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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.
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 AN ARAB CHIEF.

On the next page we have an Arab chief. How do you like his
looks? That long robe he has over his white cotton skirt, and the
scarf on his head are of camel’s hair—there is no doubt about that—
but, if you admire his bare legs and arms, and old slippers, it is more
than I do. And I can tell you of something that you can’t see in the
picture. The whole dress is shockingly dirty, and greasy.
Did you ever reflect how these “noble Arabs” get anything to eat?
They must eat, you know, and they won’t work; so, how do they
procure their food? Why, they steal it. They despise their brethren
who dwell in houses, and plow and plant seed. They think work is
degrading. But after the farmers have got their fields in good order,
and the grain is ready to cut; down comes a tribe of Bedouins and
carries off the harvest!
They entertain strangers, but only to beg from them, and what they
fail to get by begging they will steal, if they have a chance.
Their generosity seems to be a reckless wasting and giving away
of what they ought to save; and no people can drive so hard a
bargain, or cheat more readily.
As for gratitude—well—if a man has done them a favor they
perhaps tell him fewer lies, and cheat him less than they do others.
The camel is a very important animal in the deserts where the
Bedouins live, for he can easily tread the sands, and can live a long
time without water, and can bear heavy burdens. But he is very, very
stupid, and ill-natured, and obstinate. Perhaps the poor beasts would
do better if they had better masters, for the Bedouins half starve
them, and constantly ill-treat them; and I don’t blame the camels for
resenting such conduct.
It is not likely that such a race of people would treat horses any
better than they do their camels. Horses could not bear such
treatment long, however. It would kill them. And in fact, the Bedouins
have very few horses. The fleet and beautiful Arab steeds are owned
by the Arabs who dwell in the villages and try to live somewhat as
we do.
 AN ARAB ENCAMPMENT.
Tent life is very pleasant, for a few days, when you go out into the
green woods with a party of friends. But it would be a very different
thing, you would find, if you were compelled to spend your life that
way; sometimes under the shade of palms, but, more frequently on
the hot desert sands. Dirt and discomfort belong to an Arab tent; and
legions of fleas take up their abode there.
If you were to stay with these Bedouins for awhile I think you
would gladly go back to civilization and work; and you would come to
the conclusion that schools and wash-tubs were good institutions.
 FOOL-HARDY CARL HOFER, AND THE
WATER-LADY.
A good many years ago, on the banks of the Rhine, there lived a
boy named Carl Hofer. “Climbing Carl” he was often called because
he excelled in climbing; and, quite as frequently, he was called “Fool-
hardy Carl,” because he would put himself in very unsafe places,
where no sensible person would venture. Everybody said he would
be killed some day; and the wonder was that he had reached the
age of fourteen years without breaking his neck. His father and
mother had tried every means of curing him of these foolish ways;
but, although he was a pretty good boy in regard to most things, he
was very disobedient about climbing.
His parents were willing he should climb even the tallest trees; and
they were quite proud at the gymnasium to see him run lightly up the
long ladders, and across the open framework, near the roof. You
might say that this also was a dangerous thing to do. That is true, but
Carl’s skill in this art, and his long practice made it next to impossible
that he should fall. But he would go up places where no amount of
skill or practice could save him in case of accident. He would climb a
dead tree, for instance, though he knew a rotten branch might break
at any moment, and throw him headlong to the ground, or he would
go up a tottering wall. It is courageous to put yourself into possible
danger, for the sake of accomplishing some good. No boy can learn
to ride, or climb, or swim without incurring possible danger. But that
is very different from putting yourself into almost certain danger just
for the sake of doing a thing when no good is to come of it. When
people act in this way they are fool-hardy.
And Carl was not content to be courageous, which is a very good
thing, but he must also be fool-hardy, which is a very silly thing.
 THE PLACE WAS STRANGE TO HIM.
One day he set out alone for a long walk down the river. It was a
holiday, so he had plenty of time before him. He walked a very long
time before he sat down to rest; and then he looked around him to
see where he was. The place was strange to him, so that he knew
he must be a long way from home. There was no house near, and no
person was in sight. But Carl was not afraid, for he was used to
rambling about the woods, and he felt sure there was nothing there
to hurt him.
There was nothing to hurt him but his own foolish self.
Close by him was a beautiful hill, down which fell a little cascade.
It was not very high, but rose up almost perpendicularly from where
he was sitting. He felt a great desire to see what was on the other
side of that hill. He could easily have gone around it, on the inland
side, but that did not suit his taste. He remembered that he had
given his promise to his mother, that morning, that he would not do
one fool-hardy thing that day. But was this fool-hardy? The hill was
very steep, but there were trees and saplings to help him in the
ascent. He did not hesitate long. He started up the hill. If he had
continued up the side he began upon, it would not have been so very
bad, for if his foot had slipped he might have had his fall so broken
by bushes and tufts of grass that there would have been a possibility
of his reaching the ground without any great injury. But he soon
found that the side of the hill by the river was even more steep than
the one he was on, and he swung himself round by the tree
branches until he reached that side. Up he went, digging hands and
heels into the spongy turf, and catching hold of the saplings, and
bushes that came in his way. If his foot had slipped then, he would
have gone plump into the river.
But his foot did not slip, and he reached the top in safety. A little
ravine lay at his feet, and on the other side of this, close to the river
bank, there stood a stone tower. Eager to examine this curiosity, Carl
partly ran, and partly slid down the hill, which was much less steep
on that side, and ran across the ravine to the base of the tower.
It was all that was left of an old castle. Many of the stones had
fallen from the top, and some from its sides, and it was a very shaky-
looking affair. But Carl did not care for this. The walls were very
thick, and he felt sure the large broken pinnacle at the top was broad
enough for him to stand on. It would be great fun to stand on that! He
forgot his promise to his mother, and began at once to climb;
sometimes lifting himself up by taking hold of projecting stones, and
sometimes working up by putting feet and hands into crevices in the
wall.
He was not half way up when he made a mis-step. He felt that he
was slipping, and clutched frantically at a projecting stone. He
grasped the stone with both hands, but alas! it shook with the grasp,
and Carl knew that it was giving way. He hung thus but a moment,
though it seemed a long period to him, for he had time to think of his
home, and his father, and mother, and little sisters, and that he
should never see them more. He wondered if they would ever know
what had become of him, and would learn, that he did die, finally, in
a fool-hardy adventure, as everybody had always said he would.
Then the stone rolled out from the wall, and out of Carl’s hands,
falling some thirty feet, and plunging into the water with great force.
And down went Carl, right in its track.
This part of the river was the home of a kind, and beautiful Water-
Lady, called by the Germans a Nix. Looking up through the water (for
she spent nearly all her time at the bottom of the river) she saw Carl
climb the hill, and was so much pleased with his skilful climbing and
his bright face, that when he reached the top of the hill, she floated
up to the surface of the water to see what he would do next. She
watched him down the hill, and across the ravine; but, when he
stood looking up to the top of the ruined tower, the Nix guessed that
he was thinking of climbing it; and she determined to draw him away
from this dangerous place.
The Nixies play upon the harp lovely music that mortals may not
hope to play. So the Nix went down to the bottom of the river and
soon reappeared on the surface with a graceful harp, made of
beaten gold. She left the river, and, standing among the water plants
at the foot of the hill Carl had climbed, she played soft, sweet strains
of fairy music on her harp. In this way she thought she would beguile
him from the dangerous tower back to the hill; and, when he was
safe, she would disappear; for the Nixies do not care to be seen of
mortals.
But Carl was so absorbed in his foolish project of scaling the wall,
and the music was so very soft, he did not heed it. Twice in his
ascent he paused to listen to what he imagined to be lovely strains of
music. This was when the Nix, on peeping around the curve made
by the hill, saw that the boy had already started on his perilous
journey, and played louder to call him back. But Carl concluded he
was mistaken, and that the melodious sound was the wind rustling
among the vines.
When the Nix heard the plunge into the water she supposed that
all was over; and, standing her harp against a rock, she leaned her
head upon her hand, and thought sorrowfully of the bright boy who
had come to such a sudden end through his own folly.
But Carl was not dead. The force with which he struck the water
sent him far down into its depths, and rendered him unconscious. So
that when he rose to the surface again he lay on the water without
motion, and, apparently, without life. In this condition he floated to
the spot where the Nix was standing. For a moment she gazed at
him sorrowfully, and then her face suddenly brightened. For she saw
that the boy was still living, though he was insensible to everything
around him.
Quickly she seized her harp, and played the liveliest, merriest
music that the fairies know. The notes seemed to be dancing, and
jumping, and rolling and tumbling over each other in great glee, and
yet it was true music, and perfect harmony. So penetrating and so
stirring was it that it reached Carl’s benumbed senses. He opened
his eyes, and seeing a beautiful lady in white robes, holding a golden
harp, and playing this lovely music, no wonder he thought he was in
heaven.
 THE NIX GRIEVING FOR CARL.
This delusion lasted but a moment, however, for he soon felt
himself sinking again into the cold water. But he was able now to
make an effort to save himself, and he grasped tightly the long reed
stems that lay near him. This prevented his sinking far into the water,
and the Nix left her harp, and gliding swiftly into the river, supported
Carl so that his head and arms were out of the water, and he could
make some attempt to swim. And, in this way, the Nix helped him to
the bank.
 He was so weak from fright, and the long time he had been in the
water, that he could not even speak to the Nix to thank her for saving
his life. He could only look his gratitude as he lay panting on the
grass. But as soon as he revived a little and had uttered the first
word to the lady she faded from his sight, and he only saw a wreath
of white mist gliding over the reeds.
Carl sprang up in astonishment. The waves parted as if some one
had gently sunk into them, and he thought that he saw, for a moment
a gleam of bright hair. Not till then did he know that the beautiful lady,
who had preserved him, was a Nix.
Close to his side stood her harp. The Nix had forgotten it! Here
was a prize! There was gold enough in it for a moderate fortune, and
Carl was poor. Carl had always had a great desire to be a musician,
and this gold would send him to Berlin or Vienna to study at a
Conservatory of Music; and do a great deal besides for his father,
and mother, and sisters. But the boy was honest, and he knew he
had no right to take away the property of another, even if the owner
was only a Nix. But he thought he might be allowed to play upon it.
He had learned to play two or three tunes on the harp. No sooner did
he touch the strings, however, than he found he did not play his own
music at all, but the magical music the Nix played. Carl was in
ecstacies, and his fingers flew over the strings, wandering through
one fairy melody after another until his arm ached, and he saw that
the sun had set, and twilight was coming on.
He must go home. But now he felt a stronger desire than ever to
take the harp with him. How he would astonish all the town with his
music! He would give concerts in the great hall, and, perhaps, the
fame of his wonderful music would reach the king and queen, and
they would come to hear him. But all this did not make it right for him
to take what was not his own; and it would be a poor return to make
the Nix for her kindness to steal her harp.
But, perhaps she left it there, intending he should have it! How
was he to know? He called to her to tell him if the harp was his, but
there was no reply.
 He resolved he would leave it where it stood, but would return to
the spot the next day. If the harp was still there he might fairly
conclude that the Nix intended he should have it.
He left the harp reluctantly, and started on his homeward journey,
but had not gone far before he had to lie down and rest. His head
ached, and all his limbs felt tired and sore. It is probable he would
have been obliged to spend the night in the forest, if some
marketmen had not come along the road, and taken him home in
their wagon.
He related his adventures to the family, and the next day his father
accompanied him to the old tower. Everything was exactly as Carl
had described it. The place whence the stone had fallen out of the
wall was plainly to be seen, with the freshly loosened mortar strewn
about. But there was no golden harp. And there was neither sight nor
sound of Nix or Fairy Music.

FAIRY MUSIC.
From that day Carl lost all desire for fool-hardy adventures. His
love of music grew stronger and stronger, and his parents had some
trouble in getting him to attend properly to his other studies. He said
the Nix had left her harp with him for a short time that he might take
from it an inspiration of melody that would be his forever; and that
she had then taken the harp away lest he should learn too much,
and play such music as only the angels could understand.
All the beautiful things he saw; all the sweet sounds of Nature; all
the noble thoughts that God put into his heart; he wrote down in
strains of music that were sung and played in all parts of the world,
and that charmed everybody who heard them.
Carl was famous. But men declared that he had never seen the
Nix, or played upon the golden harp, but had dreamed the whole
story when he was in a half-conscious state on the bank, after he
had managed to crawl out of the river by the help of the reeds. This
narrow escape from death, they said, had given a more serious turn
to his mind, and from thenceforth he had given up boyish frolics, and
his thoughts had naturally turned to music—the art he best loved.
But Carl, himself, always believed that the Nix had bestowed upon
him the wonderful gift of melody he possessed.
WATER AND MILK FROM PLANTS.
PITCHER PLANT.
 There are upon the earth great sandy tracts, where there are no
springs, or brooks. When the rain falls, which it seldom does in these
places, the parched earth drinks it all up, and no pools are formed at
which the thirsty traveler can get a drink. And yet men are often
obliged to travel over these plains to reach some place where their
business calls them. They go in companies, and take with them
provisions, and a large supply of water. This last they regard as the
most precious of their possessions, and use it as sparingly as
possible. But, notwithstanding all their care, it often gives out before
they reach the end of their journey. And then, too, they frequently
lose their way, and wander about over the hot sand, under a burning
sun until they become sick and weak from thirst, and they sometimes
die for want of water. This would happen much oftener than it does
were it not for a little plant that a kind Providence has caused to grow
in these desolate sandy plains.
The picture of this plant, which we show you, was taken from one
that grew in a garden, but it was transplanted there from the desert,
where it is found in great abundance.
This plant grows two or three feet high, and, at the end of each
one of its broad dark green leaves, there is a strong tendril that holds
up a cup of the same substance as the leaves. During the night the
dew on the plant fills the cup with pure, clear, sweet water, which
slowly evaporates during the day. You can easily imagine how glad
the thirsty traveler is to find these cups of fresh water, all filled ready
for his drinking.
The name of this plant is Nepenthes, but we generally call it the
Pitcher Plant.
In other parts of the earth there are great marshy forests, where
the pools of water are stagnant and impure; and, if people drink from
them, they are made sick. A man might wander through these woods
for days, and not find a drop of pure, wholesome water, were it not
for the Sarracenia, or Amphora-plant.
In this the leaves are the cups. They have narrow necks, and
flaring tips, from which it is easy to drink the clear water contained in
the wonderful leaves. The full grown leaves of the larger species
hold a pint of water.

THE SARRACENIA.
We have this same plant, on a much smaller scale, in our own
marshes. It grows in damp, shaded places, and I advise you to look
for it in your summer rambles, for it is a very singular plant. The
leaves of our Sarracenia are so small they will scarcely hold a gill of
water. But we have plenty of cool springs, and limpid brooks in our
country, and do not need the large cups of water the Amphora-plant
offers to its visitors in South America.
 THE WEEPING TREE.
The common name of our Sarracenia is Pitcher-plant; but, as you
can see by comparing the two, it is very unlike the Pitcher-plant of
the Eastern deserts.
But then you know pitchers are of a great many different shapes,
and sizes, and are only alike in being able to hold water.
But the most wonderful of all the plants that give men water to
drink is a tree that is said to have been found some years ago in one
of the Canary islands. It was seen at different times by different
travelers, and they all told the same story about it. The leaves grew
thickly on its spreading branches, and, from each leaf the drops fell
so rapidly that all together they formed a steady shower of rain.
It was called the Weeping Tree.
The water fell so copiously that it formed a pond at the foot of the
tree, and the people who lived in the neighborhood got from it all the
water they used. This is certainly a very wonderful tree if the
accounts of it are true.
There is a plant of the Arum family, with broad, heart-shaped
leaves that constantly throws from the end of each leaf a drop of
water. These drops sometimes follow each other so fast that there is
a little jet of water formed in the air above the leaf.
But water is not the only drink that we get from trees. In Central
and South America grows the cow-tree, which gives milk! This milk
can be obtained during all seasons, but is much more abundant in
the spring. If a deep cut is made with a hatchet in the bark of the tree
a stream of milk gushes out, and flows freely. It yields the greatest
quantity at sunrise, and, at that hour, in the places where this tree
grows, men and women come from all directions to the tree nearest
their homes to get a supply of this refreshing drink. They bring
pitchers with them, and take some of the milk back to their families.
This white fluid is like cow’s milk in appearance, but it is not
equally good from all trees. But it is just so with the cows, you know.
Some of these animals give rich yellow milk, and some of the milk is
blue-white, and thin. Some give a great deal, and others very little.
And some cow trees yield richer and yellower milk than others, but it
is all sweet and wholesome, and of a pleasant smell. It tastes, in
fact, almost exactly like cow’s milk. Like that it is used for making
custards, puddings, &c.; and, when boiled, behaves just as ordinary
milk does, and will run over the vessel in a minute, if not watched.
When allowed to stand for a time cream forms on the top. This is
taken off, and made into a sort of cheese, not very different from our
cheeses.
 THE COW TREE.
This is a very nice kind of cow to have—this vegetable cow—as it
requires no feeding, or care, and, when it dies others spring up in its
place. It seems a pity that we cannot have these economical cows in
our country.
We have plants here that yield a milky juice when the stalks are
broken or cut, but you must not be beguiled into drinking any of
these milky saps, for they are very disagreeable in taste, being sharp
and bitter; and many of them are poisonous.
 THE JOLLY CABORDMEN.

There was once a nation of remarkably genial people who knew

no evil and would not have practiced it if they had known it. They
were very industrious, and their days were so busy and they took
such an interest in their work, that they had no time to be wicked or
sad.
They were called Cabordmen, for what reason I know not, for the
name of their country was not Cabord. Their principal industry was
tilling the soil, and they generally worked with a will.

THE JOLLY CABORDMEN AT WORK.

When they first settled their country the land was poor and very
little grew upon it that was worth having. But, year by year, the soil
became richer, on account of the care they took of it, and all sorts of
valuable grains, and grasses, and vegetables, and fruits were grown,
and these Cabordmen had all and more than they wanted of the
good things of the earth.