertebrates
vary the number of sarcomeres within a fiber to
adjust fiber length relative to the muscle’s func-
tional range of operating length.
The elastic properties of muscular systems—from
sarcomeres up to musculoskeletal attachment—
16 A N I M A L L O C O M OT I O N

(a) Inactive muscle passive elastic properties due largely to connective

tissue elements within the muscle. When an inactive
muscle is stretched from its resting length, it will
passively resist the imposed stretch by developing
Passive
force (Fig. 2.3a). Consequently, the force-length
Force

properties of skeletal muscles result from a combin-

ation of their active and passive components (Fig.
2.3b). While the force-length properties are critical
to understanding the molecular basis of muscle
force development and shortening, the passive
40% 100% 160%
elastic properties of muscles are important to their
behavior under in vivo conditions and cannot be
(b) Contracting pinnate muscle
overlooked. The passive elastic properties of mus-
cles depend on their fiber architecture and the
Passive + active
amount of connective tissue to which the fibers
attach within the muscle. Muscles with short fibers
Force

and more extensive connective tissue (see discus-

Active
sion of pinnate versus parallel fibered muscles in
Passive
Section 2.8) exhibit a steeper rise in their passive
resistance to stretch compared with longer fibered
muscles that have less connective tissue investing
40% 100% 160% the fibers (Fig. 2.3c).

(c) Contracting parallel-fibered muscle

2.4 Power, efficiency and the isotonic
Passive + active force-velocity relationship
In addition to the force-length relationship described
Force

Active in the previous section, the force-velocity (F–v) rela-

Passive
40% 100% 160%
Percent resting length
Figure 2.3 Muscles exhibit both active and passive force-length
properties. (a) When a resting muscle (i.e., not actively contracting) is
stretched from its resting length (100% length), connective tissue within
the muscle resists stretching and generates a J-shaped force-displacement
curve typical of compliant materials. (b) In a contracting pinnate muscle
with considerable connective tissue, active force generation builds from
~40% resting length starting point and then sums with its passive
connective tissue components once the muscle is stretched beyond its
resting length (100%). When stretched past resting length, the active
force declines and the stretch-resistance of the passive components
gradually increases. (c) In parallel-fibered muscles that have less
connective tissue, the passive component is much smaller than for a
pinnate muscle, (b) and there is a larger drop in tension at longer lengths.
mediate the force developed across varying amounts
of myofilament overlap (Fig. 2.3). In ­addition to
their active force-length properties, muscles possess
tionship represents a second fundamental property
of skeletal muscle (Fig. 2.4). The velocity of fiber
shortening (and lengthening) affects the amount of
force that a muscle can develop. Starting from an
isometric contraction (zero velocity; peak force, P0),
the velocity of shortening (v) increases and force
hyperbolically decreases until the muscle reaches
maximum shortening velocity (vmax) while approach-
ing zero force. The hyperbolic nature of the force-
velocity relationship was first described by A. V.
Hill in 1938, having previously won a Nobel Prize
in 1922 for his work on the energy and efficiency of
muscle contraction. As the speed of filament sliding
increases, fewer unbound myosin cross-bridge heads
are able to successfully bind to actin sites. Because
fewer cross-bridges form as a muscle shortens at a
higher velocity, the force developed by the muscle’s
fiber is reduced, thus resulting in an inverse rela-
tionship between fiber shortening velocity and
force development.
 M U S C L E S A N D S K E L E TO N S 17

(a) (b)

Muscle efficiency (work out/energy in)

0.25
efficiency 100% power

Percent maximum power

Po

Force

0.3 0.5 1 0.3 0.5 1

Lengthening Shortening v/vmax
v/vmax

Figure 2.4 The Hill isotonic force–velocity curve explains tradeoffs between force generation and contraction velocity while also revealing the
combination of force and velocity that allows a muscle to generate peak power output. (a) The Hill isotonic force–velocity curve for skeletal muscle
during muscle shortening and lengthening. When compared to peak isometric force (P0), muscle lengthening (x-axis negative values) can yield
much greater forces over short distances than occurs during muscle shortening (x-axis positive values). The x-axis variable (ratio of shortening
velocity (v) relative to maximum velocity (vmax)) is typically used, because it allows for comparisons across muscle sizes and speeds. (b) Maximum
muscle power (work per unit time) occurs at higher v/vmax on the force–velocity curve (~0.4 v/vmax) than maximum muscle efficiency (mechanical
work output/metabolic energy input) which occurs at 0.3 v/vmax on this graph. Efficiency and power both converge at zero when muscles contract
isometrically (zero velocity; v /v max = 0 ) and at maximal velocity (zero force; v /v max = 1 ). Therefore, muscle contraction rates are likely to vary
according to whether an animal is maximizing efficiency versus power or velocity output.

In addition to the examples of force development
during fiber shortening, muscles also generate force
when lengthening and, indeed, can briefly generate
much higher forces during lengthening than are
achieved during isometric contractions (Fig. 2.4a).
If a muscle contracts when loaded by a force that
exceeds its maximal isometric force, it will be
actively lengthened. This can occur, for instance,
when a person lands from a jump. Upon landing,
the knee extensor muscles contract to prevent the
legs from collapsing, are lengthened as the knee ini-
tially flexes and then are re-extended to absorb
the energy of the falling body. Active lengthening of
the extensor muscle occurs, because the weight of the
body exceeds the isometric (P0) contractile force of
the muscles’ fibers. With an increase in the rate of
lengthening, the force developed by a muscle rises
sharply. The additional force that the muscle gener-
ates while being actively lengthened is provided by
a rapid stretch of the myosin cross-bridges attached
to the actin filaments. This heightened level of force
(up to 1.8 times peak isometric force) can only occur,
therefore, over very short lengthening distances
and short time periods. At greater distances of fiber
lengthening, or longer time periods, the cross-bridges
detach and the additional elastic restoring force of
the cross-bridge is lost. Indeed, excessive muscle
stretch may be a leading contributor to m ­ uscle
injury. Active muscle lengthening and the enhance-
ment of force that it facilitates is thought to occur in
the locomotion of many animals, but it normally
happens over brief instances in time and short
length changes.
Given that force times velocity is equal to power,
peak-power output of a muscle can be predicted by
plotting the product of force and velocity from the
empirically-determined force-velocity relationship
(Fig. 2.4b). For most skeletal muscles, maximum
power is developed at about 0.4v / vmax. Therefore,
muscles that function to generate mechanical power
(e.g. flight muscles of insects and birds, axial mus-
cles of fish, mantle muscles that power the jetting
of squid) operate with shortening velocities in the
range that yields maximal power output. One inter-
esting consequence of peak power occurring at a
particular combination of muscle force and velocity
is that animals of larger body size or that are push-
ing against large loads may be constrained to oper-
ate at a different point on the force-velocity curve,
thus leading to sub-maximal power output. For
example, large animals that support substantial
body weight must operate their locomotor muscles
18 A N I M A L L O C O M OT I O N
with greater force and lower velocity, thereby decreas-
ing their power output and speed compared to
smaller animals. Even in aquatic systems with ani-
mals of varying body size, the dynamic effects of
size on drag forces cause frogs of different sizes
to operate at different points on the F–v curve
(Clemente and Richards, 2013) and thus fail to oper-
ate at optimal power output.
Also, key to a muscle’s performance is its effi-
ciency, yet peak efficiency occurs at a different
point on the force-velocity curve than peak power
(Fig. 2.4b). Muscle efficiency is defined as the
amount of work (force times distance) that a ­muscle
performs divided by the chemical energy (ATP)
that it consumes during a contraction. Because dir-
ect measurements of ATP use are difficult to make,
extremely sensitive thermal measurements of the
heat released by a contracting muscle (energy lost),
relative to the amount of work performed, have
provided a reliable alternative approach for meas-
uring muscle efficiency  = Work / ( Work + Heat )  .
These measurements have shown that the effi-
ciency of skeletal muscle is maximal at a lower
shortening velocity ( 0.3 v / vmax , Fig. 2.4b) than
the velocities that m ­ aximize mechanical power.
Consequently, when locomotor efficiency is more
important than power output, muscles can be
expected to contract more slowly than in circum-
stances when maximum power is required (e.g.
during a high-power escape response).
2.5 “Work loops”: time varying force-
length behavior of muscles
While the isometric force-length and isotonic
force-velocity relationships described have proven
extremely useful for understanding the design and
properties of different muscles, neither provides an
accurate description of how muscles function under
dynamic conditions. The force-velocity relationship
is determined by stimulating the muscle and allow-
ing it to shorten against a fixed load over a very
short range of length (<5 percent); however, in liv-
ing animals, muscles develop force and change
length under dynamic conditions, in which both
force and length change at different rates during the
period of a contraction. Consequently, the mechanical
and physiological properties of muscles are likely
to differ from the classical description of their
­force-length and force-velocity properties, which
are based on idealized isometric and isotonic
­contractile states.
The muscle work loop is a contractile method
(Josephson, 1985) for calculating net muscle work
by variably activating a muscle during imposed
sinus­oidal changes in length and force. For many
muscles that propel an undulating body or recipro-
cating limbs, the length changes of the muscle may
be approximated by a sinusoidal pattern of length
change. The particular timing of muscle activation
relative to its shortening and lengthening is critical
to the net work that the muscle performs during a
contraction cycle. The work loop technique varies
the length and activation of a muscle to examine
how these factors affect the force generated and dis-
tance of contraction—in other words, the varying
work output (∆F × ∆L) of the muscle.
Force development is examined during muscle
shortening and lengthening—in the example shown
(Fig. 2.5), a sinusoidal length pattern is imposed.
Work loop experiments measure the force that the
muscle develops when it is activated at varying pre-
set lengths. When activated so that the force devel-
oped by a muscle is greatest during shortening,
counter-clockwise vectors of force development cir-
cumscribe an elliptical region representing positive
work. In the small region of muscle-lengthening,
“negative” work is generated as the muscle is
stretched. Although somewhat nonsensical in the
context of physics, the term negative work is simply
a convention among muscle physiologists to dis-
tinguish between shortening, positive work and
lengthening, negative work performed by muscles.
Negative work represents the energy absorbed by a
muscle. When the work loop experiment is run
such that a muscle generates more force during
lengthening than shortening, the vectors change
direction to circumscribe an elliptical region in the
clockwise direction, thereby generating mostly
­negative work.
A muscle’s work performance is primarily deter-
mined by the timing and duration of muscle activa-
tion relative to the muscle’s changing length (Fig.
2.5) in relation to the magnitude of force developed.
When a muscle is activated, it generates force, but
 M U S C L E S A N D S K E L E TO N S 19

1 2 3 4
(a)
2

3 Force

Force
1
Net +

4
Length
Length
Activation
(b)
2

3
1
Force

Net – Length

4
Activation
Length
Time

Figure 2.5 Muscle work loops allow experimental examination of time-varying patterns of muscle force, activation patterns and length change
that are common to the in vivo locomotor behavior of many muscles. Work loops generated from sinusoidal oscillations of muscle force and length
yield positive (a, counter-clockwise) and negative (b, clockwise) work loops depending on whether the muscle is activated and force is generated
during muscle shortening (a) or lengthening (b). (a) In a positive work loop, the area in the center of the loop is the net work that the muscle
performs over the contraction cycle. The hatched area at lower right is the negative work (energy absorbed) by the muscle while being lengthened
during this phase of the cycle. The negative work is subsequently recovered when the muscle shortens, yielding the net work within the loop. The
muscle activity in a positive work loop occurs during muscle shortening. The zero phase of muscle activity is defined by the length of the muscle
and in this example, it occurs at point 1, when the muscle begins to shorten. (b) A clockwise “negative work loop” results from a delay in the
phase of muscle shortening and associated muscle activation. This causes the muscle to do little work while it is shortening (hatched region: Force
is low or zero) and absorb energy by developing greater force while being lengthened.

length changes can occur at varying time points
after force development begins. We can define
phase zero as the moment at which a muscle begins
to shorten. Activation of a muscle immediately
before the onset of shortening (negative phase: –0.1
to 0) and with a duration lasting midway through
shortening (relative phase: 0.25) is most favorable
for effective force development and subsequent
positive work during shortening (Fig. 2.5a). This
is because the initial period of muscle activation
occurs while the muscle is briefly being stretched
or develops force under near-isometric conditions.
From the force–velocity relationship (Fig. 2.4), we
know that muscles develop greater force under
these conditions. If activation of the muscle is
delayed until after it begins to shorten (relative
phase: 0 to 0.5), its ability to develop force and do
work during shortening will likely be reduced. If
activation of the muscle occurs later, when the
­muscle is nearly finished shortening, and the acti-
vation lasts into a substantial period of lengthening,
the muscle’s force-length behavior will result in a
clockwise (negative) work loop (Fig. 2.5b). Finally,
if a muscle’s activation is limited to when it under-
goes little, or no length change, it will develop force
isometrically and do little work (not shown).
Work loop experiments have provided insights
into the muscle properties underlying the dynam-
ics of muscle length change and force develop-
ment, which are thought to operate during in vivo
locomotor activity. Muscles that function to do
work and generate power (equal to the work per
contraction times the contraction frequency), such
as the leg muscles that power locust and frog
jumping, and the flight muscles of birds, character-
istically have broad counter-clockwise work loops
20 A N I M A L L O C O M OT I O N
(Fig. 2.5a). Fish axial body muscles have been
studied extensively using the work loop tech-
nique. These studies have examined the effects of
swimming speed in relation to cycle frequency,
length change, timing of activation, and tempera-
ture on the muscles’ ability to generate mechanical
power. During swimming, the axial musculature
on the convex side of the body’s bend is activated
to generate force just before shortening, during the
time when the fibers finish being stretched. This
allows the fibers to develop force rapidly, as they
subsequently shorten and the animal’s body to
bend in the opposite direction (becoming concave).
This local force is either transmitted posteriorly
down the length of the animal’s body to the tail or
is transmitted directly to the fluid adjacent to the
body surface for propulsion. Thus, muscle work is
transformed into hydrodynamic work. Traveling
waves of bending and fluid propulsion are driven
down the animal’s body in this way, by means of a
transmitted wave of electrical activation by the
nervous system to the muscles along the body
axis.
In contrast to the counter-clockwise positive work
loop of fish swimming, muscles that operate as
brakes to absorb energy, such as when overcoming
the inertia of a moving limb or decelerating the
body’s motion, can be expected to generate clock-
wise negative work loops (Fig. 2.5b). Finally, as
we’ll see in Chapter 4, muscles may also function to
contract economically by developing force with lit-
tle or no change in length, so that they do little net
work. When this occurs, the force-length behavior
of these muscles results in little or no area contained
within the loop. Indeed, in this case the term “work
loop” is a misnomer, and the overall pattern of
force-length behavior is actually much more similar
to that of a spring (see Fig. 4.12).
2.6 Excitation–contraction coupling
and motor units
In addition to the levels and dynamics of force gen-
eration described in the previous sections, the amount
of force developed by a muscle is also influenced by
the number of cross-bridges formed in parallel across
the myofilament lattice, which is ultimately deter-
mined by the number of muscle fi ­ bers stimulated
by the nervous system (see Chapter 8). Inverte­
brate and vertebrate skeletal muscle fi ­ bers can be
distinguished most generally as being either twitch
or tonic. When twitch fibers are activated, they
develop force, and when their ­stimulation ceases,
they relax. In contrast, slow tonic fibers can maintain
their tension for long periods of time by maintain-
ing cross-bridge attachment and limiting cross-
bridge cycling, well after their neural activation
has ended. As a result, slow tonic muscle fi ­ bers
provide a means for adjusting and maintaining ten-
sion at low energy cost for long time periods. We
primarily focus on the properties of twitch-type
skeletal muscle fibers, and the faster contracting
non-twitch fibers of invertebrates, in relation to
how they are recruited for adjustments in muscle
force, speed and endurance.
In the vertebrates, skeletal muscle fibers respond
in an all-or-nothing fashion as the depolarization
of the fiber spreads rapidly along the fiber’s length
from the motor endplate. As a result, they are
­considered “twitch” type fibers. The firing rate of
action potentials transmitted to the motor end-
plates influences the magnitude and time course of
force that the muscle develops by regulating the
amount of calcium that is released from the SR.
Nearly all vertebrate skeletal muscles that power
locomotion are comprised of “twitch” fibers, which
develop a characteristic pattern of force (Fig. 2.6)
in response to an endplate depolarization. Multiple
stimuli at slow to moderate frequencies result in
an “unfused tetanus” that yields an elevated, but
rippled force pattern (Fig. 2.6b). With an increase
in stimulation frequency, the magnitude of force
increases further (a property termed “summation”)
and achieves a smooth force plateau, or “fused
tetanus” (Fig. 2.6c). The stimulation frequency
required to elicit a fused tetanus is greater in faster
contracting muscle fibers. Faster contracting m ­ uscles
develop force more rapidly than slower contracting
muscles, but fatigue more quickly. In most instances,
vertebrate skeletal muscles generate fused tetanic
contractions during locomotion. For very fast ­muscles,
such as rattlesnake shaker muscle or humming-
bird flight muscle, this is the case even if the muscle
is activated with relatively few stimulating spikes
(Altshuler et al., 2010; Rome and Lindstedt, 1998;
Tobalske et al., 2010).

(a)
Relative force
Nerve stimulus
(b)
Relative force
Nerve stimulus
(c)
Relative force
Nerve stimulus
Time
Figure 2.6 Muscle force response to varying frequencies of stimulation in (a) a single twitch stimulus, (b) unfused tetanus, and (c) fused tetanus.
These patterns are for twitch-type muscle fibers. A fused tetanus is achieved when the stimulation frequency is high enough to produce a smooth
(and elevated) plateau in muscle force.
In the case of invertebrate muscles, a majority
of the fibers typically do not respond in an all-
or-nothing fashion. Instead, these fibers respond to
nerve stimulation by developing graded patterns of
­depolarization produced by multiple motorneuron
terminals that are distributed along the length of
the muscle fiber. Local motor junction potentials
sum over the length of the fiber to produce a net
depolarization in the fiber, as a whole. In addition,
invertebrate skeletal muscle fibers may also receive
inhibitory input from their motorneurons, in con-
trast to vertebrates whose motorneurons act solely
in an excitatory fashion. The graded activation of
invertebrate muscle fibers, therefore provides a
fundamentally different mechanism compared to
the vertebrates for controlling the force output of a
muscle.
M U S C L E S A N D S K E L E TO N S 21
Twitch
Unfused tetanus
Fused tetanus
Most skeletal muscles are activated directly by
motorneurons that innervate a subpopulation of
fibers within a muscle (except for the asynchronous
flight muscles of insects; see Chapter 6). A motor unit
consists of the motorneuron and the set of muscle
fibers that it innervates. In nearly all mammalian,
avian and reptilian muscles, adult muscle fibers are
innervated by a single motorneuron; however, in
some fish and amphibian muscles, as well as those
of various invertebrates, a muscle fiber may be
innervated by more than one motorneuron (poly-
neuronal innervation). In animals lacking polyneu-
ronal innervation, the fibers innervated by the
motorneuron (i.e. those comprising the motor unit)
share similar contractile properties. This may result,
in part, from a trophic influence of the motorneuron
on the fibers. In other words, the activation frequency
22 A N I M A L L O C O M OT I O N
from the motorneuron affects the biochemical and
contractile properties of the fiber(s).
Modulation of force output by twitch-type s­ keletal
muscles is therefore achieved by the ­nervous sys-
tem’s recruitment of motor units within a muscle
(covered in detail in Chapter 8). The number of
­fibers innervated by a motorneuron can vary. For
example, finer control of force can be achieved by
having a larger number of small motor units. The
steering muscles of flying insects can be innervated
by a single motorneuron. In this case, force is modu-
lated by varying the number and frequency of nerve
stimuli as well as the time-course of d­ epolarization
(Tu and Dickinson, 1994).
2.7 Muscle fiber types
Both vertebrate and invertebrate skeletal muscles
commonly have twitch fiber populations that pos-
sess differing contractile and metabolic characteris-
tics. Distinguishing among these features has led to
a series of descriptive classifications of muscle fiber
types. Although these classification schemes sug-
gest discrete types of muscle fibers, in fact variation
can exist within a population of fibers of a given
type. Consequently, differences between fiber types
are often qualitative, yielding more of a continuum
of properties across the spectrum of muscle fiber
types. Nevertheless, differences in motor recruit-
ment and function can be usefully ascribed to dif-
ferences in fiber type within and between muscles
within a species and can often have profound physio­
Table 2.1 Twitch (phasic) skeletal muscle fiber types (based largely on mammalian patterns).
Property/feature Slow-oxidative (SO)
Alternative slow twitch
classifications type I
Myosin isoform slow cross-bridge cycling
SR Ca ATPase
2+
slow SR Ca uptake
2+
Contraction speed slow
Krebs cycle enzymes high
# mitochondria and capillaries high
Contraction endurance high
logical and ecological significance when comparing
multiple species. The characteristics and properties
of twitch muscle fiber types have been most thor-
oughly studied in mammals; the classification
scheme used here is largely based on these studies.
Although this classification reflects the bias of
twitch mammalian fiber types, it provides a concep-
tual scheme that can be usefully extended to the
broader diversity of skeletal muscle fibers found in
other animal groups. Characteristics of non-twitch
invertebrate muscle fibers will be discussed in Chapter
8, when we consider the neural control of motor
function.
Three main types of twitch muscle fibers are gen-
erally recognized within mammals, birds and rep-
tiles: slow-oxidative (SO), fast-oxidative-glycolytic
(FOG) and fast-glycolytic (FG). Table 2.1 lists sev-
eral key contractile, metabolic and cytological fea-
tures of these three types of fibers. Myosin isoforms
are determined by protein immunohistochemistry.
Qualitative descriptions of contractile and meta-
bolic properties determine whether fibers are classi-
fied as SO (also termed type I fibers), FOG (also
referred to as IIa and IIx) and FG fibers (also termed
type IIb). Myosin with a fast ATPase rate (i.e. fast
cross-bridge cycling rate) is characteristic of fibers
that contract rapidly. More oxidative fibers have
slower myosin ATPase rates, which means that they
develop force and shorten more slowly. A slower
rate of shortening is also associated with their reli-
ance on aerobic synthesis of ATP via mitochondrial
oxidative phosphorylation. Hence, slow-oxidative
Fast-oxidative- Fast-glycolytic
glycolytic (FOG) (FG)
fast-twitch red fast-twitch white
type IIa type IIb
rapid cross-bridge cycling rapid cross-bridge cycling
2+
fast SR Ca uptake fast SR Ca2+ uptake
fast fast
intermediate low
intermediate low
intermediate low

fibers show a high quantity of oxidative enzymes,
such as succinate dehydrogenase or citrate syn-
thase. In contrast, fast-glycolytic fibers store large
amounts of glycogen and have a high quantity of
glycolytic enzymes, such as glycerol diphosphatase,
enabling them to generate ATP rapidly via anaerobic
metabolism. FG fibers fatigue quickly (due to meta-
bolic acidosis), whereas SO fibers can contract for
long periods without becoming fatigued. As their
name suggests, fast-oxidative-glycolytic (FOG) ­fibers
possess intermediate properties.
Associated with their metabolic reliance on
­aerobic ATP synthesis, SO fibers are also more richly
supplied with capillaries and myoglobin (reflecting
a high capacity for vascular supply of O2), and con-
tain many more mitochondria than FG fibers. FG
fibers, on the other hand, have a more extensive,
well-developed sarcoplasmic reticulum, associated
with the need for rapid Ca2+ activation and uptake
for fast contraction speed. Recruitment among fiber
populations with these differing metabolic and con-
tractile properties allows animals to use particular
sets of muscles or muscle fibers for particular tasks.
Rapid burst activity, as during escape or prey cap-
ture, is best powered by FG fibers, whereas slower
movements and control of posture favors recruit-
ment of SO fibers. Finally, it is worth emphasizing
again that slow twitch-oxidative fibers are distinct
from and not to be confused with the slow-tonic
­fibers found in certain muscles of invertebrates and
vertebrates.
Fiber type features vary within and across clades.
As ectotherms, most reptilian species rely on burst
activity rather than sustained locomotion in order
to obtain food and avoid predation. The leg muscles
of lizards, not surprisingly, have a predominance of
FG fibers that are well suited to burst anaerobic
activity. On the other hand, mammals and birds are
able to sustain locomotor activity that is fueled
by aerobic metabolism for much longer periods.
Consequently, their muscles have much higher pro-
portions of oxidative (SO and FOG) fibers. Most
spectacularly, the high wing beat frequency of hum-
mingbirds (45–60 Hz) requires that nearly 50 p ­ ercent
of flight muscle volume is occupied by mitochon-
dria (the other half consists of myofilaments and
sarcoplasmic reticulum). Nearly all their flight ­muscle
is comprised of FOG fibers. This is also true of many
M U S C L E S A N D S K E L E TO N S 23
small- to moderate-sized birds. For example, up to
85 percent of a pigeon’s primary flight muscle con-
sists of FOG fibers. Clear differences exist among
mammals as well. Whereas canids (dogs, coyotes,
wolves) have high proportions of oxidative fibers
allowing them to hunt and forage actively for long
periods, felids (cats, lions) have relatively few oxi-
dative fibers, relying on stealth and burst pursuit to
catch their prey. Such differences clearly distinguish
the temperaments and personalities of our most
popular pets!
In most fish, two distinct populations of fibers
occur within the axial musculature: the red fibers
are slow-oxidative, whereas the white fibers are
fast-glycolytic (Fig. 2.7). Typically, the red fibers
constitute a relatively small portion of the myotome
and are found in a longitudinal band either near the
body surface (most fish) or closer to the backbone,
within the larger white component, in certain spe-
cialized “regionally endothermic” fish (tunas, bill
fish, mackerel and lamnid sharks). These fish are
capable of maintaining their deeper red muscle at a
warmer temperature than the surrounding water. At
slow swimming speeds, only the red slow-oxidative
fibers are activated to produce a slow traveling
wave of propulsion. As swimming speed increases,
white muscle fibers are also recruited to power
swimming, providing faster and stronger waves of
propulsion. Because the white (FG) fibers are less
oxidative than the red (SO) fibers, however, endur-
ance is progressively reduced at faster swimming
speeds. The locomotor performance of most fish
(which are ectotherms) is strongly affected by water
temperature. Interestingly, at low temperatures,
several fish begin to recruit faster contracting white
fibers at slower swimming speeds in order to com-
pensate for reduced muscle power output at these
low temperatures (see Fig. 8.10, Rome et al., 1984).
In regionally endothermic fish, such as tunas and
bill fish, countercurrent heat exchangers maintain
internal red muscle temperatures as much as 10°C
greater than the surrounding water. By keeping
their red musculature warm, the fish are able to
achieve greater endurance and faster swimming
speeds in colder waters.
By alternately shortening and lengthening to bend
the fish’s body and tail back and forth, the axial
­musculature of swimming fish does mechanical work
24 A N I M A L L O C O M OT I O N

5 cm

Red
muscle

(a) (b)

Figure 2.7 Red and white axial muscle organization is evident in cross-sections of (a) mackerel and (b) tuna (two scombrid fish). In most fish,
such as the mackerel, the red muscle represents a limited portion of the myotomal muscle and is located just beneath the skin lateral to the white
muscle. In tuna and other fish which warm their red muscle, the red muscle is more extensive and lies medially to much of the white muscle.
Counter-current heat exchange keeps the red muscle warmer than the water and the rest of the fish (some fish also maintain elevated brain and
eye temperatures). Reproduced from Westneat and Wainwright (2001) with permission from Elsevier.

during the shortening phase of its length cycle as it
contracts to develop force. Studies of the neural acti-
vation of muscle segments at different sites along the
length of swimming fish show that the muscles are
typically activated just as they finish being pas-
sively lengthened, so that they develop force while
shortening (Fig. 2.5). This allows the muscles at
any one location on the animal’s body to do work
( force × shortening distance ) . This work is transmit-
ted posteriorly along the animal’s body, to its tail, and
used to produce the hydrodynamic thrust necessary
to propel the animal forward. Studies of both the

slow-oxidative red and fast-glycolytic white muscle
fibers from fish indicate that they shorten at a vel­
ocity that is close to their optimum (0.3 to 0.4 v / vmax ;
Fig. 2.4) for doing work efficiently and generating
power (work/time). Hence, fish typically cruise at a
steady uniform speed using their red muscle to maxi-
mize their swimming efficiency and reduce their
cost of movement. When they accelerate or swim
quickly, they use their white muscle to maximize
power output for escaping predation or to catch prey.
2.8 Fiber architecture and its effects on
muscle volume and energy use
In addition to a muscle’s intrinsic force-length and
force-velocity properties and its fiber type character-
istics, the arrangement and orientation of a m­ uscle’s
fibers (fiber architecture) also affect its contractile
function. Muscles are traditionally divided into two
fundamental classes based on their architecture:
Parallel Unipinnate Bipinnate
Ft
α
If
Fm
α brate and vertebrate animals (although, certain
(Aponeurosis)
(External tendon)
Ft = Fm cosα
Figure 2.8 In contrast to parallel-fibered muscle, the fibers of
pinnate muscles exert force at an angle to the muscle and tendon
long-axis. The effective force is a product of the cosine of the muscle
fibers’ pinnation angle (α). Ft, tendon force; Fm, muscle fiber force; lF,
muscle fiber length. However, because the number of fibers and their
cross-sectional area (for a given muscle volume) is much greater,
pinnate muscles commonly generate much larger forces compared
with parallel-fibered muscles.
M U S C L E S A N D S K E L E TO N S 25
parallel-fibered and pinnate-fibered ­muscles (Fig.
2.8). Parallel-fibered muscles have fi ­ bers that run
end-to-end within the muscle in a direction parallel
to the muscle’s axis of force transmission. Typically,
parallel-fibered muscles have relatively long fibers
and attach directly to the skeleton with little or no
external tendon. In contrast, pinnate-fibered mus-
cles are built with shorter fibers attached at an angle
to the muscle’s principal axis of force transmission.
Pinnate muscles often attach via an external tendon
to the animal’s skeleton.
Pinnate muscles can be architecturally quite com-
plex. Uni-pinnate muscles have fibers that are all
oriented at similar angles in a single plane and
attach to the distal tendon. Bi-pinnate muscles have
two sets of fibers at roughly mirror-image angles,
which attach to a central distal tendon. Multi-pinnate
muscles have more complex fiber architectures with
varying planes of angled fibers. In general, muscles
that are more pinnate also have shorter fibers.
Due to differences in fiber length, parallel-fibered
muscles of equal mass (and volume) have a smaller
fiber cross-sectional area compared with pinnate
muscles (Figs 2.8 and 2.9). As previously noted,
because all striated muscles depend on the same
myofilament interaction for force generation, the
force developed by a muscle generally varies in
direct proportion to its fiber cross-sectional area. In
other words, the maximum isometric stress (force/
fiber area) that striated muscles can develop is
largely constant across a broad diversity of inverte-
invertebrate muscles with long sarcomeres, such as
crab pincers, are able to generate unusually high
stresses). Consequently, because of their shorter
fibered architecture, pinnate muscles of equal mass
are capable of generating greater forces than paral-
lel-fibered muscles. Although pinnate muscles suf-
fer some loss of force transmission due to the angle
of their fibers, this is more than offset by their
greater fiber area.
The cross-sectional area of a parallel-fibered
muscle (Am) can be determined from its mass and
mean fiber length (lf), given a known density (1060
kg m–3 is a typical value for striated muscles), as
follows:
Am = m / ρ m lf (2.1)
26 A N I M A L L O C O M OT I O N

The effective “physiological” cross-sectional area of
a pinnate muscle (*Am, also referred to as PCSA) can
be calculated by accounting for the muscle fibers’
pinnation angle (α, Fig. 2.8) as,
*Am = Am cos α
These equations enable the following simple
comparison between a parallel-fibered and pinnate
muscle. If we assume the two muscles have equal
mass, set the parallel fibers equal to ten times the
length of the pinnate fibers, and set the pinnation
angle to 20° in the pinnate muscle, the parallel-
fibered muscle will have a fiber area that is only
1 / 9.4 [= (1 / 10 × cos (20°)] or 0.106 times that of the
pinnate muscle. Correspondingly, the effective
force that the pinnate muscle transmits to its tendon
(Ft) equals the force developed by the muscle’s
­fibers ( Fm ) × cos α , which in this case is 9.4 times
greater than the parallel fibered muscle. An important
advantage of a parallel fiber architecture is that it
provides a greater range of shortening (in the previ-
ous example, the parallel-fibered muscle would
contract ~ tenfold greater distance than the pinnate
muscle). In terms of muscle work, the increase in
force achieved by a pinnate architecture is coun-
tered by the decreased shortening capacity of its
­fibers. Consequently, all muscles have generally the
same capacity for doing work on a per unit mass
(2.2)
basis, irrespective of their fiber architecture.
A muscle’s fiber architecture also affects its rate
of energy use based on the volume of muscle that
must be activated to generate a given force. Longer
parallel-fibered muscles require more energy to
generate a given force than short, pinnate-fibered
muscles, because longer fibers require the forma-
tion of more cross-bridges to transmit force along
their length than short fibers (Biewener and Roberts,
2000; Roberts et al., 1997). Consequently, the ATP
cost per force generated, a measure of a muscle’s
force economy, increases with muscle fiber length.
For example, two muscles of equal volume, but
with fiber lengths that differ by threefold will also
differ in their fiber cross-sectional areas (Af) by
threefold (Fig. 2.9). To generate a given force, both
muscles must recruit the same Af; however, the
longer fibered muscle has three times the volume

Vactive Af
Muscle A
Muscle A
parallel-fibered

lf = 3
Muscle B

lf = 1
Af
Muscle B
pinnate-fibered

Vactive

Figure 2.9 Muscle pinnation, fiber length and recruitment of fibers influence force generation and energetic costs. In this drawing of a wallaby
leg, the hamstrings are parallel-fibered with long fiber lengths (lf) and the gastrocnemius and plantaris (calf muscles) are pinnate with short fiber
lengths. Long-fibered muscles (Muscle A; from a parallel-fibered muscle) require a greater activated volume (Vactive) than short-fibered muscles
(Muscle B; from a pinnate muscle), given the same cross-sectional area of recruited fibers (Af). In the example shown, because Muscle A has fiber
lengths (lf) that are three times longer than Muscle B, Muscle A requires a three-fold greater active volume and cost for the same cross-sectional
area of fiber activation as in Muscle B. Thus, muscles with shorter fibers can achieve greater force economy.

and three times the number of cross-bridges. Con­
sequently, given that both muscles contract under
similar conditions, the cost to generate a given force
will be three times as great in the longer fibered
muscle. As we’ll see, this simple effect of muscle
geometry on ATP utilization can have profound
effects on the energy use of a muscle and its role in
locomotor function.
Pinnate fiber architecture offers an additional
level of control because pinnation angles may change
during a contraction affecting the force and short-
ening velocity of the muscle as a whole (Azizi
et al., 2008). For example, in turkey gastrocnemius
muscles that are activated to achieve high velocity
muscle contractions at the fiber level, the muscle
changes shape to increase overall muscle velocity
rather than muscle force. Specifically, as the muscle
contracts, its pinnation angle increases which simul-
taneously reduces force transmission, but enhances
the overall velocity output of the muscle. By con-
trast, at high forces, the pinnation angle decreases
such that the fiber’s force vector is directed more in
line with the muscle’s action, increasing overall
muscle force output, but at the expense of overall
muscle velocity. This phenomenon is referred to as
“variable gearing,” and demonstrates that muscles
can enhance or offset the underlying force-velocity
tradeoffs of their fibers at the myofibril level by
shifting the force vectors arising from the dynamic-
ally changing pinnate muscle fiber angles.
2.9 Skeletons
Locomotion requires effective transmission of
­internal muscle forces to the external environment.
In unicellular and multicellular animals, this is
accomplished by having a combination of rigid
compression-resistant and flexible tension-resistant
elements. Multicellular animals possess three types
of skeletons: endoskeletons, exoskeletons and hydro-
static skeletons. Endoskeletons and e­ xoskeletons
transmit force using rigid materials that deform
minimally. Hydrostatic skeletons use liquid as an
incompressible skeletal component and, less-com-
monly, pneumo-hydrostatic skeletons use a com-
bination of liquid and gas (found in terrestrial
crabs) (Taylor and Kier, 2006). Tensile ­elements,
M U S C L E S A N D S K E L E TO N S 27
such as tendons, apodemes and ligaments, help to
stabilize the joints and link muscles to the skeleton.
In this section, we consider the three major c­ ategories
of skeletons and the role of muscle attachment for
varying locomotor output.
2.10 The connection between muscle
and skeleton
To transmit forces, muscles must connect to the
skeleton. Vertebrates and arthropods use tendons
and apodemes, respectively, to transmit muscle forces
to the skeleton. Tendons not only attach m ­ uscle and
skeletons, they also serve as an ­important part of
energy storage and release. Tendons and apodemes
can function as highly ­resilient springs (Fig. 2.10),
returning up to 93 percent of the energy that is stored
when stretched. The slight loss of energy (7 percent),
reflected by the “hysteresis” in the loading versus
unloading behavior of tendon is not uncommon for
many tissues and reflects the fact that tendons dis-
play both viscous (energy lost) and elastic (energy
recovered) properties.
In addition to losing some energy when unloaded,
tendon also exhibits “non-linear” stress-strain behav-
ior, having a characteristic “J”-shaped curve. At
low stresses, the “toe” region of the curve has a
low slope. As stress increases, the slope increases
until it becomes relatively constant at moderate to
higher stresses (and strains). The change from low
to higher stiffness (or modulus) results from the
sliding and re-alignment of collagen fibrils within
the tendon at low stresses, which are then pulled on
directly when the tendon’s stiffness increases. The
toe region is fairly small; above a strain of about
two to three percent, the slope of the tendon’s
stress–strain curve can be considered nearly con-
stant. Over this linear range of behavior, tendon has
an elastic modulus of about 1.2 GPa. Tendon rup-
tures at stresses in the range of 100–120 MPa, indi-
cating a failure strain of about 10 percent. Based on
measurements of tendon stresses in running verte-
brates, maximal tendon strain ranges from ~5 to 6
percent.
The non-linear and slightly viscoelastic behavior
of the tendon contrasts with the linearly elastic
behavior that was used to provide a simple overview
28 A N I M A L L O C O M OT I O N

100

Tendon

Stress (MPa) 50 Loading

Energy lost
(∼7%)
Unloading

4 8
Strain (%)

Figure 2.10 The stress-strain curve of vertebrate tendon illustrates the hysteresis that occurs between loading and unloading. The area within
the hysteresis loop (white) reflects the energy that is lost as heat due to the viscous properties of the tendon. For vertebrate tendons, hysteresis is
as low as 7%. The remaining area (shaded) represents the energy that is recovered elastically (93% of energy used to stretch the tendon) and that
can be used to offset muscle work. Although tendon is less stiff at lower stresses, its overall properties are well-suited to function as an effective
spring for energy recovery. Most tendons operate at strains up to about 5–6%.

and comparison of the properties of various bio-
logical materials introduced in Chapter 1. Never­
theless, the tendon is stiff (1.2 GPa) and highly
resilient (93 percent) over much of its functional
range, making it an excellent material for storing
and recovering elastic strain energy. This cycling of
elastic strain energy reduces the mechanical work
and the metabolic cost of locomotion. A reasonable
estimate for the strain energy recovery of vertebrate
tendons is: 0.5 F∆L × 0.93 , or 0.465 F ΔL (where F is
the maximum force transmitted by the tendon and
ΔL is its total change in length). Variation in tendon
and apodeme stiffness allows tuning to the dur-
ation of muscle force development during elastic
energy storage, as has been demonstrated in grass-
hoppers and bullfrogs that store elastic energy in
their springs over short and long durations, respect­
ively (Rosario et al., 2016).
The consequences of muscle-skeleton connections
have also been intensively studied in fish. Forces
developed by the axial muscles (myomeres) of fish
are anchored by or transmitted to the vertebral col-
umn and to the tail. In sharks, a cross-fibered array
of collagen fibers beneath the skin is also used as an
“external body tendon” to which the muscles attach,
allowing the shark to transmit force p ­ osteriorly
with a large mechanical advantage to bend its body
and ultimately its tail (Wainwright et al., 1978). In
tunas, well-developed lateral tendons emanate from
the axial muscles to attach to the tail. The presence of
these large tendons is strong evidence that they
transmit significant forces and ­corresponds with the
dominant use of caudal fin propulsion. Recordings
of forces from these tendons confirm their role in
powering oscillation of the tail (Knower et al., 1999).
The complex arrangement of fish axial muscles and
the many connective tissue and skeletal components
to which they attach makes their study a fascinating
and ongoing challenge.
2.11 Vertebrate endoskeletons
Internal bony elements comprise the skeletons of
vertebrates. Except for certain elements of the skull,
the skeleton first develops and grows as cartilaginous
elements that later ossify by means of calcification
of the cartilage and subsequent mineralization of
collagen (a process known as “endochondral ossifi-
cation”). The bones of mature animals are compos-
ites—consisting of two or more materials—generally

(a)
Bone mechanical properties
Wf
62 67
Percentage mineralization
Figure 2.11 Mineralization and stress-strain curves vary across skeletal materials. (a) Bone properties (S, strength, or maximum stress; E, elastic
modulus, or stiffness; and W f , work of fracture) vary as a function of bone mineralization (modified from Currey, 1984). (b) The stress-strain
behavior of various skeletal tissues varies dramatically and matches the mechanical function of the skeletal tissue in support and energy flow.
two-thirds mineral (hydroxyapatite) and one-third
type I collagen. The mineral phase of bone is a
hydrated calcium phosphate salt secreted by bone
cells, which crystallizes and grows on the type I col-
lagen fibers that these cells also deposit into the
extracellular matrix. As the collagen becomes min-
eralized, the bone’s stiffness (ratio of load versus
deformation, see Chapter 1) increases.
Increased mineralization of a bone increases its
stiffness and makes it stronger, but this diminishes
its ability to absorb the energy of impact loads
(making it more brittle). Mineralization levels for
a diversity of limb bones occupy a fairly narrow
range (63–70 percent), suggesting that this tradeoff
between stiffness, strength and energy absorption is
important (Currey, 1984; Fig. 2.11a). Consequently,
bone is a rigid supportive material providing stiff-
ness to transmit forces effectively, yet is capable of
deforming sufficiently (<1 percent) so that it can
absorb a substantial amount of energy before failing
(Fig. 2.11b). Interestingly, distal wing bones of bats
have mineralization as low as 60 percent, suggest-
ing a potential role of wing flexibility in flight
(Papadimitriou et al., 1996; Swartz and Konow,
2015). In contrast, highly brittle materials like glass
are often strong, but easily break: they have a high
failure stress, but absorb little energy due to their
extremely high modulus. More compliant mater-
M U S C L E S A N D S K E L E TO N S 29
(b)
E
Bone
S
Shell Cuticle
Stress
Cartilage
72 Strain
ials, such as cartilage, absorb energy by undergoing
considerable deformation (Fig. 2.11b). However, as
a consequence, they are not rigid enough to func-
tion effectively for force transmission as a lever or
over long distances. Consequently, bone appears
to have evolved a level of mineralization that
­enables it to meet these competing requirements.
One interesting exception is the calcified cartilage
that secondarily evolved within elasmobranchs
(sharks and rays), and provides an alternative solu-
tion for a rigid vertebrate endoskeleton. As a rela-
tively thin tissue layer at the articular end of a bone,
cartilage functions well to absorb energy and distrib-
ute loads transmitted across a joint. The c­ artilage
found in synovial joints (which represent most of
the mobile joints of the vertebrate body) also pro-
vides excellent lubrication through the synovial
fluid that is secreted into the joint cavity, taken up
by the cartilage, and squeezed into a low-friction film
between the load-bearing surfaces of the articular
ends of the bones.
While bone fracture and tendon rupture do occur,
they are relatively rare events. Failure of important
skeletal elements likely poses a significant biological
cost to an animal’s fitness. This cost is successfully
avoided by the evolution of material and structural
properties that are sufficient for a skeleton to bear the
loads normally applied during an animal’s lifetime.
30 A N I M A L L O C O M OT I O N
As a result, skeletons operate with safety margins—
strengths that exceed their maximum likely loads
by as much as three to fivefold, or even greater. In
addition to the large size range of growth that they
allow, a distinct advantage of bony endoskeletons is
their ability to be repaired, so that fracture need not
incur a permanent and likely fatal cost (Currey,
1984).
2.12 Invertebrate exoskeletons
The invertebrate exoskeleton necessitates internal
attachment of muscles and apodemes. By contain-
ing the soft tissues inside, exoskeletons have the
advantage of providing good protection and, in the
case of terrestrial animals, resistance to desiccation.
On the other hand, exoskeletons severely limit the
animal’s growth and are susceptible to damage
on their exterior surface. Wounded arthropods can
perform minimal repairs to the exoskeleton; major
fractures necessitate molting (shedding) of the old
exoskeleton and growth of new exoskeleton. To per-
mit growth, arthropod exoskeletons must be shed
at regular intervals. The calcium carbonate shells of
bivalve molluscs and brachiopods grow by accre-
tion at the border of the shell. Growth in size of
­molluscan soft parts is facilitated by shells with
geometries (cone, hemi-ellipsoid) that allow an
increase in size while maintaining a similar shape
(isometry).
The cuticle of arthropod exoskeletons, like bone,
is also a composite material. Most arthropod exo-
skeletons contain approximately 15–20 percent stiff
polysaccharide chitin fibers (similar in structure
to cellulose) embedded in a protein matrix. Within
crustaceans, additional stiffness is achieved by the
incorporation of calcium carbonate. The cuticle of
most exoskeletons, however, is stiffened mainly
by “tanning” (sclerotization), a process in which
the cuticle matrix proteins become cross-linked by
­quinones and dehydrated to provide stiff reinforce­
ment of the chitin fibers. The chitin fibers are bonded
to each other in cross-ply layers, much like ply-
wood. In apodemes, the chitin fibers lie parallel to
each other similar to the organization of collagen
fibers in vertebrate tendons. Tanned cuticle has
approximately half the stiffness and strength of
bone, but, as a result, absorbs more energy before
failing (Fig. 2.11b). Joints within the exoskeleton are
achieved by hinged articulations between adjacent
rigid cuticle elements with flexible (untanned) c­ uticle
lying over the joint to allow movement.
The calcium carbonate shells of bivalve mollusks,
due to their absence of a significant organic compo-
nent, are extremely stiff and fairly brittle (Fig. 2.11b).
The extremely hard skeletal surface conferred by
calcium carbonate enhances the resistance to damage
by boring organisms common in aquatic environ-
ments. However, mollusks still must resist impact
and crushing loads from predators and intense
wave-action in intertidal habitats. When the shells
are used for locomotion, as in scallops, the shells
articulate by a simple hinge joint at their base allow-
ing them to be clapped together to expel water out
of the animal’s mantle cavity (see Chapter 5).
2.13 Hydrostatic skeletons
Hydrostatic skeletons are the most widely distrib-
uted types of skeleton in the animal kingdom (espe-
cially prevalent in cnidarians, worms, spiders and
mollusks) and form important components within
the endo- and exoskeletons of other animals as well.
For example, hydrostatic compressive support is
im­portant to single-celled organisms, against which
arrays of actin filaments and microtubules can act to
transmit tensile forces. In vertebrates, the articular
discs present between the vertebrae represent hydro-
static components that are effective in resisting com-
pressive loads transmitted between the vertebrae.
Most commonly, a hydrostatic skeleton is formed
by a pressurized fluid-filled body cavity that is
surrounded by a tension-resisting, fiber-reinforced
skin, or wall. In the case of vertebrate articular discs,
the annulus of the disc has collagen fibers arranged
in layers that resist the gel-like nucleus pulposus
contained inside. The hydrostatic ­skeletons of cnidar-
ians, worms and other animals that must rely on
their skeleton for movement as well as support. The
walls of these hydrostatic skeletons are typically made
of fiber-reinforced layers and two sets of antagonis-
tic muscles (e.g. circular and longitudinal).
Because liquid is incompressible, hydrostatic
skeletons transmit the forces developed by the ani-
mal’s muscles to enable changes of body shape and
 M U S C L E S A N D S K E L E TO N S 31

(a) (b) (c)

Knee extensor
agonists

Knee flexor
antagonist

Ankle extensor
agonists F
F r = G R = T’
Ankle flexor
antagonist ds ds = r dθ
r
G r
Ankle joint R R
dθ
dL

(d) (e) (f)

ds ds
r/ G/ r/ R r
2 R 2 2
dθ dθ
dL /
2
dL

Figure 2.12 Muscle attachment location influences skeletal output. (a) Organization of muscle agonists and muscle antagonists within a
vertebrate limb. (b) Schematic diagram showing the torque (T ´, or moment) balance of an extensor muscle force (F ) relative to the ground reaction
force (G) at the ankle joint, which depends on the mechanical advantage, or moment arms (r and R), of each force vector. This torque balance
ignores torques due to segment inertia and weight, which are quite small in relation to the torque produced by the ground reaction force (G)
during limb support. (c) The mechanical advantage, or “in-lever”, of a muscle affects joint motion and limb displacement (dL). Angular motion (dθ)
of a distal segment (in this case, the foot) depends on muscle shortening (ds) in relation to its moment arm (r). (d) The torque that a muscle (ankle
extensor) can produce is reduced in half when its moment arm is reduced by 50% (i.e., the muscle acts closer to the joint). (e) However, by acting
more closely to the joint, or with a shorter “in-lever” (moment arm = r/2), shortening of the muscle (ds) produces twice the range of motion (and a
twofold increase in joint velocity). (f) With a shorter “out-lever” (defined as the length of the distal segment, or foot, in this case), the range of
motion is reduced for a given joint angle displacement compared with (c) above. These differences in muscle mechanical advantage reflect a
fundamental tradeoff between force (or torque) and velocity of movement, as well as the range of motion that a muscle can produce. This affects
locomotor performance and how muscles are arranged with respect to the skeletons of animals.

locomotor movement. Consequently, animals that
have hydrostatic skeletons do not depend on the
rigid mechanics of force transmission that are char-
acterized by animals with endo- and exoskeletons.
In most instances, locomotion is slow and non-­
dramatic. However, spiders use a hydraulic system
to rapidly move their legs. Similarly, high ­performance
jetting locomotion has evolved within certain ceph-
alopod molluscs (squid) that use hydrostatic pres-
sure developed within their mantle cavity to move
at high speeds (see Chapter 5).
2.14 Skeletons as jointed lever systems
In animals with rigid skeletons, muscles produce
movement and transmit force by developing tor-
ques (or moments) at specific joints. Because mus-
cles can only generate tensile (pulling) forces,
reciprocal movements of appendages (e.g. flexion
and extension of a joint) require the action of oppos-
ing, or antagonistic sets of muscles (Fig. 2.12a). As
already noted, this is also true for animals with
hydrostatic skeletons. In some animals, a single
muscle may power locomotion, but the muscle is
32 A N I M A L L O C O M OT I O N
always associated with a passive elastic element (in
the case of scallops, an abductin pad) that acts as the
muscle’s antagonist by storing elastic strain energy
when the muscle contracts and restoring this energy
when the muscle relaxes to produce the reciprocal
motion of the skeleton.
The joint torque (T´, or moment) developed by a
muscle (Fig. 2.12b) depends on its force (F) and its
mechanical advantage, or moment arm (r):
T ′ = Fr (2.3)
Correspondingly, muscle shortening (ds) can be
related to joint displacement (Fig. 2.12d) by the fol-
lowing relationship:
ds = r dθ (2.4)
or,
ds / dt = r dθ / dt (2.5)
for velocity, where dθ is the change in joint angle
measured in radians (1 radian = 180 / π ) . Equations
2.4 and 2.5 are approximations, but they hold well
for small angles (<0.5 rad). Attachment further
from the joint’s center of rotation increases a mus-
cle’s mechanical advantage, but increases the dis-
tance that a muscle must shorten to produce a given
angular displacement of the joint. Consequently, the
torque that a muscle can develop varies inversely with
the range of joint motion that it can produce.
The mechanical advantage of the limb shown in
Figure 2.12b is twice that of the limb in Figure 2.12c,
allowing it to develop twice the force against the
ground (G) for a given extensor muscle force. However,
the angular excursion of the foot is 50 percent less
(Fig. 2.12d versus 2.12e). The length of the s­keletal
segment to which a muscle or its tendon attaches also
affects its relative mechanical and displacement
advantage for generating force and movement at the
end of the segment. The longer the distal skeletal seg-
ment (Fig. 2.12d versus 2.12f), the greater the range of
movement achieved for a given angular displace-
ment of the joint or range of muscle shortening. Thus,
as will become evident in subsequent chapters, the
mechanical organization of muscles in relation to an
animal’s skeleton greatly influences how animals
adjust to the effects of size, their locomotor kine-
matics, and their ability to accelerate and maneuver.
While these geometric force-displacement rela-
tionships offer an excellent starting point for
­interpreting musculoskeletal dynamics, these rela-
tionships can shift dramatically when the loading
regime changes either in terms of muscle dynamics
or environmental forces acting back onto the skeleton.
When realistic environmental loads are imposed on
these systems, the force-displacement relationships
are less clear-cut. For example, in a spring-loaded
locust jump, when spring-mass dynamics are
included, the leg velocity is actually independent of
the system’s mechanical advantage. Similarly, in the
rapidly rotating mantis shrimp’s appendage with
mechanical advantage geared for speed, the drag
forces impose such a large cost that the long out-
lever actually reduces the output velocity (McHenry
et al., 2012).
The fiber architecture of muscles is often related
to their mechanical advantage and organization
within a limb. Muscles that attach further from a
joint’s rotational axis typically have longer fibers.
This enables them to maintain a fractional shorten-
ing range similar to that of muscles with shorter
­fibers that act closer to the joint. This is advanta-
geous due to the force-length property of striated
muscle fibers (Fig. 2.3). An animal can achieve
­muscle gearing, much like the transmission of an
automobile, through muscle action at different loca-
tions relative to a joint. A close attachment to the
joint provides a high gear for fast, but less forceful
movements (Fig. 2.12d and e). Action further away
from the joint offers a low gear for slower, more
forceful movement (Fig. 2.12b and c). Muscles that
act in concert to produce a similar joint movement
are termed “agonists” or “synergists” and are opposed
by an antagonist muscle or muscle group.
The range of motion at a joint is largely dictated
by the shape of the joint. Many exoskeletal and
some endoskeletal joints are hinged, single degree
of freedom joints, which means that rotation can
occur only about a single axis (these joints have two
sets of muscle antagonists: flexors and extensors).
However, there is a considerable diversity of joints
beyond this most simple arrangement. Exoskeletal
and vertebrate endoskeletal joints range from hinged,
single degree of freedom joints to ball-and-socket
joints in which rotation can occur about three inde-
pendent axes. With a greater range of motion, the
Another random document with
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his power, 266;
his theory of internal politics, 272;
contradictions in his character, 277;
his hopefulness, 307 et seq.;
as a man of science, 310;
his dislike for New Englanders, 310 et seq.;
his letter to Paine, 316;
attacked by Callender, 322;
sensitiveness of, 324;
his relations with Callender, 325 et seq.;
sends Lear to St. Domingo, 389;
ignorant of Bonaparte’s schemes, 403 et seq.;
his eyes opened, 409;
his letter to Dupont de Nemours, 410;
writes to Livingston defining his position with respect to
France and Spain, 424;
his annual message, 1802, 427;
ignores the war party, 428;
replies to their demand for papers touching the right of deposit
at New Orleans, 430;
quiets the West, 432;
attempts the purchase of New Orleans, 432 et seq.;
his language to Thornton, 436;
prefers Natchez to New Orleans as a seat of trade, 443;
his apparent inconsistency, 443 et seq.;
the essence of his statesmanship, 445;
proposes alliance with England, ii. 1, 78;
instructs Pinckney to offer a consideration to Spain for New
Orleans and Florida, 22;
writes a defence of his use of patronage for the Boston
“Chronicle,” 82;
his amendment to the Constitution regarding Louisiana, 83;
his letter to Breckenridge on the subject, 84;
to Paine, 86;
draws up a new amendment, 86;
his reply to W. C. Nicholas, 89;
his message, Oct. 7, 1803, 92;
his bill for the administration of Louisiana, 119;
his view of the Louisian treaty and legislation, 130;
requests Congress to enlarge the Mediterranean force, 140;
interview with Burr, 175;
declines to appoint Burr to an executive office, 176;
his knowledge of Federalist schemes, 192;
his confidence in his popularity, 202;
receives the electoral votes of Massachusetts and New
Hampshire, 204;
his message, November, 1804, 206;
his disappointment at the acquittal of Justice Chase, 243;
his authority in foreign affairs, 245;
desires to obtain West Florida, 245;
explains to Senator Breckenridge his course toward Spain,
248;
his plan to obtain West Florida, 249;
instructs Monroe with regard to the Spanish claims, 250;
the harvest season of his life, 252;
sends troops to Natchez, 254;
makes no demand for West Florida when Louisiana is
delivered, 256;
declares Mobile within the United States, 263;
entertains Yrujo at Monticello, 266;
his conviction of the power of American commercial interests,
330;
anxious for friendship with England, 342;
his intimacy with Thornton, 347;
his opinion of Bonaparte, 347, 353, 381;
decides to maintain the neutral rights of the United States
more strictly, 356;
his social habits, 363;
establishes a new social code, 365;
receives Merry, 366;
invites him to dinner with Pichon, 369;
sends list of impressments to the Senate, 384;
improves his style of dress, 405;
his enemies, 409.
Judiciary Act, the, i. 274 et seq.;
repeal of, moved, 278 et seq., 284 et seq.;
repealed, 298.
Judiciary system, the, Jefferson’s recommendations concerning,
i. 255.

Kentucky in 1800, i. 2, 43;

Resolutions of 1798, 140 et seq., 205.
Key, Philip Barton, ii. 228.
King, Rufus, American minister in London, i. 109;
sends the treaty of the retrocession of Louisiana to Jefferson,
409; ii. 23, 178 et seq.;
obtains from Pitt a definition of neutral importation, 328, 340;
his negotiations with the British government, 345, 347;
returns with favorable conventions, 358;
opinion of F. J. Jackson and Anthony Merry, 361;
leaves England, 410.

Langdon, John, i. 220.

Latrobe, Benjamin H., report on steam-engines, i. 68, 70, 112;
letter of, to Volney, 130.
Laussat, prefect in Louisiana, ii. 5;
arrives at New Orleans, 10, 13;
defines the boundaries of the Louisiana purchase, 255;
declares the Rio Bravo the western limit of Louisiana, 298.
Lea, Thomas, i. 257.
Lear, Tobias, consul to St. Domingo, i. 389;
quits St. Domingo, 407;
negotiates a treaty with the Pacha of Tripoli, ii. 434.
Leclerc, General, in command of the expedition against
Louverture, i. 378;
seizes Toussaint Louverture, 396;
insults American shipmasters, 407;
reports French losses, 414;
blamed by Napoleon, 416;
his death, 418; ii. 13.
Lee, Charles, ii. 228.
Leib, Michael, member of Congress from Pennsylvania, i. 298;
ii. 123, 194, 196 et seq.
Lewis, Morgan, i. 108.
Lewis, William, i. 127.
Liancourt, Duc de, describes Philadelphia, i. 28, 117;
on the Virginians, 33;
on life in Pennsylvania, 42, 45, 52;
on Virginia culture, 133, 157, 165.
Libraries, i. 61, 63, 129, 152.
Lincoln, Abraham, i. 171.
Lincoln, Levi, Attorney-General, i. 219, 304; ii. 2;
on the acquisition of new territory by the United States, 78.
Linn, James, member of Congress from New Jersey, i. 295.
Linn, John Blair, i. 123.
Liston, Robert, British minister, ii. 340, 367.
Literature, American, in 1800, i. 41, 75 et seq., 93.
Livingston, Edward, district-attorney and mayor of New York, i.
233, 295; ii. 259.
Livingston, Robert R., Chancellor, i. 69, 108, 112, 219;
appointed minister to France, 233, 295, 404;
discusses the price of Louisiana, ii. 31;
his claims convention, 46;
his estimate of the importance of the cession of Louisiana, 67;
claims West Florida, 68 et seq.;
his plan of gaining West Florida, 246, 275;
his situation after the treaty, 289;
distrusts Napoleon, 290.
Logan’s Act, ii. 259.
Longstreet, Judge, author of “Georgia Scenes,” i. 52.
Louisiana, loss of, regretted by France, i. 353;
retrocession by Spain to France, 363;
Talleyrand’s projet of treaty, 368;
treaty of retrocession signed, 370;
Bonaparte plans an expedition to occupy, 399;
boundaries fixed by Decrès, ii. 5;
commercial relations and sentiments prescribed toward the
United States, 8;
 treaty of cession to the United States signed, 42;
price of, 45;
importance of cession, 49;
Napoleon’s reasons for selling, 53;
Talleyrand’s explanation of, 55;
treble invalidity of sale, 56;
Constitutional question debated in Congress, 96 et seq.;
plans with regard to the status of, 116;
admitted without an amendment, 118;
bill for temporary government of, 120;
Breckenridge’s bill defining boundaries and government, 120
et seq.;
bill defining territorial government of, 125, 130;
Spain protests against sale of, 252 et seq.;
people regarded as unfit for self-government, 399;
they urge the execution of the treaty, 400;
report of Randolph upon their claims, 400.
“Louisianacide,” Napoleon’s, ii. 37.
Louverture, Toussaint, i. 354;
story of, 378 et seq.;
champion of Republican principles, 392;
seized and sent to France, 396;
his dependence on the United States for supplies, 406, 416;
his death, ii. 20.
Lowndes, William, i. 151.
Luisa, Queen of Spain, i. 345 et seq.
Lyman, Theodore, ii. 169.
Lyon, Matthew, member of Congress from Vermont, i. 295;
from Kentucky, his attack on Randolph, ii. 123, 216.

McKean, Thomas, Governor of Pennsylvania, i. 228;

declines to remove Judge Brackenridge, ii. 196, 259.
Maclay, William, senator from Pennsylvania, his description of
Jefferson, i. 185.
Macon, Nathaniel, of North Carolina, i. 149, 261;
chosen Speaker of the House, 267; ii. 95, 123;
opposed to the impeachment of Judge Chase, 150.
Madison, Bishop, of Virginia, i. 136.
Madison, James, and the Virginia Resolutions, i. 140 et seq.,
148, 177;
personal characteristics of, 188 et seq.;
appointed Secretary of State, 218;
makes no removals in the Department of State, 236;
distrust of, 248, 261;
a commissioner in the Yazoo sale, 304, 322, 332;
instructions of, respecting the retrocession of Louisiana, 405;
asks Pichon to remonstrate with Leclerc, 408;
writes to Livingston, 423, 426;
his orders to Pinckney, 427, 432;
invokes Pichon’s aid, 438, 439, 441;
writes instructions for Livingston and Monroe, ii. 2;
conversation with J. Q. Adams respecting the Louisiana
treaty, 117;
favors Yazoo compromise, 211;
instructs Monroe to bargain with Spain for West Florida, 248,
251;
explains the failure to demand West Florida, 256;
sends the ratified claims convention to Madrid, 260, 278, 279;
hopes to be relieved of Yrujo, 267;
communicates with Livingston respecting West Florida and
Yrujo, 262;
attempts to cajole Turreau, 273;
Turreau’s description of him, 274;
compromised by Pinckney, 276;
recalls Pinckney and hurries Monroe to Spain, 286;
denies that the Government aids desertion of seamen, 345;
communications to Thornton, 362;
proposes a convention with regard to impressments and the
blockade, 385;
remonstrates with Merry respecting impressments, 393.
Mail routes in 1800, i. 15.
Maine, convention for fixing the boundary between, and Nova
Scotia, ii. 358, 383.
Maitland, General, at St. Domingo, i. 385.
Malbone, Edward G., i. 149.
Manhattan Company of New York city, i. 65, 70.
Manners and morals, American, in 1800, i. 48 et seq.
Manufactures in New England in 1800, i. 22.
Marbois, Barbé, favors the cession of Louisiana, ii. 26.
Marbury against Madison, case of, ii. 145 et seq.
Marietta, Ohio, in 1800, i. 2.
Marshall, Chief-Justice, i. 133;
Jefferson’s antipathy to, 192;
personal characteristics of, 193;
detests Jefferson, 194;
his views of the Constitution, 260, 275, 290;
opinion of, respecting the powers of Government in the
Louisiana case, ii. 125;
appointment of, obnoxious to Jefferson, 145;
his decision in the Marbury case, 146;
his decision in the Yazoo case, 214.
Martin, Luther, his view of impeachment, ii. 223, 227, 231.
Mason, George, i. 133.
Massachusetts society in 1800, i. 76.
Meade, Bishop, of Virginia, i. 193.
Mediterranean Fund, the, ii. 141.
Merry, Anthony, appointed British minister to the United States,
ii. 360;
his arrival and reception by Jefferson, 361 et seq., 380, 381,
390;
dines at the White House, 369;
considers himself affronted and declines the President’s
invitations, 375;
union of, with Burr, 390;
writes to his Government, 392;
remonstrates with Madison respecting the enlistment of
deserters, 393;
receives a message from Burr, 395;
communicates Burr’s plan to his Government, 403.
“Messenger,” stallion, i. 51.
Milledge, Governor, and the Yazoo sale, i. 305.
Mint, opposition to, i. 299; ii. 77.
Mississippi, district of, created, ii. 257.
Mitchill, Dr. Samuel L., i. 69, 93, 110; ii. 153, 218, 238.
Mobile treated as a part of the United States, ii. 255, 257, 260–
263, 291, 293, 304, 380.
“Modern Chivalry,” i. 125.
Monroe, James, and the Callender scandal, i. 325;
nominated minister extraordinary to France and Spain, 433;
his instructions, 442;
sails for France, ii. 1;
his arrival in France, 26;
illness of, in Paris, 39;
his draft of claims convention, 41;
his share in the negotiation, 50;
under the influence of other men, 67;
commissioned to negotiate with Spain for West Florida, 248;
takes Rufus King’s place in London, 275, 288, 410;
his distrust of Livingston, 289;
returns to Paris, 292, 301;
is instructed to insist upon the right to West Florida, 301;
writes to Talleyrand, 304;
starts for Madrid, 307, 422;
receives answer from Talleyrand, 313;
in ignorance of Pitt’s schemes, 419;
interview with Lord Harrowby, 420;
warns the President to expect a change in British policy, 422.
Moore, Thomas, i. 48;
lines of, on the Philadelphia literati, 122;
his verses on Jefferson, 167.
Morfontaine, treaty of, i. 362, 370, 388; ii. 21, 42, 46, 47, 293,
296, 297, 383.
(See Treaties.)
Morocco, ii. 137.
Morris, Commodore, dismissed, ii. 137.
Morris, Gouverneur, i. 93, 279;
assails the Government, 435; ii. 99, 101, 283.
Morse, Jedediah, i. 78, 93.
Napoleon, i. 334;
and Talleyrand, 359;
restores peace in Europe, 360;
obtains retrocession of Louisiana, 363–370;
his anger with Godoy, 373–375;
makes peace with England, 374;
attacks Louverture, 390;
fears a war with the United States, ii. 2;
abandons his colonial system, 14 et seq.;
scene with Lord Whitworth, 19;
reveals his determination to cede Louisiana, 25;
angry scene with his brothers, 34 et seq.;
his projet of a secret convention respecting Louisiana, 40;
objects to the payment of claims, 51;
his inducement to sell Louisiana, 52;
his conduct toward Spain, 56;
his avowal as to the sale of Louisiana, 61;
his reasons for betraying Charles IV., 63;
for selling Louisiana, 63 et seq.;
repudiates drafts on the public Treasury, 270;
his irritation at Jerome’s marriage, 379.
Nash, Thomas, ii. 333.
Natchez delivered to the United States, i. 355.
“National Intelligencer,” i. 121.
Naturalization law adopted, i. 301.
Naturalization, the law of, in England and America, ii. 337 et
seq.
Navigation laws, British, ii. 318, 321, 413.
Navy, Jefferson’s opinion of, i. 222, 223, 238;
Gallatin’s views on, 222, 240, 252;
Giles’s views on, 287;
Leib’s proposal to abolish, 299;
condition in 1801, 242–245;
economies in, 272;
four sloops-of-war and fifteen gunboats built in 1803, ii. 77;
cost and estimates, 77, 136;
at Tripoli, 137–141, 425–436.
Nelson, Roger, ii. 229.
New England in 1800, i. 18;
school-houses, 19;
population, 20;
poverty, 21;
commerce and manufactures, 21 et seq.;
social system, 76;
schools, 76;
society, organization of, 108.
New Haven, i. 75.
Newspapers, American, in 1800, i. 41, 120.
New York city in 1800, tax valuation of, i. 23;
behind New England, 23;
population, 24;
like a foreign seaport, 24;
expenses and sanitary condition, 25;
business, 25 et seq.;
society of, 113.
New York State in 1800, i. 3, 6, 23, 108–114.
Nicholas, Wilson Cary, i. 221;
dissuades the President from raising Constitutional question,
ii. 88, 94, 111, 221.
Nicholson, Joseph H., i. 261, 268, 433; ii. 95, 100, 124, 144;
and the attack upon Judge Chase, 149, 225, 228;
offers an amendment to the Constitution, 240.
North Carolina in 1800, i. 36;
cotton planting, 37, 148.

Offices, Jefferson’s removals from, i. 230 et seq.

Ohio, admitted, i. 302.
Ohio River settlements in 1800, i. 2.
Ohio, Territory of, ii. 121.
Olcott, Simeon, senator from New Hampshire, ii. 160.
Orleans, Territory of, ii. 121.
Osgood, Samuel, i. 108.
Otis, Harrison Gray, ii. 163.
Paine, Robert Treat, i. 330.
Paine, Thomas, Jefferson’s letter to, i. 316, 327.
“Palladium,” the, i. 314.
Parker, Admiral, ii. 340.
Parliament. (See Acts of.)
Parma, Duchy of, i. 363, 371.
Parsons, Chief-Justice Theophilus, i. 48, 87, 89, 93; ii. 164.
Party, the Federalist, in New England, i. 76, 82–89, 329; ii. 160,
170, 202;
in New York, i. 109; ii. 171, 191;
views on government, i. 252;
on the Judiciary, 273–275, 279, 290, 297;
on the treaty-making power, ii. 99–100, 105, 110, 111.
Party, the Republican, in New England, i. 76, 329, 330; ii. 81,
201, 202;
in New York, i. 108, 109, 113, 229–236, 331; ii. 171–191;
in Pennsylvania, i. 116, 194–200;
in Virginia, 138–143, 145–148, 179;
in North Carolina, 148;
in South Carolina, 152–154;
political principles of, 199–217, 238–243, 247, 251, 272, 287;
ii. 77, 78, 130, 134, 142, 203, 205, 254–262;
leaders of, in Congress, i. 264–269;
views of, on the Judiciary, 275, 276, 288–290, 297; ii. 143–
159, 221–244;
on the treaty-making power, 78–80, 83–91, 94–99, 100–104,
106–112;
on the power of Congress over territories, 116–129;
on exclusive privileges, 208–210;
on British relations, 349, 355, 356;
success in 1803, 74–77;
in 1804, 201.
Patronage, public, Jefferson’s course regarding, i. 224, 294.
Patterson, Elizabeth, ii. 377.
Paulus Hook, i. 11.
Peace, Prince of. (See Godoy.)
Pêle-Mêle, ii. 365, 372, 390.
Pellew, Captain, of the “Cleopatra,” ii. 340.
Pennsylvania in 1800, i. 29, 114, 115;
schism, the, ii. 194 et seq.
Perkins, Jacob, i. 182.
Philadelphia in 1800, i. 28, 29;
library company, 61;
intellectual centre in 1800, 117.
“Philadelphia,” the frigate, captured, ii. 138.
Physick, Dr., i. 127.
Pichon, French chargé d’affaires, remonstrates with Leclerc and
is superseded, i. 408; ii. 268;
complains to Talleyrand of the attitude of the United States,
437, 439;
observes Jefferson’s close relations with Thornton, 354;
invited by Jefferson to meet Merry at dinner, 369.
Pickering, Judge John, impeachment of, ii. 143 et seq.;
trial of, 153 et seq.;
irregularity of trial, 158.
Pickering, Senator Timothy, i. 88;
and Yrujo, 425;
on the admission of Louisiana to the Union, ii. 105, 110 et
seq., 160;
his letter to George Cabot on the impending dangers, 161,
164;
receives Cabot’s reply, 166 et seq.;
letter of, to Rufus King on Burr’s candidacy for the
governorship, 179, 390, 391.
Pinckney, Charles, i. 152;
appointed minister to Madrid, 294, 427;
obtains a convention for Spanish depredations, ii. 249 et seq.;
indiscretions of, at Madrid, 275;
compromises Madison, 276;
adopts a high tone with Cevallos, 279;
sends him a threatening letter, 280;
excuse for his conduct, 281;
in an awkward situation, 284;
his recall asked for, 286;
 asks the Spanish government to be permitted to resume
relations, 315.
Pitt, William, ii. 316, 320, 324, 326, 328, 330, 336, 342;
restored to power, 396, 418;
determined to re-establish the former navigation laws, 419.
Pittsburgh in 1800, i. 2.
Plumer, William, senator from New Hampshire, ii. 160, 364, 405.
“Polly,” case of the, ii. 328, 340.
Population of the United States in 1800, i. 1;
centre of, near Baltimore, 1;
west of the Alleghanies in 1800, 3;
of cities, 59.
“Portfolio,” the, i. 85, 119, 121.
Postal system of the United States in 1800, i. 61.
Pozzo di Borgo, ii. 66.
Preble, Commodore Edward, appointed in command of the
Mediterranean squadron, ii. 137;
at Tripoli, 426.
Prevost, J. B., ii. 220.
Priestley, Dr. Joseph, i. 157.
Prince of Peace. (See Godoy.)
Princeton College in 1800, i. 129.
Prisons in 1800, i. 128.

Ramsay, David, i. 151.

Randolph, John, i. 143, 209;
in favor of anti-Federal declarations, 260, 267, 296, 338;
demands papers relating to the right of deposit at New
Orleans, 429; ii. 95;
defends the President in Congress, 97, 120, 124, 133, 142,
144;
impeaches Judge Chase, 151;
opposes remission of duties on school-books, 208;
decline of his influence, 210;
on the Yazoo claims, 210;
his violent temper, 213;
supported by the Administration, 220;
 opens the trial of Judge Chase, 229;
his closing speech, 236;
his amendment to the Constitution, 240, 241;
asserts title to West Florida, 255;
complains of Jefferson’s credulity, 409.
Randolph, Thomas Mann, ii. 95, 124.
Rawle, William, i. 127; ii. 259.
Reeve, Judge Tapping, ii. 168.
Representation, ratio of Congressional, fixed, i. 301.
Republicans. (See Party.)
Retaliation acts, ii. 397 et seq.
Rhode Island, roads in, i. 64.
Rigaud, i. 384, 386.
Roads in 1800, i. 2, 5, 11 et seq., 14, 63, 64;
over the Alleghanies in 1800, 2.
Robbins, Jonathan, case of, ii. 333.
Rochambeau, General, succeeds Leclerc at St. Domingo, ii. 15.
Rodgers, John, at Tripoli, ii. 429.
Rodney, Cæsar A., elected to Congress in place of James A.
Bayard, ii. 76, 95;
a Republican leader, 100;
defends the Louisiana treaty, 102;
reports Jefferson’s bill for administering Louisiana, 119;
shares in the trial of Judge Chase, 219, 228, 234.
Rose, George, vice-president of the board of trade, ii. 419.
Roume, Citizen, French agent in St. Domingo, i. 384, 387.
Rule of the war of 1756, ii. 322, 323, 329.
Rutledge, John, i. 269, 271.

Sailors, British, their desertion to American service, ii. 332 et

seq.
St. Cyr, General, pledges France never to alienate Louisiana, i.
400; ii. 61.
St. Domingo ceded to France, i. 354, 378 et seq.;
destruction of the French army in, 414;
relations of United States to, ii. 326.
Saratoga, i. 92.
Sauvé, Pierre, ii. 401, 406.
Scott, Dred, case of, ii. 126, 129.
Scott, Walter, i. 126.
Scott, Sir William, his judgments in admiralty cases, ii. 327.
Schuylers of New York, the, i. 108.
Search, right of, ii. 322.
Senate, as a court of impeachment, ii. 223.
Sheffield, Earl of, his devotion to the British navigation laws, ii.
413.
Shippers, British, ii. 318, 320.
Shipping, character of, in 1800, i. 6;
American, increase of, ii. 325.
Sidmouth, Lord. (See Addington.)
Silliman, Professor Benjamin, i. 310.
Skipwith, Fulwar, U. S. consul, attacks Livingston, ii. 289.
Slave-trade, restrictions of, in Louisiana, ii. 122.
Slavery, i. 134–136, 150, 154.
Smith, Senator Israel, of Vermont, ii. 218.
Smith, John Cotton, i. 269.
Smith, Senator John, of New York, ii. 153.
Smith, Senator John, of Ohio, ii. 218.
Smith, Robert, appointed Secretary of the Navy, i. 220 et seq.,
373, 431.
Smith, Samuel, member of Congress from Maryland, appointed
temporarily Secretary of the Navy, i. 219;
his character, 267;
moves to purchase Louisiana, 433;
his vote on Chase’s impeachment, ii. 238;
his wish to be minister to Paris, 378.
Smiths, the, of Baltimore, i. 93.
Somers, Lieutenant, at Tripoli, ii. 427.
South Carolina in 1800, i. 37;
brilliant prospects of, 39, 149 et seq.;
contrast in the character of its people, 153 et seq.
Spain, relations of, with the United States, i. 337 et seq.;
clumsiness of her colonial system, 419;
declares war with England, ii. 303.
Spanish claims convention, ii. 249;
defeated in the Senate, 250;
ratified, 278;
conditions on ratification imposed by Spain, 280.
Spanish depredations claim. (See Pinckney.)
Spencer, Ambrose, i. 109, 112, 228, 233.
Stage-coaches, travel by, i. 11 et seq.
State-rights, asserted by Virginia, i. 138–140;
by Kentucky, 140–143;
by Georgia, 304; ii. 215;
affected by Jefferson’s acts, i. 203, 205, 254, 255, 260, 263,
298; ii. 78, 85, 90, 114, 118, 125, 130, 203, 205, 210;
Gallatin’s attitude toward, i. 116; ii. 79, 80;
Bayard on, i. 292;
Randolph on, ii. 97, 98, 104, 120, 209, 211;
Nicholson on, 102, 209;
Rodney on, 103, 119;
Pickering on, 105;
John Taylor of Caroline on, 105–107;
Breckenridge on, 109, 121;
W. C. Nicholas on, 111–113;
Chief-Justice Taney on, 127;
Justice Campbell on, 127–129.
Steam-engines in America in 1800, i. 66, 68, 70.
Stevens, Edward, consul-general at St. Domingo, i. 385 et seq.,
389.
Stevens, John, i. 69, 182.
Stewart, Charles, at Tripoli, ii. 428.
Stoddert, Benjamin, i. 192, 219.
Story, Joseph, his description of Fulton’s discouragements, i. 71;
of Marshall, 193, 260;
of Jefferson’s dress, ii. 366.
Stone, Senator David, of North Carolina, ii. 95, 157.
Stowell, Lord. (See Sir William Scott.)
Stuart, Gilbert, i. 127.
Sugar, stimulated production of, and subsequent glut in the
West Indies, ii. 415.
Supreme Court, the, i. 274;
sessions suspended for a year by Congress, ii. 143.
Sutcliffe, Robert, i. 34.
Swartwout, John, i. 109, 230;
his duel with De Witt Clinton, 332.

Talleyrand, i. 335;
his colonial schemes, 352 et seq.;
becomes French minister of foreign affairs, 353;
his negotiations with the American commissioners, 355;
his instructions for Guillemardet, 355;
his mistakes, 357;
obliged by the X. Y. Z. affair to retire, 358;
restored by Bonaparte, 359, 412;
his letter with regard to Louisiana, 400;
denies the retrocession of Louisiana, 409;
his instructions to Bernadotte, ii. 11;
opposes the cession of Louisiana, 25;
proposes it to Livingston, 27;
explanation of the sale of Louisiana, 55;
assures Cevallos of Napoleon’s opposition to the American
claims, 293;
his instructions to Turreau, 295;
reassures Cevallos, 297;
his attitude toward the United States, 309;
report to the Emperor on Monroe’s note, 310;
answer to Monroe, 313.
Taney, Chief-Justice, opinion of, respecting governmental
powers in the Louisiana case, ii. 126, 128.
Taxes, abolition of, i. 240, 270, 272.
Taylor, John, of Caroline, i. 143, 146, 263, 338; ii. 94;
his remarks on the Louisiana purchase, 105.
Taylor, Judge, ii. 177.
Temperance in United States in 1800, i. 47.
Tennessee, population of, in 1800, i. 2.
Terry, Eli, i. 181.
Texas, a part of the Louisiana purchase, ii. 256.
Theatre in New England in 1800, i. 49.
Theatres in Boston, i. 90.
Thompson, Smith, i. 108.
Thornton, Edward, his description of the inauguration of
Jefferson, i. 198, 436, 440;
letter to Hammond, ii. 342, 388;
complains that desertion of seamen is encouraged, 345;
Jefferson’s confidential relations with, 347;
proposals with regard to Monroe’s mission, 351;
on change on tone in 1804, 387, 388.
Thornton, Dr. William, i. 111.
Ticknor, George, i. 63, 94.
Tracy, Senator Uriah, of Connecticut, his reply to John Taylor of
Caroline, ii. 107, 238.
Travel in America, difficulties of, in 1800, i. 11 et seq.
Treaty, preliminary between Great Britain, France, and Spain,
Nov. 3, 1762, i. 353; ii. 7, 70;
definitive between the same, Feb. 10, 1763, i. 353; ii. 6;
definitive between Great Britain and Spain, Sept. 3, 1783, i.
353;
definitive between the United States and Great Britain, Sept.
3, 1783, ii. 90, 411;
Jay’s, between the United States and Great Britain, Nov. 19,
1794, i. 348; ii. 316, 334, 339, 355, 421, 424;
of Basle, between Spain and France, July 22, 1795, i. 354;
Pinckney’s, between the United States and Spain, Oct. 27,
1795, 348, 349; ii. 246;
between Toussaint and Maitland, June 13, 1799, i. 385;
of Morfontaine, between the United States and France, Sept.
30, 1800, 362, 388; ii. 21, 42, 46, 47, 293, 296, 297, 383;
Berthier’s, between Spain and France, retroceding Louisiana,
Oct. 1, 1800, i. 370, 401, 403; ii. 43, 58, 70, 254;
of Lunéville between France and Austria, Feb. 9, 1801, i. 370;
of Lucien Bonaparte between Spain and France, March 21,
1801, 372, 406, 409; ii. 299;
of Badajos between Spain and Portugal, June 5, 1801, i. 372;
 preliminary, between Great Britain and France, Oct. 1, 1801,
374; ii. 344;
settling British debts between Great Britain and the United
States, Jan. 8. 1802, 358, 410;
of Amiens between Great Britain and France, March 25, 1802,
59, 290, 326, 347, 385, 414, 416;
of claims between the United States and Spain, Aug. 11,
1802, 21, 250, 259, 278, 280, 293, 296, 297, 383;
between France and the United States, ceding Louisiana and
settling claims, 39–49, 51, 67, 85, 88, 92, 97, 100, 102,
105, 107, 108, 111, 245, 275, 289, 302, 308, 355, 399–
401;
between the United States and Great Britain for settling
boundaries, May 12, 1803, 358, 383, 384, 391, 392, 410,
420, 424;
between the United States and Tripoli, Nov. 4, 1796, i. 244;
June 4, 1805, ii. 434, 436.
Treaty-making power, defined by W. C. Nicholas, ii. 87, 88, 112;
by Jefferson, 89, 90;
by Gaylord Griswold, 96, 97;
by Randolph, 98, 99;
by Gouverneur Morris, 100;
by Nicholson, 101;
by Rodney, 102, 103;
by Pickering, 105;
by John Taylor of Caroline, 106, 107;
by Tracy, 108;
by Breckenridge, 109;
by J. Q. Adams, 111;
by Cocke, 113;
summary of opinions on, 114, 115.
Tripoli, the war with, ii. 137, 426 et seq.;
Pacha of, 430;
peace with, 436.
Trumbull, John, i. 101.
Turnpikes, prejudice against, i. 64 et seq.
Turreau, Louis Marie, appointed minister to the United States by
Napoleon, ii. 268;
his domestic quarrels, 269;
complains of the discredit of France, 271;
embarrassments of, 272;
his description of Madison, 274;
receives instructions from Talleyrand, 296;
presented to Jefferson, 405;
describes General Wilkinson, 406.

Unitarians in New England, i. 89.

United States, banking capital of, in 1800, i. 26;
credit and trade of, 27;
monetary valuation of, in 1800, and distribution of wealth, 40;
popular characteristics of the people of, in 1800, 41 et seq.;
standard of comfort, 42.
Urquijo, Don Mariano Luis de, i. 355, 365, 368.
Utica in 1800, i. 3.

Van Ness, William P., i. 109;

author of pamphlet by “Aristides,” ii. 73, 171;
carries Burr’s demand to Hamilton, 186.
Vanderbilt, Cornelius, i. 28.
Varnum, Joseph B., member of Congress from Massachusetts,
ii. 123.
Victor, Marshal, to command the forces in Louisiana, ii. 5.
Vincent, Colonel, i. 382.
Virginia in 1800, i. 32;
farming in, 33, 131 et seq.;
horse-racing, 51;
Washington’s views on the value of land in, 135;
Church and State in, 136;
adoption of the Constitution by, 139;
Resolutions, 140 et seq.;
law to prevent extradition, ii. 334, 345, 398.
Virginians, i. 133 et seq.;
of the middle and lower classes, 137;