Theagarten Lingham-Soliar

The Vertebrate
Integument
Volume 2
Structure, Design and Function
The Vertebrate Integument Volume 2
A design principle of alternate layers of oppositely oriented crossed fibers widely
occurring in nature. The figure shows some of its diverse occurrences in animals
and plants. Centre shows a schematic view of the crossed-fiber architecture in the
white shark Carcharodon carcharias and top right, an exploded schematic view.
Bottom, left is a schematic view of the cuticle of the worm, Ascaris lumbricoides
(Chap. 2) and far right an unmineralized barbule from a duck 3500 BP (Chap. 5)
Theagarten Lingham-Soliar

The Vertebrate Integument

Volume 2
Structure, Design and Function

13
Theagarten Lingham-Soliar
Environmental Sciences
Nelson Mandela Metropolitan University
Port Elizabeth
South Africa
and
Honorary Academic Address
Life Sciences
University of KwaZulu-Natal
Durban
South Africa

ISBN 978-3-662-46004-7 ISBN 978-3-662-46005-4  (eBook)

DOI 10.1007/978-3-662-46005-4

Library of Congress Control Number: 2013957128

Springer Heidelberg New York Dordrecht London

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Dedicated to the Children of Soweto 1976
Preface

In Volume 2 of The Vertebrate Integument the emphasis is on the structure and

functional design of the integument (including its derivatives) and contribution to
locomotion in phylogenetically diverse vertebrates. The need for such a book was
precipitated by seminal research by many workers, some who have become close
colleagues but all whose work is inspirational. The subject of the book may appear
complex but again as in Volume 1, it is profusely illustrated with figures and
photographs. The primary discussions involve motion in fluid—swimming and aerial
flight. The book starts with a discussion on some of the physics involved in motion
in fluid, including Newton’s Three Laws of Motion.
Our knowledge of how the integument contributes to vertebrate flight dynamics
has expanded exponentially from about the last half of the twentieth century and
in swimming major developments were seen from about the last quarter of the last
century. The integument of fast swimming marine vertebrates revealed a design
mechanism of crossed-fibers that are in many cases directly connected with high
speed. Among vertebrates besides snakes, the role of the integument in terrestrial
locomotion may not have the same mechanical implications in comparison with
marine vertebrates. However, many of the principles associated with the crossed-
fiber architecture in marine animals can be applied to the design structure of organ
systems in terrestrial vertebrates, e.g., in medicine the same mechanical principles
are involved to achieve stiffness and flexibility in blood vessels, the linea alba,
and the gut. In dinosaurs the crossed-fiber architecture is found in many parts of
the animal, for instance in a Psittacosaurus dinosaur the skin reinforces the ribs
by forming a Fink truss and in another part of the dinosaur over 20 layers of
oppositely oriented fibers reinforce the gut.
The role of the skin in flight in a number of modern-day and extinct gliders
is considered and discussed in the context of the latest research. Among these
gliders is the tree snake, Chrysopelea, which rather than being flattened as
previously thought, the latest research shows that it flattens the body during the
glide by special modified ribs. Pterosaurs were the first vertebrates to use the
integument as a membrane in true flapping flight. We look at these interesting
extinct animals through past and present research with respect to their giant size

vii
viii Preface

and flight potential, quadrupedal or bipedal launch, and perhaps most intriguingly
the structure of the flight membrane. Classic research on bat flight is described and
the book brings us up-to-date with the latest research that shows the complexities
of the wing beat cycle, significantly different from birds, as revealed by particle
image velocimetry.
The largest chapter in the book is occupied by birds and includes the most
­complex derivative of the integument to be found in any vertebrate animal, the
feather. The chapter starts with Archaeopteryx and some of the controversies asso-
ciated with it right up to the present and continues with over the past 50 years
or more seminal research into bird flight and ends with the material that made it
all possible, β-keratin and the most recent developments on the microstructure of
the feather and the associated biomechanics. Biomimetics may be mentioned only
briefly but there is no question that studies on structure and design at macro- to
nano-structural levels in birds and many of the other vertebrates mentioned in the
book will have a profound effect on the subject
In recent years it has been alleged that fine filamentous structures associated
with the preserved soft tissue of a number of dinosaurs in the Jehol biota and else-
where represent primal feathers, i.e., protofeathers. Chapter 6 takes a hard look at
these allegations through mainly published critiques.
The last chapter of the book is concerned with the highly polarized question of
the origin of birds and of the feather and the extent to which the freedom of the
press has been compromised in recent years, the latter shown to be of grave con-
cern by a number of prominent editors. This new absolutist censorship is encap-
sulated in public outbursts by scientists and editor such as, “[b]irds are dinosaurs.
The debate is over.” It is the climate created by such intolerance that has led to
some of the poorest and/or highly biased articles being accepted in ‘primetime’
journals of which numerous examples, all on record, are presented in the chapter.
Scientific values have given way to sensationalism and dogma and the harm that is
being done to evolutionary biology and the future of secular societies by some of
the leading journals in the world will impact for years to come.
It is hoped that the book will be useful to students at both undergraduate and
postgraduate levels. Perhaps, it may also help young scientists to reevaluate the
aims of science, which was beautifully expressed by an author writing an article
for a children’s magazine who wanted my view on the origin of birds, saying, “I
want this article to present both views and be as fair as possible. That’s why I need
your help.”
Acknowledgments

To the people I expressed my thanks to in Volume 1, I am equally indebted to

here. I have just a few names to add or re-mention here. They are Elizabeth Wager
(Sideview), Andrew Leitch (Nelson Mandela Metropolitan University (NMMU)),
Renzo Perissinotto (NMMU), Denise née Westenberg (NMMU), Anton Cloete
(NMMU), Achim G. Reisdorf (Universität Basel), and Michael Wuttke (GDKE).
My work has gained inspiration from the research of many workers over the years
but I should like to mention a few here for the indelible mark they have made
in various fields. For the evolution of birds and evolution per se, Walter Bock
(Columbia University), for functional studies on large swimming vertebrates, Ann
Pabst (University of North Carolina, Wilmington) and Philip Motta (University of
South Florida), for the flight of birds, Colin Pennycuick (University of Bristol), for
simply birds, Alan Feduccia (University of North Carolina, Chapel Hill) and for
vertebrate flight mechanics, Ulla M. Lindhe Norberg (Göteborg University). For
any errors there may be in interpretation of their studies or any others, the fault is
entirely my own.
To the many workers who generously responded with time and help in the use
of their valuable figures in the book I am enormously appreciative. Many of the
figures have been adapted in some small way and while I take the responsibility
for that, I gratefully acknowledge these authors in the respective figure descrip-
tions and add here that without them the book would have been the poorer for it.
For the many beautiful photographs on a number of bird species I owe special
thanks to Clint Ralph (https://www.facebook.com/pages/Clint-Ralph-Photography/
714373005250511?ref=hl) whose flair for bird photography produced just the pic-
tures I needed for a wide range of functions in different birds and environments.
For the excellent pictures on soaring seabirds my thanks are due to Lloyd Edwards
(www.raggycharters.co.za) (I owe him dinner and promise not to use the remains
of my lab dissections as requested).

ix
Contents

1 Swimming and Flying in Vertebrates . . . . . . . . . . . . . . . . . . . . . . . . . . . 1

1.1 Some Associated Physics. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
1.1.1 Forces Acting on Materials. . . . . . . . . . . . . . . . . . . . . . . . . . . 2
1.1.2 I-Beams (or H Beams). . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
1.1.3 Thin-Walled Cylinders. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9
1.2 Newton’s Three Laws of Motion. . . . . . . . . . . . . . . . . . . . . . . . . . . . 11
1.3 Fluid Mechanics. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13
1.3.1 Dimensionless Theorems. . . . . . . . . . . . . . . . . . . . . . . . . . . . 14
1.3.2 Dynamic Similarity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18
1.3.3 Fluid Responses. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19
1.4 Flight and Fluid Mechanics. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 25
1.4.1 The Aerofoil. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 27
1.4.2 The Bound Vortex. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 27
1.4.3 Drag . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 29
1.4.4 Angle of Attack . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 32
1.4.5 Wing Planform. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 33
1.5 Points of Debate. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 38
1.5.1 Bernoulli or Newton’s Laws for Lift? . . . . . . . . . . . . . . . . . . 38
1.5.2 Flying Upside-Down . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 39
1.5.3 Turbulence and Supercomputers . . . . . . . . . . . . . . . . . . . . . . 40
1.6 Aquatic Locomotion. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 43
1.6.1 Axial Undulatory Swimming (Anguilla). . . . . . . . . . . . . . . . 45
1.6.2 Axial Subundulatory to Axial Suboscillatory
Swimming (Most Fishes). . . . . . . . . . . . . . . . . . . . . . . . . . . . 47
1.6.3 Oscillatory Swimming (Thunniform). . . . . . . . . . . . . . . . . . . 50
1.7 Energy Saving Devices in Vertebrate Swimming. . . . . . . . . . . . . . . . 55
1.7.1 Reverse Von Karman Vortex Street . . . . . . . . . . . . . . . . . . . . 55
1.7.2 Diamond-Shaped Shoals . . . . . . . . . . . . . . . . . . . . . . . . . . . . 56
1.7.3 Porpoising. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 56
References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 58

xi
xii Contents

2 Vertebrate Swimming. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 61
2.1 The Deeper Dermis of Marine Vertebrates. . . . . . . . . . . . . . . . . . . . . 65
2.1.1 Non-thunniform Sharks. . . . . . . . . . . . . . . . . . . . . . . . . . . . . 65
2.1.2 Thunniform Swimmers . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 70
2.1.3 Anguilliform Swimmers. . . . . . . . . . . . . . . . . . . . . . . . . . . . . 99
References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 100

3 Vertebrates Make Their Flight Reservations. . . . . . . . . . . . . . . . . . . . . 105

3.1 Gliding: Economy Class Air Travel. . . . . . . . . . . . . . . . . . . . . . . . . . 105
3.1.1 Exploiting the Laws of Physics . . . . . . . . . . . . . . . . . . . . . . . 106
3.1.2 Evolution of Flapping Flight: Is a Transition
from Gliding Flight Possible? . . . . . . . . . . . . . . . . . . . . . . . . 127
References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 130

4 Flight by Membrane. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 131

4.1 The First True Fliers, Pterosaurs . . . . . . . . . . . . . . . . . . . . . . . . . . . . 131
4.1.1 The Pterosaur Wing . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 133
4.1.2 Huge Body Size and Flight in Pterosaurs. . . . . . . . . . . . . . . . 142
4.1.3 Pterosaur Feeding Behavior. . . . . . . . . . . . . . . . . . . . . . . . . . 147
4.2 Bats, the Only Mammalian True Fliers . . . . . . . . . . . . . . . . . . . . . . . 149
4.2.1 Wing Structure and Mechanics . . . . . . . . . . . . . . . . . . . . . . . 150
References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 159

5 Birds. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 163
5.1 Archaeopteryx, the First Bird or Urvogel. . . . . . . . . . . . . . . . . . . . . . 163
5.1.1 Ground-Up or Trees-Down Origin of Flight? . . . . . . . . . . . . 166
5.2 Feather Evolution. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 178
5.3 The Unique Flight Apparatus of Birds. . . . . . . . . . . . . . . . . . . . . . . . 182
5.3.1 Wing Structure. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 182
5.3.2 Flight Muscles . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 182
5.3.3 Flight Feathers. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 185
5.4 Flight Control Center. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 187
5.4.1 Bird Brains. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 189
5.5 The Phenomenon of Flapping Flight in Birds. . . . . . . . . . . . . . . . . . 192
5.5.1 Some Early Observations on Bird Flight. . . . . . . . . . . . . . . . 192
5.5.2 Understanding Flapping Flight. . . . . . . . . . . . . . . . . . . . . . . . 193
5.5.3 Departures and Arrivals. . . . . . . . . . . . . . . . . . . . . . . . . . . . . 199
5.6 The Power of Flight. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 199
5.6.1 The Power Curve. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 203
5.6.2 Wake Vortices. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 205
5.7 Behavior and Flight in Birds: Horses for Courses. . . . . . . . . . . . . . . 208
5.7.1 Wingbeat Kinematics in Slow-Flying . . . . . . . . . . . . . . . . . . 208
5.7.2 Going Nowhere Fast—Hovering. . . . . . . . . . . . . . . . . . . . . . 209
5.7.3 Silent Flight . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 218
Contents xiii

5.8 Offsetting the Costs of Bird Flight. . . . . . . . . . . . . . . . . . . . . . . . . . . 221

5.8.1 Bounding Flight. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 221
5.8.2 Soaring. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 221
5.8.3 Flying in Formation. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 237
5.9 How β-Keratin Crucially Influenced Bird Evolution. . . . . . . . . . . . . 239
5.9.1 Feather Structure at Angstrom and Molecular Levels. . . . . . 239
5.9.2 Feather Microstructure—Fibers and Foam . . . . . . . . . . . . . . 241
5.9.3 Feather Biomechanics at the Microstructural Level. . . . . . . . 247
References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 257

6 Integumental Taphonomy. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 263

6.1 Ichthyosaur Soft Tissue . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 263
6.2 Death of a Dolphin. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 266
6.3 The Dermis in Extant Reptiles. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 269
6.4 Sinosauropteryx, A Basal Theropod. . . . . . . . . . . . . . . . . . . . . . . . . . 271
6.5 Pushing Feathered Dinosaurs into the Mid-Triassic . . . . . . . . . . . . . 274
6.5.1 Beipiaosaurus. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 274
6.5.2 Psittacosaurus. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 277
6.6 Return to Sinosauropteryx. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 279
6.6.1 Rufous-Colored Dinosaur. . . . . . . . . . . . . . . . . . . . . . . . . . . . 279
6.6.2 Death by Volcano. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 284
6.7 One Day in the Life of Kulindadromeus Zabaikalicus. . . . . . . . . . . . 287
References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 292

7 The Last Best Hope. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 295

7.1 Freedom of Expression. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 295
7.2 Peer Review. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 296
7.3 The Birds are Dinosaurs Debate. . . . . . . . . . . . . . . . . . . . . . . . . . . . . 300
7.3.1 How Did We Sink so Low? . . . . . . . . . . . . . . . . . . . . . . . . . . 301
7.3.2 Science and the Falsifiability Criterion . . . . . . . . . . . . . . . . . 305
7.3.3 Birds are Dinosaurs and Cladistics. . . . . . . . . . . . . . . . . . . . . 310
7.3.4 “Prime Time” Journals: Does the Bite Match the Bark?. . . . 314
7.4 COPE’s Proposals on Fraud in Science. . . . . . . . . . . . . . . . . . . . . . . 315
7.4.1 Should the Status of the Institution or Individual Make
Fraud More Palatable?. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 315
7.5 National Geographic. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 322
7.6 Education and Freedom in Apartheid South Africa. . . . . . . . . . . . . . 324
7.7 The US Constitution’s First Amendment. . . . . . . . . . . . . . . . . . . . . . 328
References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 335

Index. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 339
Chapter 1
Swimming and Flying in Vertebrates

Natural selection over millions of years has ensured that the mechanical systems
evolved in swimming and flying vertebrates are highly efficient with regard to the
habitat and mode of life for each species.
In living animals the body size and shape (morphology), the manner of move-
ment (locomotion), the way of life (ecology), and the environmental conditions
(habitat) are all strongly related to one another and to survival. Locomotion stems
from four categories of survival: (1) to perpetuate the species such as for mating,
breeding, nursing, and dispersing; (2) for obtaining food, e.g., searching, prey-
ing, and homing; (3) for escaping from enemies/predators; and (4) for migrating,
which affects all the other categories but also economizes on energy consumption
(Azuma 2006) (Fig. 1.1).
Mechanics, from physics and engineering, and its application to biological sys-
tems as biomechanics and biophysics has seen increasing importance in the past
50 or more years. Conversely, in more recent years we have seen that an increas-
ing understanding of biomechanical structures and materials in plants and animals
is contributing to complex bioinspired materials and designs leading to major
technological applications at all levels from macro- to nanostructures (Meyers
et al. 2013). In the first section of this chapter some background physics are intro-
duced, which provide the framework in which analyses of fluids are conducted
from the standpoint of classical fluid mechanics. In some instances, the mathemat-
ics is complicated, particularly when the flow field involves highly chaotic sys-
tems and large Reynolds numbers (increasingly aided today by supercomputers).
Notwithstanding, analytical theories and calculations have provided some insight
into the subject and give us an estimation of aero- and hydrodynamic characteris-
tics involved in flying and swimming.

© Springer-Verlag Berlin Heidelberg 2015 1

T. Lingham-Soliar, The Vertebrate Integument Volume 2,
DOI 10.1007/978-3-662-46005-4_1
2 1  Swimming and Flying in Vertebrates

1.1 Some Associated Physics

Many terms, e.g., strong or weak, to describe a material may be adequate for everyday
conversation, but in mechanics there is frequently a need for more precise defini-
tions. Some, relevant to the following discussions are taken from Lingham-Soliar
(2014b), to which others are added.

1.1.1 Forces Acting on Materials

Two terms that are frequently confused in common use are stress and strain.
Stress, numerically, in any direction at a given point in a material is simply the
force or load that happens to be acting in that direction at the point, divided by the
area on which the force acts. If the force at a certain point is s, then
load F
Stress = s = =
area A
Strictly then, how strong a material is, is the stress required to break a piece of
the material (e.g., MN/m2, i.e., mega-newtons per square meter). Strain involves
deformation, i.e., when a stress s is applied to a material such as a metal, the mate-
rial experiences a change in dimension, volume, or shape (Fig. 1.2). Put in another
way, strain tells us how far the atoms at any point in a solid are being pulled apart,

Fig. 1.1  Strong ties among habitat, ecology, morphology, and locomotion. Modified after
Azuma (2006)
1.1  Some Associated Physics 3

Fig. 1.2  Stress. Metal bar

under tension increases in
length and decreases in cross
section. F = Force, A = Area,
L = Length. Redrawn after
Lingham-Soliar (2014b)

i.e., by what proportion the bonds between atoms are being stretched, in contrast
to stress that tells us how hard—that is, with how much force—the atoms at any
point in a solid are being pulled apart (Gordon 1978). Strain has no units because
it is a ratio of two lengths
increase of length Ln − L o
Strain = =
original length Lo
Elastic deformation involves various constants that relate the magnitude of
the strain in response to the applied stress. These elastic constants include the
following:
(1) Stiffness of a material, i.e., the modulus of elasticity or Young’s modulus
(E) is the ratio of the applied stress to a body over the strain. Young’s modulus is
a measure of the ability of a material to withstand changes in length when under
lengthwise tension or compression. If a metal bar of cross-sectional area A is
pulled by a force F at each end, the bar stretches from its original length Lo to a
new length Ln. (Simultaneously the cross section decreases.) The stress is the quo-
tient of the tensile force divided by the cross-sectional area, or F/A (above). The
units in the English system are pounds per square inch, usually abbreviated psi and
in the metric system newtons per square meter (N/m2). Thus, Young’s modulus or
E may be expressed mathematically as
stress F/A
Young’s modulus = =
strain Ln − Lo /Lo
(2) Shear modulus (µ) is the ratio of the applied stress to the distortion (rotation) of
a plane originally perpendicular to the applied shear stress; it is also termed the modu-
lus of rigidity. It is the numerical constant that describes the elastic properties of a solid
under the application of transverse internal forces such as arise, for example, in tor-
sion, as in twisting a metal pipe about its lengthwise axis. Within such a material, any
small cubic volume is slightly distorted in such a way that two of its faces slide paral-
lel to each other a small distance and two other faces change from squares to diamond
shapes. The shear modulus is a measure of the ability of a material to resist transverse
deformations and is a valid index of elastic behavior only for small deformations, after
which the material is able to return to its original configuration (Fig. 1.3).
(3) Poisson’s ratio (σp). The ratio of the transverse strain to the longitudinal
strain is called Poisson’s ratio. When, e.g., a metal bar under tension is elongated,
its width is slightly diminished. This lateral shrinkage constitutes a transverse strain
that is equal to the change in the width divided by the original width. The average
4 1  Swimming and Flying in Vertebrates

Fig. 1.3  Shear stress. Top, shows wire under tension. Bottom, shows metal tube under tension
(acting at about ±45°). In the metal tube, the right angle CAF in the unstrained tube decreases to
the acute angle BAF when the tube is twisted. The change in the right angle is, therefore, equal
to angle BAC the tangent of which, by definition, is the ratio of BC divided by AC (shear strain).
Redrawn after Douglas (1963) and Lingham-Soliar (2014b)

Fig. 1.4  Work of fracture in some materials. After Gordon (1978)

value of Poisson’s ratio for steels is 0.28, and for aluminum alloys, 0.33. The vol-
ume of materials that have Poisson’s ratios less than 0.50, increase under longitudi-
nal tension and decrease under longitudinal compression.
(4) Fracture. Work, e.g., work of fracture, in physics means the transfer of
energy, i.e., a mechanism for the transfer of strain energy to fracture energy. This
idea to the whole problem of fracture by way of energy rather than force and stress
was new and developed by A.A. Griffiths, after whom this form of crack propaga-
tion is named, the Griffiths fracture. Fracture quite specifically requires that new
surfaces shall be created, which requires energy (work); hence, fracture is the pro-
cess of balancing the energy within the material (Fig. 1.4). Here we concern our-
selves with just one form of energy, strain energy, and also for simplicity consider
1.1  Some Associated Physics 5

Fig. 1.5  Work of fracture. a Clamped material is cracked. Dotted areas relax and give up strain
energy, which is now available to propagate the crack further. b Graph showing Griffith energy release
or why things go pop. OA represents the increased energy requirement as the crack extends, and it is
a straight line. OB represents the energy released as the crack propagates, and it is a parabola. The
net energy balance is the sum of these two effects and is represented by OC. Lg is the critical crack
length and ZX is the negative amount of energy required to get the crack going (the margin of safety
or threshold energy, the “true factor of safety”). Modified from Gordon (1978)

just uniaxial stressing (Wainwright et al. 1976). The quantity of energy required to
break a given cross-section of material defines its “toughness,” technically called
its “fracture energy” or “work of fracture.” This property is quite different to and
separate from the “tensile strength” of the material, which is defined as the stress
(not the energy) needed to break the solid (Gordon 1978).
Sudden failure begins at a notch or crack that locally concentrates the stress, and
the energy required to extend such a crack in a solid is a measure of the solid’s tough-
ness (Fig. 1.5a). In a hard, brittle material, toughness is low, while in a “soft,” ductile
material, e.g., some metals or many biological materials (e.g., collagen), the “work of
fracture” is enormously higher (Wainwright et al. 1976; Gordon 1978) (Fig. 1.4).
Work of fracture is measured as the product of the force applied to a body and
the distance moved by that body in the direction of the force. For example, work
of fracture is the transfer of energy from one object to another, especially in order
to make the second object move in a certain direction. Work (W) is equal to the
amount of force (F) multiplied by the distance over which it is applied (s)
W = Fs.
For example, if a force of 10 newtons is applied over a distance of 3 m, the work
is equal to 30 N/m, or 30 J. The unit for measuring work is the same as that for
energy in any system of units, since work is simply a transfer of energy.
6 1  Swimming and Flying in Vertebrates

The quantity of energy needed to break most kinds of chemical bonds is well
known in chemistry and in most of the structural solids we are concerned with in
technology. The total energy required to break all the bonds in any one plane or
cross-section is much the same particularly when we are dealing with a range of
materials called “brittle solids,” stone, brick, glass, and pottery (which accounts
for the effects of bulls in china shops) (Figs. 1.4 and 1.5). On the other hand the
technical and biological materials that are used in tension, usually safely, all
require a great deal more energy in order to produce a fracture. In other words,
the work of fracture is high and in many cases the material is ductile. Remarkably,
biological materials seem to have developed methods of achieving high works of
fracture that are very “cunning” indeed (Gordon 1978) (Fig. 1.4).
One way in which crack-stopping works in materials such as soft metals
is because they are ductile (able to be shaped or molded without breaking). For
instance, the “dislocation mechanism,” i.e., by sliding of atoms over each other,
it enables the material to get rid of much of the crack-generating energy (Gordon
1978; Wainwright et al. 1976, and references therein). It is also true that in a tough
material the fine structure of the material is disturbed to a much greater depth and
relative to the small percentage of broken bonds (see below), the energy needed
to produce a new surface may be increased a millionfold. Soft materials are also
prone to be pulled out in tension a great deal before a crack appears (Fig. 1.5).
According to the Griffith principle, the strain energy needed to diminish the stress
needs to be obtained from internal resources. As a crack appears in a material it will
gape under the stress and the material immediately surrounding the crack will become
relaxed and give up strain energy (Fig. 1.5b). Roughly speaking, two triangular areas
shaded in the diagram in Fig. 1.6—will give up strain energy—whatever the length, L,
of the crack these triangles will keep roughly the same proportions, and so their areas
will increase as the square of the crack length, i.e., as L2. Thus the strain energy release
will increase as L2. This is the core of the Griffith principle, that while the energy debt
of the crack increases only as L, its energy credit increases as L2; in other words, the
energy needed to produce a new surface is significantly increased (Fig. 1.5b).
In Fig. 1.5b, up to point X the whole system consumes energy; beyond point
X energy begins to be released. It follows that there is a critical crack length we
might refer to as Lg, which is called the “critical Griffith crack length.” Cracks
shorter than this are safe and stable and will not normally extend; cracks longer

Fig. 1.6  Work of fracture. The work of fracture is proportional to the volume of material plasti-
cally distorted, i.e., to the shaded area, and thus is roughly as t2. Hence the work of fracture of a
thin sheet may be very low. Redrawn after Gordon (1978)
1.1  Some Associated Physics 7

than Lg are dangerous and spread faster and faster through the material. Thus most
cracks are safe providing they do not reach a critical point (Gordon 1978).
We have dealt with fracture mechanics in some detail because of its impor-
tance and because even experienced people get it wrong when applied to biology.
I was recently told by a reviewer of one of my papers on feather microstructure
that “longitudinal creasing and splitting” in the feather rachis “is relatively easy,”
recommending Gordon (1978) in support of his view. However, Gordon (1978,
p. 131) said quite the opposite, i.e., “feathers probably do not need to be especially
strong, but they do need to be stiff and at the same time resilient and to have a high
work of fracture” which intuitively made sense to him despite as he said “the work
of fracture mechanism of feathers is something of a mystery; at the time of writing
I do not think anybody knows how it works.” We will see in Chap. 5 from the latest
microstructural studies on the feather (Lingham-Soliar et al. 2010; Lingham-Soliar
and Murugan 2013) how Gordon had hit the nail precisely on the head, as he so
often did, despite us having to wait over 30 years for the proof.
In this section, two structures are chosen because of their common occurrence
in both engineering systems and in the natural world, the I- or H-beam and the
thin-walled hollow cylinder.

1.1.2 I-Beams (or H Beams)

The development of beam theory in the mid-1700s by Euler, who generally mod-
eled beams as elastic lines that resist bending, e.g., buckling under compressive
loading, remains among the most immediately useful aspects of solid mechanics,
in part for its simplicity and in part because of the pervasiveness of beams and col-
umns in structural technology and nature (Fig. 1.7).
In the 1930s, my grandmother was an important property-developer in Port
Elizabeth, South Africa. At one point, she had employed some of the best archi-
tects to design modern residential apartment blocks that included business

Fig. 1.7  I-beams (or H
beams). I-beam (here, a
cantilever) in which most
material is concentrated in
the upper (tension) and lower
(compression) surfaces to
resist maximum stresses–with
the ‘‘web’’ in the middle to
resist shearing forces at ~45°.
The figure shows clearly why
it is called an “I” beam. From
Lingham-Soliar and Murugan
(2013) Plos one open access
8 1  Swimming and Flying in Vertebrates

Fig. 1.8  Cantilever. Nascent or simple triangular arrangement (dark gray). W, is directly kept

from falling down by the action of the upward component of tension in the slanting (45°) mem-
ber 1. As more panels are added, more slanting members are added to take the shear, i.e., by a
multiple lattice or by a continuous plate. Modified after Gordon (1978)

premises on the ground floor, the front overhung by the latest fixed cantilever roof
(pillar-less) giving maximum space beneath for shoppers. There is the occasion,
which my mother recounted to me, when my grandmother drove past one such
new property and almost had seven fits. New tenants occupying a first floor flat (a
large Afrikaner family of particularly large individuals), were sprawled over the
cantilever roof near its tip, sunbathing and watching the world go by. My grand-
mother was not an engineer but common sense warned her of the added stresses
placed on the cantilevered roof, supported solely by the wall. She did not suffer
fools gladly and her short instruction to her chauffeur involved the quickest route
to her lawyers. Knowledge of engineering principles tells us her fears were justi-
fied given that in cantilever beams the highest tension and compression forces are
close to its fixed end where the greatest danger of fracture exists. The horizontal
struts cannot sustain the weights directly but transfer the stresses horizontally to
the vertical retaining wall. All other stresses in a cantilever beam occur as down-
ward shearing forces directed at ±45° to the long axis (Fig. 1.8).
Consequently, one additional way of supporting the downward load or “shear-
ing force” is by reinforcing the structure with diagonal members oriented at 45° to
the long axis (Gordon 1978). If, however, the cantilever is made very long then the
horizontal and longitudinal tension and compression forces and stresses close to
the fixed end may be very high. Coping with these added stresses would be to add
more and more oppositely oriented slanting (45°) members (Figs. 1.7 and 1.8).
In the following equation, a nonuniformly distributed load (Fig. 1.9) is shown
as a point load W at the end of the beam:
Point load W at end. Condition at distance x from end of beam
M = Wx Max M = WL at B

1W  3 
Deflection at x is y = x − 3L 2 x + 2L 3
6 EI
1 WL 3
Max deflection ymax = at A
3 EI
1.1  Some Associated Physics 9

Fig. 1.9  Cantilever.
Nonuniformly distributed
load. All materials and
structures deflect, to greatly
varying extents, when they
are loaded. a A cantilever
in nature. The material
of the bough is stretched
near its upper surface and
compressed or contracted
near its lower surface by the
weight of the monkey (wood
may be reinforced by layers
of fibers at ±45° to the long
axis, acting as a truss (see
inset, after Gibson 2012)).
b Point load W at end.
Condition of X from end of
the beam (equation in text).
Modified after Gordon (1978)

Note, the cantilever does not have to be horizontal but can in effect be vertical,
with the deflection acting horizontally as, e.g., wind against trees or tower blocks
(a tree must respond to both vertical and horizontal stresses). In Fig. 1.9a, the tree
branch is horizontal and downward shearing forces directed at ±45° to the long
axis with the branch cross-fibers aligned in approximately the same direction. In
the vertical trunk, the cross-fibers would change direction (see Gibson 2012).
From a biological perspective, the cantilever is very important. For instance,
it is commonly seen in the trunk and rib-cages of most vertebrates, which can be
considered as a sort of simply supported beam. A more obvious example of the
cantilever beam is the attachment of a horses’ head and neck to the body and a
similar arrangement in ostriches (Fig. 1.10), requiring a complex web of ligaments
angled at about 45° to the long axis that braces the horizontal forces against the
body. In Chap. 5, we will also see from recent studies that the cantilever system is
fundamental to the structure and mechanics of the feather.

1.1.3 Thin-Walled Cylinders

Thin-walled cylinders acting as support structures are found widely in engineering

systems as well as in diverse biological structures (Lingham-Soliar 2005b).
In mechanical engineering, as a structure that is subjected to direct loading, a
thin-walled cylinder is defined by the thickness, t, of the cylinder wall which is
10 1  Swimming and Flying in Vertebrates

Fig. 1.10  Many vertebrates form a sort of Fink truss with muscles and tendons making a rather
complicated diagonal shear bracing between the ribs. The nuchal ligaments (among others) of the
neck and shoulder, e.g., in horses and ostriches (silhouette), perform the same function

small in relation to the cylinder radius, r (generally if its radius r is larger than 5
times its wall thickness t (r > 5 × t)). In pressure cylinders, e.g., the loading on a
thin cylinder is due to the internal pressure, P, of the fluid contained within the
cylinder. The pressure, P, inside a cylinder causes two types of stress to develop
as a consequence of pressure along the cylinder and pressure around its circum-
ference (Fig. 1.11), which are different. If we call the stress along the cylinder S1
and that around the circumference S2, we see that the stress along the shell S1 is
equivalent to all the resultants of all the pressure forces on the inside curved sur-
face of a cylinder,
S(stress) = load/area πr2p/2πrt = rp/2t
Hence, stress along the length of a cylinder:
rp
s1 =
2t
To obtain S2, the circumferential stress in the shell of the cylinder, the cylinder is
viewed in the other plane (Fig. 1.11):
rp
s2 =
t
where s = stress, t = thickness, p = pressure, r = radius.
1.1  Some Associated Physics 11

Fig. 1.11  A thin-walled
cylinder. Slice in the cylinder
shows circumferential stress
(σc) which is twice the
longitudinal stress. Double-
headed arrow long axis of
cylinder. Modified after
Lingham-Soliar (2014b),
courtesy of Springer

This leads to an important definition: the circumferential stress in the wall of

a pressure vessel is twice the longitudinal stress, i.e., S2 = 2S1 (Wainwright et al.
1976; Gordon 1978).
Thus, the hoop or circumferential stress is twice as much as the longitudinal
stress. Hence, a cylinder of homogeneous material under pressure would fail by
splitting longitudinally (as Gordon aptly compared, when sausages swell during
frying they split along their length) and can be reinforced by fibers crossing at 45°
to the long axis, as we saw above.
The same principles of reinforcing a cylinder or beam by diagonally oriented
cross-fibers are applied to diverse biological systems; for instance, many more or
less cylindrical animals have their skin or cuticle reinforced by crossed-helical fib-
ers (Clark and Cowey 1958) and we will see how the principle is applied to vari-
ous integumental systems in Chaps. 2 and 5. The feather rachis may be considered
a thin-walled cylinder and in Chap. 5 we will see how some workers tried to use
the principle to propose Archaeopteryx was incapable of flapping flight.

1.2 Newton’s Three Laws of Motion

Perhaps apocryphal, but known to many school children is the story of Sir Isaac
Newton’s observation of an apple falling to the ground and remarkably, his con-
necting the force drawing the apple to the ground with that keeping the moon
in its orbit. Newton’s synthesis of the laws of motion famously united the heav-
ens and earth. Interestingly, his inspiration came from the natural sciences as we
glimpse in the title of Newton’s (1687) work the Philosophiae Naturalis Principia
Mathematica (Mathematical Principles of Natural Philosophy), one of the most
12 1  Swimming and Flying in Vertebrates

Fig. 1.12  Isaac Newton put forward the law of gravitation in 1687 and used it to explain the
observed motions of the planets and their moons. Inset is Newton’s own telescope with which he
observed planetary motions

important single works in the history of modern science, which was fired by his
mathematical imagination (Feingold 2004). Newton assumed the validity of the
principle of inertia which he formulated in the Principia as the first law of motion.
He introduced two fundamental concepts: that the main attractive gravitational
force acting on a planet is a central force directed toward the sun, and that the
magnitude of this force is proportional to the planet’s acceleration (Fig. 1.12). As a
consequence, Newton concluded that his laws of motion universally allow that all
bodies whatsoever are endowed with a principle of mutual gravitation—which can
be applied to problems such as in fluid dynamics.
Newton’s first law states that, if a body is at rest or moving at a constant speed
in a straight line, it will remain at rest or keep moving in a straight line at constant
speed unless it is acted upon by a force. This postulate is known as the law of iner-
tia, and it is basically a description of one of the properties of a force: its ability to
change rest into motion or motion into rest or one kind of motion into another kind.
Newton’s second law is regarded as the most important of the three. It is a
quantitative description of the changes that a force can produce in the motion of
a body. It states that the time rate of change of the velocity (directed speed), or

Fig. 1.13  Comparison of
deformation of solids and
liquids under application
of a shear stress. a Solid.
b Liquid. Permission
McDonough (2009, online),
physics lecture notes
1.2  Newton’s Three Laws of Motion 13

acceleration, α, is directly proportional to the force F and inversely proportional to

the mass m of the body; i.e., α = F/m or written in the iconic form as
F = ma
The larger the force, the larger the acceleration (rate of change of velocity); the larger
the mass, the smaller the acceleration. Both force and acceleration have direction
as well as magnitude and are represented in calculations by vectors (arrows) hav-
ing lengths proportional to their magnitudes. The acceleration produced by a force is
in the same direction as the force; if several forces act on a body, it is their resultant
(sum) obtained by adding the vectors tail-to-tip that produces the acceleration.
From Newton’s second law, all of the basic equations of dynamics can be
derived (McDonough 2009) by procedures developed in the calculus (branch
of mathematical analysis) of which there has been some debate whether Isaac
Newton had priority of its discovery or Gottfried Wilhelm Leibniz of Germany
(both men are now credited). A simple case is a freely falling body. Neglecting air
resistance, the only force acting on the body is its weight acting down, and it pro-
duces a downward acceleration equal to the acceleration of gravity, g. We will see
further on the significance of Newton’s second law in fluid dynamics.
Newton’s third law states that the actions of two bodies upon each other are
always equal and directly opposite; i.e., reaction is always equal and opposite to
action. The proposition seems obvious for two bodies in direct contact; the down-
ward force of a book on a table is equal to the upward force of the table on the
book. It is also true for gravitational forces, e.g., a flying aeroplane pulls up on the
Earth with the same force that the Earth pulls down on the aeroplane. The third
law is important in forces that act on bodies at rest (static). It permits the separa-
tion of complex structures and machines into simple units that can be analyzed
individually with the least number of unknown forces.

1.3 Fluid Mechanics

Fluid mechanics deals with the study of all fluids under static and dynamic situa-
tions. It is a branch of continuous mechanics which deals with a relationship between
forces, motions, and statical conditions (resisting energy) in a continuous mate-
rial. This study deals with flow round bodies (solid or otherwise), flow stability, etc.
Almost any action a person is doing involves some kind of a fluid mechanics problem.
Two definitions are better placed here than in the preceding section. First, what
is a fluid? A fluid is any substance that deforms continuously when subjected to a
shear stress, no matter how small (McDonough 2009) (Fig. 1.13). This is not seen
in a number of common substances that appear to “flow,” for example, various
household granular cooking ingredients such as sugar, salt, flour, many spices, etc.
Clearly, any of these can be “poured,” but their response to shear stress is very dif-
ferent from that of a fluid—all you get, e.g., with sugar is a pile, induced by grav-
ity, having a nearly conical shape—it lies there but there is no deformation—sugar
is not a fluid. By way of contrast, a cup of coffee spilled onto a table, the coffee
14 1  Swimming and Flying in Vertebrates

will spread across the surface of the table, and it is clear it cannot pile up–the shear
stresses induced by gravitational forces cannot be supported, and deformation
occurs—coffee is a fluid. Nevertheless, authors such as Bar-Meir (2013) believe
the boundary between some solids and fluids is a gray area and consequently fluid
mechanics involves many fields that have no clear boundaries between them. For
example, materials like sand (e.g., quick sand) with grains should be treated as liq-
uids and even material such as aluminum just below the mushy zone also behaves
as a liquid similar to butter, while yet other materials behave as a liquid solid mul-
tiphase flow. These special distinctions, however, need not concern us here.
Our second definition is viscosity. In plain terms it is a fluid’s thickness or sticki-
ness. In physics, viscosity is that fluid property by virtue of which a fluid offers
resistance to shear stresses. At first glance this may seem to conflict with the earlier
definition of a fluid (a substance that cannot resist deformation due to shear stresses),
but resistance to shear stress, per se, simply implies that the rate of deformation may
be limited—it does not mean that there is no deformation. In particular, we intuitively
expect that water would deform more readily than honey if both were subjected to
the same shear stress under similar physical conditions, especially temperature.
Furthermore, our intuition would dictate that water and air would likely have
relatively low viscosities while molasses and tar would possess rather large vis-
cosity—at least if all were at standard temperature. Observations of this sort can
be more precisely formulated by Newton’s law of viscosity—for a given rate of
angular deformation of a fluid, shear stress is directly proportional to viscosity.
Newton’s law of viscosity may at first seem somewhat convoluted but it is not cru-
cial for the present discussion (McDonough 2009).
On molecular scales, viscosity arises due to two main physical effects: intermo-
lecular cohesion and transfer of molecular momentum. It should be expected that
the former would be important (often dominant) in most liquids for which mole-
cules are relatively densely packed, and the latter would be more important in gases
in which the molecules are fairly far apart, but moving at high speed. These obser-
vations are useful in explaining the facts that the viscosity of a liquid decreases as
temperature increases, while that of a gas increases with increasing temperature.
Fluid mechanics deals with the study of all fluids under static and dynamic situa-
tions and includes many diverse problems such as surface tension, fluid statics, flow in
enclosed bodies, or flow round bodies (solid or otherwise), flow stability, etc. In fact,
almost any action a person is doing involves some kind of a fluid mechanics problem.

1.3.1 Dimensionless Theorems

An animal’s speed is dependent on environmental conditions, manner of locomo-

tion, and body shape. Air, of course, is less viscous (thick and sticky) than water
and for most vertebrates presents less of a problem in passing through it than that
presented by the aquatic medium. However, the energy cost or cost of transport
for a unit mass travelling a unit distance is higher for land animals than for swim-
ming and flying animals (because of assistance gained from air and water; below).
1.3  Fluid Mechanics 15

Nevertheless, whether in water or in air for animals to achieve high speeds, certain
modifications of body structures and surfaces are necessary. This is most effec-
tively demonstrated in engineered systems such as in fast cars and airplanes in
which smooth surfaces and tapered structures are an important part of the design
(we will look at design in engineering and in nature further on). We will consider
some of the principles involved in locomotion in the aquatic medium, in which
because of its higher viscosity than air some of the problems of passing through
it are more apparent but nevertheless apply also to locomotion on land and in air.
Among the early workers who were laying the foundations of hydrodynamics
were Euler and Bernoulli. Because of its importance in fluid dynamics, Bernoulli’s
equations are dealt with in some detail below. Before that, we will look at an
important dimensionless theorem known as the Reynolds number (see Fig. 1.14).

1.3.1.1 Reynolds Number (Re No)

The Reynolds number (frequently shortened to Re No) is undoubtedly the most

famous dimensionless parameter in fluid mechanics which can be used as a crite-
rion to distinguish between laminar and turbulent flow. Re No is the ratio of inertial
forces to viscous forces, i.e., it is a measure of the relative importance of viscosity

Fig. 1.14  Table of some important dimensionless theorems in fluid motions. Permission Bar-

Meir (2013)
16 1  Swimming and Flying in Vertebrates

versus inertia. We will also encounter some other dimensionless quantities used in
fluid mechanics later, which are summarized (Fig. 1.14). In fluid mechanics, the Re
No represents a criterion of whether fluid (liquid or gas) flow is absolutely steady
(streamlined, or laminar) or with small unsteady fluctuations (turbulent), as
ρua/η
here ρ and η are the density and viscosity of the fluid and u is its velocity relative
to the body and a is a length.
If the Re No of a fluid flow is small, viscous forces (friction) are larger than inertial
forces in the flow. Re No range from 10 for the smallest flying insects to greater than 107
for large, high-speed aircraft. Reynolds numbers for birds usually range from 103 for
passerines to 105 for larger birds such as Frigate birds. At Re No 0–0.1 viscous drag
is particularly important while at Re No above 1, pressure drag is more important (see
below). Size and speed affect the Re No, e.g., small animals move relatively slowly
and have low Re No while large animals move fast and have high Reynolds number.
If the Re No is infinite, the flow becomes an ideal fluid flow (with zero viscosity).
Flows about bodies that are geometrically similar (and similar in roughness) are com-
pletely the same if their Reynolds numbers are the same (see dynamic similarity,
below). Fluids flowing through tubes flow faster at its center than near the wall and the
mean velocity is used as u. Researchers distinguish between orderly flow and chaotic
flow as laminar and turbulent (Fig. 1.15). Whenever the Reynolds number is less than
about 2,000, flow in a pipe is generally laminar, whereas at values greater than 2,000,
flow is usually turbulent. Actually, the transition between laminar and turbulent flow
occurs not at a specific value of the Reynolds number but in a range usually begin-
ning between 1,000 and 2,000 and extending upward to between 3,000 and 5,000. We
will see how the Re No can be applied to laboratory experiments in the next section on
dynamic similarity and application in the rest of the chapter and in succeeding chapters.
There are a number of other dimensional parameters in fluid mechanics, which
will be mentioned briefly here. One dimensionless quantity frequently, connected
with the Re No and used to indicate the influence of gravity on fluid motion, is the
Froude number.

Fig. 1.15  Laminar and turbulent flow of water from a faucet (tap). a Steady laminar. b Periodic
wavy laminar. c Turbulent. Permission from McDonough (2009, online), physics lecture notes
1.3  Fluid Mechanics 17

1.3.1.2 The Froude Number (Fr)

The Froude number is defined as the ratio of a characteristic velocity to a gravita-

tional wave velocity. It may equivalently be defined as the ratio of a body’s inertia
to gravitational forces. In fluid mechanics, the Froude number is used to determine
the resistance of a partially submerged object moving through water, and permits
the comparison of objects of different sizes. Named after William Froude, the
Froude number is based on the speed–length ratio as defined by him. The greater
the Froude number, the greater the resistance. It is generally expressed as

F = v (gd)−1/ 2

in which d is depth of flow, g is the gravitational acceleration (equal to the specific

weight of the water divided by its density, in fluid mechanics), v is the celerity of
a small surface (or gravity) wave, and F is the Froude number. When F is less than
1, small surface waves can move upstream; when F is greater than 1, they will
be carried downstream; and when F = 1 (said to be the critical Froude number),
the velocity of flow is just equal to the velocity of surface waves. It means that
movements that are affected by gravity cannot be dynamically similar unless their
Froude numbers are equal and is the basis for testing models against the full-sized
equivalent. The Froude number enters into formulations of the hydraulic jump
(rise in water surface elevation) that occurs under certain conditions, and, together
with the Reynolds number, it serves to delineate the boundary between laminar
and turbulent flow conditions in open channels (Bar-Meir 2013) (Fig. 1.14).

1.3.1.3 The Prandtl Number (Pr)

The Prandtl number is a dimensionless number; the ratio of momentum diffusivity

(kinematic viscosity) to thermal diffusivity. It is named after the German physicist
Ludwig Prandtl. It is defined as
v viscous diffusion rate cp µ
Pr = = =
α thermal diffusion rate k
where
v  = kinematic viscosity, v = µ ρ, α  = thermal diffusivity, α = k ρcp ,
  

µ = dynamic viscosity k = thermal conductivity, Cp = specific heat, P = density.

The Prandtl number is often used in heat transfer and free and forced convec-
tion calculations. It depends on the fluid properties.

1.3.1.4 The Strouhal Number (St)

The Strouhal number (St) is a dimensionless number describing oscillating flow

mechanisms. The parameter is named after Vincenc Strouhal, a Czech physicist who
18 1  Swimming and Flying in Vertebrates

experimented in 1878 with wires experiencing vortex shedding and singing in the
wind. The Strouhal number is an integral part of the fundamentals of fluid mechanics.
The Strouhal number is often given as
fL
St = ,
V
where f is the frequency of vortex shedding, L is the characteristic length (for
example hydraulic diameter, or chord length) and V is the velocity of the fluid. In
certain cases like heaving (plunging) flight, this characteristic length is the ampli-
tude of oscillation. This selection of characteristic length can be used to present a
distinction between Strouhal number and Reduced Frequency.
ka
St = ,
πc
where k is the reduced frequency and a is amplitude of the heaving oscillation.
The Strouhal number can be important when analyzing unsteady, oscillating
flow problems as, e.g., vortex wakes, which will be discussed later in this chapter
and in Chap. 5. It represents a measure of the ratio of inertial forces due to the
unsteadiness of the flow or local acceleration to the inertial forces due to changes
in velocity from one point to another in the flow field. In animal flight or swim-
ming, propulsive efficiency is high over a narrow range of Strouhal constants, gen-
erally peaking in the 0.2 < St < 0.4 range. This range is used in the swimming of
dolphins, sharks, and bony fish, and in the cruising flight of birds, bats and insects
(below). These and some other dimensionless numbers can be found in Fig. 1.14.

1.3.2 Dynamic Similarity

Because of the great diversity in their body shape and size, animals have devel-
oped a variety of forms of locomotion, many converging despite phylogenetic dif-
ferences, which will be discussed more in later chapters. However, to understand
fundamental modes of locomotion and characteristics, body shapes and locomo-
tion can be organized into a convenient framework for analysis, through accu-
rate and systematic descriptions of the dynamics related to locomotion (Azuma
2006). A much smaller model can be tested provided the objects are geometri-
cally similar and the flows around them are dynamically similar. We saw above
the nondimensional parameters, e.g., Reynolds numbers that are used for describ-
ing the motions of animals and of the surrounding medium which is frequently
linked to the Froude number. This can be utilized in understanding the dynamic
similarity in animals as well as how it can be used in the laboratory study of ani-
mals (and machines). This similitude law forms the basis of wind tunnel testing
(see Chap. 5). For instance, forces acting on an aircraft can be obtained by testing
a small-scale model of that aircraft in a wind tunnel. A suitable combination of
density and velocity can be used to obtain the same Re No for the model as for the
1.3  Fluid Mechanics 19

Fig. 1.16  Dynamic
similarity. The bird on the left
can be considered identical in
shape to the one on the right.
We also assume that no body
forces are significant. The
only dimensionless parameter
required to completely set the
flow behavior is the Reynolds
number

full size aircraft. This enables the flow characteristics and force coefficients for the
model to be the same as for the actual aircraft (McDonough 2009) (Fig. 1.16).

1.3.3 Fluid Responses

We discuss the response of fluids to forces exerted upon them as a branch of classical
physics, armed with some of the basic knowledge presented above. We will see that the
applications of fluid mechanics are of great importance in engineering and in biology.

1.3.3.1 Bernoulli Equation

Euler and Bernoulli treated the fluid as an idealized inviscid substance in which,
as in a fluid at rest in equilibrium, the shear stresses associated with viscosity are
zero and the pressure p (static) is isotropic (physical properties that do not vary
with direction). They arrived at a simple law relating the variation of p along a
streamline to the variation of v (the principle is credited to Bernoulli, but Euler
seems to have arrived at it first), which serves to explain many of the phenomena
that real fluids in steady motion display.
Note, Bernoulli’s equation only holds for inviscid, steady, and incompressible
flow along a streamline and the velocity at any point in space is constant. This
calculation can give some perspective on the energy involved in fluid flow, but its
accuracy is always suspect because of the assumption of laminar flow. The simplest
step will be to neglect the second-order terms of the full equation, which from a
physical point of view represents the viscosity effects. It can be calculated as
1 2
ρv + ρgh + P = constant
2
where ρ is the density of the fluid, v is its velocity, h its height, P its pressure and g
the gravitational acceleration.
20 1  Swimming and Flying in Vertebrates

Fig. 1.17  Bernoulli pressure
venturi. In the wider diameter
section the fluid is moving
slowly under high pressure.
As the tube constricts the
pressure lowers and the fluid
moves faster

The Bernoulli Equation can be considered to be a statement of Newton’s sec-

ond law of the conservation of energy principle, which is appropriate for flowing
fluids. The qualitative behavior that is usually labelled with the term “Bernoulli
effect” is the lowering of fluid pressure in regions where the flow velocity is
increased. This lowering of pressure in a constriction of a flow path may seem
counterintuitive, but seems less so when you consider pressure to be energy den-
sity dependent. In the high velocity flow through the constriction, kinetic energy
must increase at the expense of pressure energy (Fig. 1.17).
The calculation of the “real world” pressure in a constriction of a tube is difficult
to do because of viscous losses, turbulence, and the assumptions which must be made
about the velocity profile (which affect the calculated kinetic energy). The model cal-
culation here assumes laminar flow (no turbulence), assumes that the distance from
the larger diameter to the smaller is short enough that viscous losses can be neglected,
and assumes that the velocity profile follows that of theoretical laminar flow.
Laminar flow in a straight pipe may be considered as the relative motion of a set of
concentric cylinders of fluid, the outside one fixed at the pipe wall and the others mov-
ing at increasing speeds as the center of the pipe is approached. We saw this above in
everyday life as we open a tap, a little, then more, and finally full—the flow is lami-
nar, then wavy and, lastly turbulent, respectively (McDonough 2009) (Fig. 1.15).

1.3.3.2 Shape of Structures in Fluid Motion (Machines)

Different body shapes have varying pressure gradients and different boundary layer
transition and separation points. The concept of the boundary layer was first intro-
duced around 1904 by Ludwig Prandtl. Friction drag is due to shear stresses in the
boundary layer (thin layer of a flowing gas or liquid in contact with a surface such
as that on an airplane wing) and pressure drag depends on the shape of the body, i.e.,
the pressure differences between the front and rear of the body which determines the
wake thickness that the body drags behind it. Dependence of pressure drag on body
1.3  Fluid Mechanics 21

shape can be seen where both bodies have approximately the same drag at high
Reynolds number. For instance, drag of an airfoil of chord c is relatively the same as
the drag on a cylinder of diameter 0.005c (Thwaites 1960). Experimental observa-
tions show that when the flow field region is away from a solid body, the inviscid
flow as in the Bernoulli equation, approximates the flow. In this way, the viscosity
effects can be viewed as a mechanism in which the information is transferred from
the solid body into depth of the flow field. On the other hand, in a very close prox-
imity to the solid body, the region must be considered as viscous flow while the flow
far away from the body is an inviscid flow. The connection between these regions
was proposed by Ludwig Prandtl, of which we will see more later.
Hoerner (1965) demonstrated when Re No is about 4 × 105 that during flow
around a continuous cylinder (Fig. 1.18a) the laminar boundary layer does not
have sufficient kinetic energy, and separates, thereby increasing pressure drag,
resulting in a turbulent wake. In contrast, the flow pattern in the streamline section
shown in Fig. 1.18b is shaped and angled so that the change in the flow direc-
tion is much smaller than the change around the cylinder (continuous cylinder or
sphere) and results in a small, almost nonexistent, wake trailing behind it (tur-
bulence), which is the reason that the drag coefficient reduces by roughly 80 %.
However, there sometimes is a circulation behind the sphere. Fluid that comes
round the cylinder close to it moves away from it before reaching the rear point of
symmetry. As a result, two “attached eddies” exist behind the cylinder; the fluid in
these circulates continuously, not moving off downstream. These eddies get bigger
with increasing Re No. Later we will see a consequence of these eddies.
What happens for still larger Reynolds numbers? As the speed is increased fur-
ther, the wake increases in size again and the drag increases. The latest experi-
ments, which go up to Re = 107 or so, indicate that a new periodicity appears in
the wake, either because the whole wake is oscillating back and forth in a gross
motion or because some new kind of vortex is occurring together with an irregular
noisy motion (Fig. 1.19).

Fig. 1.18  Flow around
sphere and streamlined body.
Variation in flow pattern
and drag coefficients for
two-dimensional bodies
of different shapes at Re
No greater than 4 × 105.
Redrawn after Hoerner
(1965)
22 1  Swimming and Flying in Vertebrates

Fig. 1.19  At very high Re

No. Here the speed increases
and the wake increases in
size and the drag increases.
The latest experiments go up
to Re = 107 or so, indicating
that a new periodicity appears
in the wake, either because
the whole wake is oscillating
back and forth in a gross
motion or because of some
new kind of vortex

The tendency for the most striking flow features to occur downstream of the
cylinder becomes even more marked as one goes to higher Reynolds numbers.
This region is called the wake of the cylinder. For Re > 40, the flow becomes
unsteady and there is suddenly a complete change in the character of the motion.
As with transition to turbulence in a pipe, this unsteadiness arises spontane-
ously even though all the imposed conditions are being held steady. The insta-
bility together with a large local variation in fluid velocity develops to give the
flow pattern, known as a Kármán vortex street, shown schematically in Fig. 1.20.
What happens is that one of the vortices behind the cylinder (Fig. 1.18a) gets so
long that it breaks off and travels downstream with the fluid to form vortices of
the street. Then the fluid curls around behind the cylinder and makes a new vor-
tex. The vortices peel off alternately on each side of the wake, so an instantaneous
view of the flow looks roughly as sketched in Fig. 1.20b. We will see below how
the phenomenon Kármán vortex street may be associated with thrust generation.
Laminar flow over a horizontal surface may be thought of as consisting of thin
layers, or laminae, all parallel to each other. The fluid in contact with the horizon-
tal surface is stationary, but all the other layers slide over each other, as a deck of
new cards, which “flows” in a laminar fashion. Laminar flow is common only in
cases in which the flow channel is relatively small, the fluid is moving slowly, or
its viscosity is relatively high. Oil flow through a thin tube or blood flow through
capillaries is laminar. Most other kinds of fluid flow are turbulent except near solid
boundaries, where the flow is often laminar, especially in a thin layer just adja-
cent to the surface. Turbulent flows are chaotic or unstable motions in a fluid, e.g.,
around moving objects such as air planes or birds excessive turbulence can make
their motion inefficient and even difficult to control. Moin and Kim (1997) note
that all the fluid flows that influence scientists and engineers are turbulent ones and
that turbulence is the rule not the exception in fluid dynamics. Because the speed
of the fluid at any point is continuously undergoing changes in both magnitude and
direction it is why it is so difficult to calculate, and presents the greatest challenge
in attempts to calculate such changes (see the Navier–Stokes equations below).
1.3  Fluid Mechanics 23

Fig. 1.20  After a certain value of Reynolds number, a Vortices are created in an infinite parade,
which break off and re-form on the left and right side of an object. This phenomenon is called
Von Karman vortex street. b Diagrammatic view of (a)

The concept of turbulence was first mentioned by Leonardo da Vinci over

500 years ago and features in one of his famous sketches, which captures
with remarkable clarity the chaotic nature of the flow (Fig. 1.21a). Although
the analysis is difficult, modern technology is helping to analyze flow fields
(McDonough 2009). For instance, Spedding and colleagues (2005) used a
relatively new measurement technique involving velocimetric particle imag-
ing (VPI) in which a pulsed laser sheet illuminates the flow field being studied
(Fig. 1.21b, c).
When and why is it justifiable to neglect viscosity? There is no single answer.
For instance, if a drastic enough reduction in pipe radius is used to yield a pres-
sure in the constriction which is less than atmospheric pressure, there is almost
certainly some turbulence involved in the flow into that constriction but in most
of the above examples where fluid flow is streamlined we can consider that turbu-
lence is negligible and the Bernoulli equation will suffice. However, given as we
have said that turbulence is the rule not the exception in fluid dynamics another set
of equations is necessary in such calculations. These are the Navier–Stokes equa-
tions (the general differential equations arising from applying Newton’s second
law to viscous fluid motion) in which the viscosity (μ) of a fluid is included, may
be used. There has been a tendency to ignore these equations largely because they
are complicated and notoriously difficult to use. However, we must emphasize
here the importance of the Navier–Stokes equations, regarded as the “equations of
fluid motion” (McDonough 2009), although it is formidable to apply particularly
in solving problems with respect to vorticity and turbulence.
The Navier–Stokes equations was the driving force behind the development
of supercomputers in the U.S. aerospace industry and NASA laboratories. Today,
24 1  Swimming and Flying in Vertebrates

Fig. 1.21  Turbulent flow. a Leonardo da Vinci sketch depicting turbulence. b Spanwise vorticity

at (L/D) max for flat plate and c cambered plate. The disorderly flow behind the flat plate sup-
ports the L/D data from previous studies. b and c reproduced by permission of Geoff Spedding,
after Spedding et al. (2005)

computational fluid dynamics (CFD) is rapidly becoming the dominant flow anal-
ysis technique, especially in industrial environments and it is only a matter of time
before it is widely used in biomedical and bioengineering fields. We will see fur-
ther on how computer analysis and simulations have made the equations much
more accessible in resolving questions of turbulent flow of liquids. Given this, a
brief discussion of the Navier–Stokes Equation is presented.
1.3  Fluid Mechanics 25

1.3.3.3 Navier–Stokes Equation

Fluid motion is described by a set of three equations known as the Navier–Stokes

equations. The derivation of the Navier–Stokes equations begins with an applica-
tion of Newton’s second law, conservation of momentum (often alongside mass and
energy conservation) and can be written for an arbitrary portion of the fluid. There
is one equation, each for the X, Y, and Z direction of three-dimensional space. For
instance, one may have a situation where forces in any two planes may exert stress
on the third, i.e., the force available to accelerate a particle of fluid is the vector sum
of the pressure differences acting across it, its weight, and the viscous force due to
shear gradients in the surrounding fluid. The general form of the equation is
 
∂u
ρ + u · ∇u = −∇p + µ∇ 2 u + f.
∂t
where ρ is the density of fluid, P is the pressure, μ is the viscosity, and f is the sum
of the external forces per unit mass which sustains the motion.
These accelerations, and corresponding accelerations in the other two direc-
tions, are described by the equation of motion of the fluid. For a fluid moving so
slowly compared with the speed of sound that it may be treated as incompressible
and in which the variations of temperature from place to place are insufficient to
cause significant variations in the shear viscosity η.
A limitation is simply the complicated nature of the equations. Time-tested for-
mulations exist for common fluid families, but the application of the Navier–Stokes
equations other than for Newtonian fluids (in which the viscosity is constant for dif-
ferent rates of shear and does not change with time) is extremely complicated.

1.4 Flight and Fluid Mechanics

Both swimming and flying involve moving through a three-dimensional medium

(fluid), water and air, respectively, and many of the significant differences between
the two locomotory modes involves the fact that water is much more viscous than
air and is almost incompressible.
Early attempts to replicate bird flight in mechanical systems failed because it
was impossible to obtain lift and thrust from the same organ, i.e., wings. It was
necessary to separate lift and thrust generation, so that aircraft wings provide lift
while a propeller generates thrust. In striking contrast birds, e.g., generate lift and
thrust by flapping their wings, which continuously change shape and deform elas-
tically throughout the wing stroke, conditions that are virtually impossible to repli-
cate in a single structure in flight machines (in Volume 1 (Lingham-Soliar 2014a),
we saw how essentially the same problem has plagued our understanding of plesi-
osaur underwater flight, with impractical, albeit occasionally clever, mathematical
discussions that ignore the biological constraints particularly the poor elasticity of
their “wings”). An analytical solution of Navier–Stokes equations which describe
26 1  Swimming and Flying in Vertebrates

the aerodynamic forces that keep fliers aloft, would, in principle, solve the problem
of how birds fly, but there are still questions that concern the downwash on wings
and turbulence and solutions to these equations defy scientists to this day.
Among general principles considered above was the bound vortex and the effects of
a tear-drop shape compared to a cylinder or sphere. The same principle in the aerofoil
structural design enables an animal to cleave through the air while at the same time
reacting against the forces of gravity. The aerofoil shape may involve (1) the shape of
entire organism, (2) the shape of the limbs, e.g., wings, and, uniquely in birds, and
(3) the shape and structure of the integumental structures covering the body, namely
feathers (all three conditions are found in birds). The wings produce lift and thrust but
any object moving through air or water experiences a slowing down force called drag,
which will be dealt with in detail later on but suffice it to say that the design of the
wing and its inclination will play a vital part in reducing drag and increasing thrust.
To calculate lift commonly the front end (usually maximal front cross-section)
is used. Sometimes, the total surface area (‘wetted area’) is used. This is because
two different types of drag may be involved depending on the physical conditions
(friction drag and pressure drag mentioned above). The lift L on a body moving at
speed v through fluid of density p is
1 2
L= pv AP CL
2
AP is the plan area and CL the coefficient of lift.
If this appears confusing it is because neither the frontal area nor the wetted area
but the plan area (Fig. 1.22), the flattened, outstretched area of the wings including a
band across the body is used (discussed below). Hence, different areas may be used
with corresponding different lift conditions that involve factors such as shape of the
aerofoil and its speed through the air, which are referred to as the coefficient of lift.
We will now look at some of the forces that need to be considered in calculating lift
starting with the aerofoil.

Fig. 1.22  Bird. Showing
planform and frontal areas.
Redrawn after a design by
David Alexander (2002).
Photo courtesy of Jordan
Ralph
1.4  Flight and Fluid Mechanics 27

1.4.1 The Aerofoil

An aerofoil produces a lifting force that acts at right angles to the airstream and a
dragging force that acts in the same direction as the airstream (Fig. 1.23). This fig-
ure shows a wing with an asymmetrical cross-section, with the upper surface more
convex than the lower. The airflow around such an aerofoil moves faster over the
upper surface than the lower, resulting in lower pressure on the upper surface than
the lower. Because of the pressure difference of the whole aerofoil (from Bernoulli
effects) the force F acting at the quarter chord position, i.e., a point 25 % of the
chord length from the leading edge, becomes directed upwards and slightly back-
wards. This force is conventionally resolved into a drag component D along the air-
flow path and the lift force L, vertical to the airflow path (Norberg 1990). Lift and
drag are then measured perpendicular and parallel to the relative wind, respectively.
The lift and drag coefficients indicate the capacity of an aerofoil to generate
lift and drag at a given angle of attack (α). They are dependent on the shape of
the aerofoil, the Re No, and the downwash angle, the angle through which the air
is deflected at the rear of the wing. The downwash angle is in turn dependent on
the angle of attack of the wing. We will look at this in a little greater detail with
respect to a phenomenon known as the bound vortex.

1.4.2 The Bound Vortex

A general definition of a free vortex in fluid mechanics is, a circular, spiral, or

helical motion in a fluid which, often forms around areas of low pressure and
attracts the fluid and objects that may be moving within it, toward its center.

Fig. 1.23  The forces acting on an aerofoil at an angle α to the direction of motion. F is the

resultant aerodynamic force, conventionally resolved into a lift force, L, perpendicular to the
resultant direction of movement, and a drag force, D, backward along the direction of flow.
The lift: drag ratio (L/D) is determined by tan ϑ. Redrawn after Norberg (1990)
28 1  Swimming and Flying in Vertebrates

The tornado that famously carried Dorothy in her Auntie Em’s house off to Oz
is not an unrealistic view of the powerful suction forces created by such a vor-
tex. As we saw above, trailing vortices on streamlined bodies may end in turbu-
lent wakes that exert a small suction on the back of the body, which is directed
backward from the body (in effect acting against forward movement) and are of
particular interest to fluid dynamists in understanding flight.
Here, specifically, we look at what happens when air flowing horizontally
meets the front end of an aerofoil shaped structure. The aerofoil cleaves or dis-
places the airflow, part of which passes over the aerofoil’s upper surface and part
over the lower. This flow of air over a body such as an aerofoil is referred to as the
bound vortex, i.e., the attached boundary layer, which as defined by Thompson’s
theorem is a closed loop which moves with the fluid. Streamlines run along the
wings with an outward direction on the bottom surface and an inward direction
on the upper surface (Fig. 1.23). They are referred to as the bound vortices, which
are formed by the boundary layer that surrounds the wing surface. As the aerofoil
starts to move it produces an initial vortex. When the air leaves the trailing edge of
the wing, the air from the upper surface is inclined to that from the lower surface,
and helical paths, or vortices, result (Norberg 1990). A whole line of vortices trails
back from the wing, the vortex being strongest at the tips and decreasing rapidly
to zero at midspan. A short distance downstream, the vortices roll up and combine
into two distinct cylindrical vortices that constitute the ‘tip’ vortices. The tip vor-
tices cause additional downflow (or downwash) behind the wing within the wing-
span. All the air within the vortex system is moving downward (called downwash)
whereas all the air outside the vortex system is moving upward (called upwash).
The gradient, or change of downwash to upwash, can become very large at the tip
vortices and cause extreme motions in the aeroplane flying through it (Fig. 1.24).
We saw above that the delay in separation of the bound vortex is important
in the forward momentum of the aerofoil. As David Alexander notes (2002), the
magnitude of lift produced by an aerofoil is proportional to both the speed of the
movement through the air and the strength of the bound vortex (its speed of rota-
tion, or circulation). Since the bound vortex itself is created by the airflow, the cir-
culation is also proportional to the speed of the aerofoil’s movement. The lift on an
aerofoil then is proportional to the square of the speed—once for the airflow itself,
and once for the strength of the bound vortex. We will look at wing tip vortices in
a little more detail further on.
In a gliding experiment with a kestrel, Spedding (1987) calculated circula-
tion in the two trailing vortices using photogrammetry (flow visualization parti-
cle image velocimetry) techniques. Calculations on the wing beat frequencies
showed two continuous trailing vortices (Fig. 1.25a, b, bottom) and were found to
be similar to that measured behind an elliptically loaded aerofoil of the same span
(Norberg 1990), i.e., the lift coefficient values obtained through two different sets
of calculations are close enough to conclude that the lift distribution over a gliding
kestrel is elliptical. This contrasts with the wing tip vortices behind a pigeon that
shows discontinuous hoops (Fig. 1.25a). Norberg (1990) however, cautioned with
respect to flapping flight that other circulation patterns may be more useful. Later
1.4  Flight and Fluid Mechanics 29

Fig. 1.24  Trailing vortices. a Simplified vortex distribution of an aerofoil in steady flight.

The vortex system consists of a bound vortex over the wing and two trailing vortices, one on
each wake behind the wing tips. A transverse starting vortex is shed whenever the strength of
the bound vortex (= circulation Г) changes. L = lift and D  = drag (Norberg 1990). b Airflow
direction over the upper surface of the wing (left figure) and past the lower surface of the wing
(middle figure) as well as the flow in the spanwise direction as seen from in front (right figure)—
defines subpressure and + defines superpressure. Redrawn after Norberg (1990)

we will see that many flying vertebrates have more efficient pressure distributions,
e.g., in the swept-back wing tips and pointed wing tips of many birds.

1.4.3 Drag

We considered above a dimensionless theorem called the coefficient of lift, L,

involved in thrust. Another dimensionless theorem involves forces exerted by the
fluid on the aerofoil in an opposite direction to thrust, which slows it down, called
the coefficient of drag, D. Drag may be defined as the component of the net aerody-
namic (or hydrodynamic) forces acting opposite to the direction of the movement.
A fluid stream exerts a drag force F D on any obstacle placed in its path, how
large it is and how it may be reduced are questions of obvious importance to
designers of moving vehicles of all sorts (Fig. 1.26). The more aerodynamically
shaped or streamlined an object is, the more drag is reduced. It is at the rear of the
obstacle that separation occurs, and it is therefore the rear that needs streamlining.
As we saw in the introduction to the Bernoulli equation when a fluid flows over
a blunt object such as a sphere, the flow separates early from the posterior end,
which produces a wide, turbulent, low pressure wake. In contrast, when the air
30 1  Swimming and Flying in Vertebrates

Fig. 1.25  Schematic representation of the wake as reconstructed from stereophotographs. a Top

shows the vortex hoops behind a pigeon in slow flight and, bottom shows the continuous vortex
behind a kestrel in fast flight. b Shows the wing flight dynamics in the upstroke and downstroke
in vortex hoops and continuous vortex in (a). After Spedding (1987)

passes over a streamlined shape, the flow tends to follow the tapered rear of the
body, separating much later and thereby producing little or no wake (Figs. 1.18b
and 1.26).
Thus, because the low pressure area is much smaller, the forces acting against
forward movement are reduced. Drag (D) on a body moving at speed (v) through a
fluid at density p gives the following equation (also using the plan area). The drag
D on a body moving at a speed v through fluid of density p is
1 2
D= pv Ap CD
2
Ap is the plan area and the nondimensional drag coefficient CD (Alexander 1992).
Drag is a function of the angle of attack, Re No, and the surface roughness
ratio. Drag acting on a body is composed of (1) friction drag caused by the shear-
ing stress or tangential force acting on the “wetted surface” of the body or bound-
ary layer caused by fluid viscosity and (2) pressure drag which is due to pressure
differences between the front and rear of the body, which occurs because of the
turbulent wake created by the moving fluid behind. This occurs because the pres-
sure in the wake is lower than the pressure on the front of the body. Pressure drag
is more or less proportional to the frontal area and caused by (a) the viscous flow
1.4  Flight and Fluid Mechanics 31

Fig. 1.26  Streamlines over car. In engineering, understanding flow patterns can help design
vehicles with higher speed and reduced drag potential and lower fuel costs. In a the streamlines
at the rear remain attached to the body with less turbulence. In b the streamlines break away ear-
lier at the blunt end of the car roof, creating more turbulence

at very low speed for a small body, (b) flow separation or form drag, and (c) the
flow deviation resulting from the normal force to the flow, called induced drag.
Induced drag consists of two primary components, vortex drag and lift-
induced viscous drag. The vortices in the flow-field, present in the wake of a
lifting body, derive from the turbulent mixing of air of varying pressure on the
upper and lower surfaces of the body. As the lift generated by a body increases,
so does the lift-induced drag. For an aircraft in flight, this means that as the angle
of attack, and therefore the lift coefficient, increases to the point of stall, so does
the lift-induced drag. At the onset of stall, lift is abruptly decreased, as is lift-
induced drag, but viscous pressure drag, a component of parasite drag (below),
increases due to the formation of turbulent unattached flow on the surface of the
body. Induced drag behaves differently with speed changes, it is very high at low
speeds, drops rapidly as speed increases, and flattens out to a shallow decline at
high speeds.
One further term with respect to drag is parasitic drag caused by moving a
solid object through a fluid. Parasitic (form or body) drag is made up of mul-
tiple components including viscous pressure drag (form drag), and drag due to
surface roughness (skin friction drag), which we see increases with airspeed
(Fig.  1.27). The parasite drag is proportional to the cross-sectional area of
the body, and to the square of the forward speed. As we also see induced drag
32 1  Swimming and Flying in Vertebrates

Fig. 1.27  Graphs on the
power curves: form and
induced drag versus airspeed

tends to be greater at lower speeds because a high angle of attack is required to

maintain lift, creating more drag (Fig. 1.28). However, as speed increases the
induced drag becomes much less, but parasitic drag increases because the fluid
is flowing more quickly around protruding objects, which increases friction or
drag. Hence, in flight the total coefficient of lift is calculated in many instances
to include the pressure and skin friction drag and the induced drag, which is a
function of lift. We will return to these terms in discussions on bird flight in
Chap. 5.

1.4.4 Angle of Attack

The angle of attack (the angle of the aerofoil, made by its chord in relation to the
relative airflow) is important in determining lift. With a higher angle of attack
(up to the point of stall) the flow speed increases at the top of the wing, an effect
seen in Figs. 1.23 and 1.28b by the streamlines being squeezed together, which
will increase lift, i.e., the circulation (strength of the bound vortex) as the angle
of attack increases; a lower angle will decrease it. A change in lift also results in
a change in drag. When lift is increased by enlarging the angle of pitch and thus
the angle of attack, drag will increase and slow down the aerofoil. The greater the
speed, the greater the lift and drag will be. Thus, total lift is related to the shape of
the airfoil, the angle of attack, and the speed with which the wing passes through
the air. Induced drag is caused by that element of the air deflected downward
which is not vertical to the flight path but is tilted slightly rearward from it. At a
critical point, the angle of attack can become so great that the airflow is broken
over the upper surface of the wing, and lift is lost while drag increases. This criti-
cal condition is termed the stall (Fig. 1.28c).
1.4  Flight and Fluid Mechanics 33

Fig. 1.28  Illustration of
different angles of attack,
(a–c). a Low angle of attack
to direction of motion.
b High angle of attack. c Very
high angle of attack resulting
high turbulence and stall
(arrow lengths indicate the
proportions of lift and drag)

1.4.5 Wing Planform

The wing planform is the shape it forms when seen from above. The lift and drag
are variously affected by the shape of the wing planform also referred to as the
aspect ratio (Fig. 1.22), which we will turn our attention to and to how it affects
wing loading and the flying characteristics of the animal. The wing loading is the
ratio of the aeroplane or animal’s weight to its wing area.
Aspect ratio (AR) is derived from the span and area measurements by the
formula
AR = b2 /S,
while wing loading (QS) is derived from the mass and area measurements by the
formula

Qs = mg S
where g is the acceleration due to gravity, taken to be 9.81 ms−2 (Pennycuick 1972).
An aeroplane/animal with a high wing loading has to fly faster to generate the lift
to stay airborne. Hence a heavy, small-winged jet plane, e.g., has a high wing load-
ing and has to fly faster than a sailplane, which has low wing loading (Fig. 1.30). The
planform area of a wing helps to determine the amount of lift that is produced—the
34 1  Swimming and Flying in Vertebrates

greater the area of the wing, the larger area to generate lift (Fig. 1.29). The aspect
ratio as can be calculated from above is the ratio of wing span to the chord, or width
of the wing. It is a measure of how long and slender a wing is or short and broad. A
wing with a high aspect ratio is long and narrow and in contrast a short and broad
wing is of low aspect ratio. Thus, whether a wing has a high or low aspect ratio will
inform us how the wing performs and in what circumstances and conditions. Such
details of the shape of the aerofoil can have significant effects on the performance of
a wing particularly at high Reynolds numbers. These variations in aspect ratio and
wing area are found among different bird species (see Chap. 5). Lift, drag, and stall
are all variously affected by the shape of the wing planform. An elliptical wing, for
example, while ideal aerodynamically, has a more undesirable stall pattern than a
simple rectangular wing and we will see below some devices present in birds with
pointed wings to reduce stall (Norberg 1990; Azuma 2006; Chklovski 2014).
Because of low speed and small length scales, birds fly in the low Reynolds
number range, 103–105 (Fig. 1.29). In Figs. 1.29 and 1.30 insects occupy the lower
end of the scale. Large model airplanes closely resemble birds in size and flying

Fig. 1.29  Aspect ratio (b2/S) versus relative wing loading (Mg/S)/M1/3 in various birds. The
encircled foraging groups are defined solely by the flight and foraging modes of their members,
not by systematic affinity. Here just the major groups are shown. 1, continuous flight. 1a = swifts,
hirundines, Falco, Accipiter; 1b = hovering, hummingbirds; 1c = albatrosses; 1d = vul-
tures; 1e = cranes, storks, herons; 2, Perching. 2a = flycatchers; 2b = owls, many raptors; 3,
locomotion among vegetation. 4, foraging on ground or in water. 4a =  Charadris, Calidris,
Tringa, Limosa. Ground foraging within vegetation. 4b = Galliformes. Foraging in open water.
4c = Alcidae, Anatidae, Gavia, Mergus, Anser, Cygnus. Aa = Apus apus; Cc = Cygnus Cygnus;
D = diving petrels; Df = Darwin’s finches; Fm = Fregata magnificens; Ga = Gallirallus aus-
tralis; H = hirundines; SB = Sula bassana. (See Norberg 1990, Table 12.1 for full descriptions.)
Figure reproduced with permission of Ulla M Lindhe Norberg
1.4  Flight and Fluid Mechanics 35

Fig. 1.30  The great flight diagram comparing wing loading and cruising speeds of the largest
and fastest airliners to the smallest insects. After Tennekes (1996)

speeds. General aviation falls within high Reynolds numbers = 106–107 while jet
aircraft have Reynolds numbers at about 107–108 (Fig. 1.30).

1.4.5.1 High AR Wings with Pointed Tips

Classic theory says a pointed wing tip will be deleterious to the wing’s aerodynamic
performance. Due to the small surface area of the tip, local lift coefficients will be very
high leading to tip stall. This in turn will increase pressure drag. Thus viewed in the
light of standard aerodynamic theory, the pointed wing tip might be disadvantageous
36 1  Swimming and Flying in Vertebrates

Fig. 1.31  Wing tip of high aspect-ratio wing with downward configuration. In a positive angle
of attack there is an outflow component of velocity on the underwing surface near the tip, an
upflow component around the tip from the lower surface to the upper surface, and an inflow com-
ponent from the top surface to the tip. These components make a spiral vortex flow around the
tip, called tip vortex, which trails from the respective wing tips and concentrates a vortex core.
Redrawn after Azuma (2006)

to the aerodynamic performance of oceanic birds (Lissaman personal communication

in Chklovski 2014, reference in Chap. 5). On the other hand, these birds are the most
efficient fliers in nature (see below and Chap. 5) and so an interesting conflict arises.
Azuma (2006) in considering wings of different aspect ratio showed that some gains
in the effective aspect ratio can be obtained by relatively minor alteration to the tip
region of flat wings for equal span (Figs. 1.31 and 1.32). The same principle could be

Fig. 1.32  Winglet or auxiliary wing. Lift distribution on a winglet that provides both a lift and
drive component. Redrawn after Azuma (2006)
1.4  Flight and Fluid Mechanics 37

Fig. 1.33  Black-browed
albatross, Diomedea
melanophris. Wing tip
downward curve. Photo,
permission of Lloyd Edwards

applied to the nonplanar wing of downward concave arc—the important thing is to

obtain a nonplanar vortex wake specifically near the wing tips. Many sea birds, e.g.,
that have wings with pointed tips, adopt the downward concave arc wing configura-
tion (Pennycuick 1982) (Fig. 1.33; also see Chap. 5) instead of the upward concave arc
wing configuration during gliding flight. Furthermore, aerodynamic theory says that
long, narrow wings lower induced drag costs from approximately the span mid-point
to the tip (Azuma 2006).
Let us now examine the local flow behavior near the wing tip more closely.
With a positive angle of attack of the wing tip, there is as shown in Fig. 1.31, an
outflow component of velocity on the underwing surface near the tip, an upflow
component around the tip from the lower surface to the upper surface and an
inflow component on the top surface of the tip. These flow components make a
spiral vortex flow around the tip, called tip vortex, which trails from the respective
wing tips and concentrates a vortex core. As a result the local flow direction at the
tip has a greater upwash component than that of the freestream (Azuma 2006).
In addition, birds have a small auxiliary wing, alula or winglet that is mounted in
such a way that (1) its span projects radially in any direction from the wing tip,
i.e., not necessarily in parallel with the main wing, and (2) its chord forms an ade-
quate angle of attack with respect to local flow as shown in Fig. 1.32. Although,
because of the small winglet area, the lifting component is small, the driving com-
ponent or thrust contributes to reducing the induced drag of the wing (Azuma
2006). In Chap. 5, we will discuss how sea birds with high aspect ratio wings may
benefit from pointed wing tips in gliding.

1.4.5.2 Broad Low AR Wings with Slotted Tips

Land soaring birds such as eagles, vultures, and buzzards, like sea birds, also
spend much time gliding during their search for food but rather than long pointed
wings they have shorter, broad wings (Fig. 1.34). They too need to be able to
exploit thermals and air currents. Tucker (1993) showed from five independent
points of view how the slotted tips of bird wings reduce drag in the sense that they
increase the span factor.
1. Wing theory explains how the feathers in the slotted tips could reduce drag by act-
ing as winglets, and measurements show that winglets on aircraft do reduce drag.
38 1  Swimming and Flying in Vertebrates

Fig. 1.34  Cape vulture Gyps

caprotheres with slotted wing
tips. Photo, permission of
Clint Ralph

2. Slotted tips have reduced drag because the tip feathers are exposed to upwash
at the end of the base wing. The reduction in tip drag does not increase the drag
of the base wing.
3. The slotted tip maintains the span factor of the wing as the angle of attack of the
base wing increases. In contrast, the span factor of the base wing with the Clark Y
(nonsymmetrical section with greater curvature on upper than lower surface, latter
virtually flat (Tucker 1993, Fig. 5)) tip declines as the angle of attack increases.
4. In wing theory, winglets reduce induced drag by spreading vortices. Flow visu-
alization shows that winglets on a model wing spread vorticity both horizon-
tally and vertically.
5. Slotted tips occur in soaring birds of several families and always have vertical
separation between the tip feathers in flight. The fact that vertical separation is
necessary for drag reduction suggests that slotted tips result from natural selec-
tion for wing configurations with low drag.
How vultures conserve energy while gliding long distances over land as opposed
to the sea will be discussed further in Chap. 5.

1.5 Points of Debate

Before concluding this discussion on aerial locomotion a few questions may occur,
do we use Bernoulli or Newton’s laws for lift, and how do asymmetrical wings
work, e.g., when flying upside down in an aeroplane and, is there light at the end
of the tunnel in using the complicated Navier–Stokes equations to resolve the
problems of turbulence?

1.5.1 Bernoulli or Newton’s Laws for Lift?

Two different principles work in creating lift—the pressure differentials between

the upper and lower surfaces of the wing, and the downwash over the wing trail-
ing edge creating an upthrust. Which is best for describing how aircraft get the
1.5  Points of Debate 39

needed lift to fly—Bernoulli’s equation or Newton’s second and third laws involv-
ing conservation of momentum? The Bernoulli equation is simply a statement of
the principle of conservation of energy in fluids. Conservation of momentum and
Newton’s third law are equally valid as foundation principles of nature.
Advocates of lift by Newton’s laws appeal to the clear existence of a strong
downwash behind the wing of an aircraft in flight. The fact that the air is forced
downward clearly implies that there will be an upward force on the aerofoil as in
Newton’s third law of reaction force, i.e., for every action there is an opposite and
equal reaction. From the conservation of momentum viewpoint, the air is given a
downward component of momentum behind the aerofoil, and to conserve momen-
tum, something must be given an equal upward momentum. The lift includes a
vortex in the circulating air. The aerofoil similarly produces a bound vortex
because of its shape (Schlichting 1970). Newton’s third law applies similarly to
lift on a rotating cylinder or helicopter foil as in the Kutta-Joukowski theorem (Bai
and Wu 2013).
Arguments against modeling the lift process with the Bernoulli equation
include the fact that the flow is rarely incompressible (a criterion of Bernoulli’s
equation), and therefore the density changes in the air should be taken into
account. This is true—the ideal gas law should be obeyed and density changes will
inevitably result. This does not render the Bernoulli equation invalid, it just makes
it harder to apply. But the pragmatic success of modeling the lift with Bernoulli,
neglecting density changes, suggests that the density changes are small. There are
also practical difficulties for the model on lift from Newton’s third law, it is dif-
ficult to measure the downward force associated with the downwash because it is
distributed in the airstream as turbulence as it leaves the trailing edge of the aero-
foil (Batchelor 2000) (we may see this problem minimized in the future; see sec-
tion on turbulence below).

1.5.2 Flying Upside-Down

Aerobatic displays show planes that make loops in the air and fly upside-down.
If the greater curvature on top of the wing and the Bernoulli effect are evoked to
explain lift, how is this possible? An increase in airstream velocity over the top of
the wing can be achieved with aerofoil surface in the upright or inverted position.
It requires adjustment of the angle of attack, but as clearly demonstrated in almost
every air show, it can be done. While the typical asymmetric shape of an aerofoil
increases efficiency of lift production in its upright position, the asymmetry of the
aerofoil is not essential for producing lift. There is a limit to the lift that can be
generated in this way because if the inclination is too great the boundary layer
separates behind the wing’s leading edge, and the bound vortex on which the lift
depends, may be shed as a result. The animal or aircraft is then said to stall. See
Chaps. 4 and 5 for how hummingbirds (Sapir and Dudley 2012) and bats fly back-
wards during feeding despite the aerofoil shape of the wings.
40 1  Swimming and Flying in Vertebrates

1.5.3 Turbulence and Supercomputers

Because of the complexity of dealing with turbulent flow some further comments
are given here. One of the main reasons for this complexity is that in turbulent flow
the speed of the fluid at any point is continuously undergoing changes in both mag-
nitude and direction (as we saw earlier). This means constantly having to make
changes in calculations to accommodate them. Do we really need to bother? As
mentioned practically all fluid flows that we are involved with are turbulent ones,
for instance—the flow of fluids in our bodies, blood moving through vessels to our
heart, air flowing through tubes into our lungs, then in engineering, e.g., automobiles
and airplanes that travel through air and ships through the water, and last and not
least animal flight, all experience turbulence—making an understanding necessary.
Turbulence is composed of eddies or swirling bodies of air or water moving
chaotically around the overall direction of motion. Its importance unfortunately is
matched by its reputation as one of the most thorny problems of classical physics
(Moin and Bewley 1994; Moin and Kim 1997). In a fascinating article by Parviz
Moin and John Kim (1997) we get a glimpse of the significance and momentous-
ness of the question of turbulence, not just through their own descriptions but
through comments by other notable workers over the decades, which they drew
attention to. For instance Richard Feynman, the Nobel Laureate physicist called
turbulence “the most important unsolved problem of classical physics.” This was
not an exceptional view. The British physicist Horace Lamb in the 1930s, in old
age, in an address to the British Association for the Advancement of Science
remarked wittily that when he died and went to heaven there were two matters he
hoped for enlightenment, one was quantum electrodynamics and the other was the
turbulent motion of fluids. He added “about the former I am rather optimistic.”
As Moin and Kim note, Lamb’s pessimism with respect to understanding tur-
bulence could not have anticipated computers, let alone supercomputers which
would provide engineers and biologists with new invaluable insights into the prob-
lem—although even with their development it was still a while before their poten-
tial in understanding turbulence reached some realization.
The Navier–Stokes equations, despite being among the greatest achievements in
fluid dynamics, are, as mentioned above, notoriously difficult to apply. The applica-
tion of supercomputers to these equations is regarded as “one of the greatest achieve-
ments in fluid dynamics since the equations themselves were formulated” (Moin and
Kim 1997). However, the authors state that in aircraft technology with the latest com-
puters the Navier–Stokes equations has the potential to be used to calculate the veloc-
ity and pressure of the air at any point near the aircraft’s surface and allow engineers
to calculate various aerodynamic parameters such as lift, drag (the hardest to calculate
because it is most dependent on turbulence), and moments (twisting forces) exerted
on the aeroplane—invaluable in designing safer and more economical aircraft.
Drag may involve a special form of turbulence and presents problems that are
difficult to analyze. The boundary layer over an aerofoil may become turbulent dur-
ing flight, reducing momentum—causing drag. Hence, a great deal of the work by
1.5  Points of Debate 41

engineers (aero- and hydrodynamicists) involves understanding the mechanics of

the generation and destruction of turbulence (Hewitt and Vassilicos 2005). In this
context and perhaps the simplest way to define turbulence is by reference to the
Reynolds number. For instance large inertial forces, relative to viscous one (terms
described above), tend to favor turbulence whereas high viscosity staves it off. In
other words turbulence occurs when the Re No exceeds a certain value. The num-
ber is proportional to both the size of the object and the flow velocity. For exam-
ple, the Re No for air flowing over the fuselage of a cruising commercial aircraft
is around 100 million while for blood flowing in a midsize artery, it is about 1,000.
Moin and Kim note that even the apparently simple, dimpled surface on a
golf ball may appear to many nothing more than aesthetic. This could not be
further from the truth and just another example of how the correct designs can
reduce drag. Golf balls present an intriguing example of how a surface texture
can advantageously control airflow when the ball is travelling through the air
after being struck by a club, the drag comes when the air pressure in front of
the ball is significantly higher than that behind the ball. Reduction of drag is
achieved by the dimples which brings the high-speed airstream closer to the
surface of the ball and the boundary layer changes from laminar to turbulent.
The most important drag exerted on a golf ball derives from air-pressure forces.
Because of the turbulence generated by the dimples, a golf ball is able to fly
about two and a half times farther than an identical but undimpled ball. Also, the
Re No is much lower for a dimpled ball (3 × 105) than one with a smooth sur-
face (Fig. 1.35).
In the course of this work, they (Moin and Kim 1997) came across a “Soviet”
study on tooth-like structures, called denticles, on the skin of sharks. These den-
ticles strikingly resembled riblets, a fact that has been interpreted as nature’s
endorsement of the riblet concept. Ultimately, however, it was the direct numeri-
cal simulation of turbulent flow along riblets that showed how they work. The rib-
lets appear to inhibit the motion of eddies by preventing them from coming very
close to the surface (within about 50 μm). By keeping the eddies this tiny distance
away, the riblets prevent the eddies from transporting high-speed fluid close to the
surface, where it decelerates and saps the sharks’ momentum, another example of
nature’s resourcefulness (Fig. 1.36).
The study Moin and Kim referred to was actually by Wolf-Ernst Reif (and
colleagues; Reif and Dinkelacker 1982; Reif 1985), a world expert on sharks,
who was my host as a Royal Society of London postdoctoral research fellow at
Tuebingen University in Germany. In Reif and Dinkelacker’s (1982) study at the
Max Planck Institute they had noted that the riblets on shark scales were oriented
in specific anterior–posterior directions. Just as with the golf ball they found that
riblets reduce drag by inhibiting the motion of eddies by preventing them from
coming close to the surface. Wolf-Ernst Reif told me that attempts were made to
transcribe the findings to aeronautical design in efforts to reduce fuel costs. The
engineered equivalent of the micro-riblets on the wing surfaces did in fact result
in fuel savings and would have left Wolf-Ernst and his colleagues financially very
comfortable. But, with his characteristic low-key philosophy he explained that the
42 1  Swimming and Flying in Vertebrates

Fig. 1.35  Drag on a golf
ball. a The drag comes
mainly from air-pressure
forces. This drag arises when
the pressure in front of the
ball is significantly higher
than that behind the ball.
b The only practical way of
reducing this differential is
to design the ball so that the
mainstream of air flowing by
it is as close to the surface
as possible. This situation
is achieved by a golf ball’s
dimples, which augment
the turbulence very close
to the surface, bringing the
high-speed airstream closer
and increasing the pressure
behind the ball. c The effect
is plotted in the chart, which
shows that for Reynolds
numbers achievable by
hitting the ball with a club,
the coefficient of drag is
much lower for the dimpled
ball. Modified after Moin
and Kim (1997)

fuel savings were unfortunately offset by the added costs of cleaning the aircraft’s
shark-like surface. Perhaps, the next great invention would be self-cleaning artifi-
cial surfaces.
Attempts to solve the problems of turbulence using supercomputers as we men-
tioned above have only just begun. Moin and Kim (1997) are confident that fluid
dynamicists will tackle problems involving higher Reynolds numbers and begin
learning some of the deep secrets expressed through the Navier–Stokes equations
(see Hewitt and Vassilicos 2005).
Thus far we have referred to flight through the air by animals and machines.
Many of the principles apply equally to vertebrate aquatic locomotion. In the next
section we will briefly look at swimming mechanisms in vertebrate animals.
1.6  Aquatic Locomotion 43

Fig. 1.36  Riblets. a V-Shaped grooves called riblets (above) have been found to inhibit the
motion of eddies, thereby lessening the drag they can exert on an aircraft’s wing. b A cross-
section of the airflow over the grooves (above, right) shows the vorticity contours—warm colors
are clockwise, and cool colors are counterclockwise. The arrows are velocity vectors for the flow
over the riblets. To be effective, the riblets must be very closely spaced, like phonograph grooves.
c The skin of a shark has tiny, tooth-like denticles (photomicrographs at bottom) that seem to
serve the same function as the riblets, lessening the drag on the creatures as they move through
the water. With permission of Parviz Moin, after Moin and Kim (1997)

1.6 Aquatic Locomotion

The forces acting on a swimming fish such as friction and form drag are very simi-
lar to those acting on birds as discussed in the preceding sections and will not be
repeated. Bernoulli’s theorem despite constraints already mentioned was generally
useful for lift-based propulsion in air. Water is denser than air and for a fish to
propel itself at a constant speed, the momentum conservation principle requires
that the forces and moments acting on it are balanced. The total thrust it exerts
against the water has to equal the total resistance it encounters moving forward.
Also, movement in water in vertebrates involves high Reynolds number for some
large fish ~105 and motion is dominated by inertial forces that frequently neces-
sitate calculations by Euler or Navier Stokes equations. As we saw above, the Re
44 1  Swimming and Flying in Vertebrates

No is frequently linked to the Froude number which is based on the speed–length

ratio of the object that is passing through the water, the greater the Froude number,
the greater the resistance. The Navier–Stokes equations as we already know are
formidable and ordinarily can be used under clear restrictions such as velocity and
pressure gradients (see Daniel et al. 1990).
Most fishes move by generating an undulating wave along their bodies to the
caudal fin that pushes water backwards, commonly referred to as body-caudal fin
(BCF) propulsion. Some fishes incorporate a partial lift-based mechanism to this
swimming mode while a few groups use an almost entirely lift-based propulsion.
We will briefly look at these modes of propulsion and in particular some of the
advances and modern techniques used in attempts to understand them.
Braun and Reif (1985) defined fish axial locomotion into broadly four swim-
ming categories, which are modified here to include lamnid sharks and cetaceans:
(1) Axial undulation (relatively slow swimming). The body is elongated. Almost
the entire length of the body from head to tail undulates to propel the animal for-
ward through the water. The caudal fin is generally poorly developed. Example,
the eel, Anguilla anguilla. (2) Axial subundulatory as in many slow-swimming
sharks, e.g., the ragged-tooth shark, Carcharias taurus in which undulations
occur in the last two-thirds of the body. (3) Axial suboscillation (relatively fast
swimming). The body may be near tear-drop or spindle-shaped. Undulations are
confined to approximately the last third of the body as in many carangid fishes
and some sharks. The caudal fin is generally well developed. A reasonably con-
stant angle of attack of the tail fin is achieved by flexion of the posterior body.
Examples, the fish, Naucrates ductor and tiger shark, Galeocerdo cuvier.
(4) Axial oscillation (very fast swimming) or thunniform swimming. The tear-
drop-shaped body is highly stiffened and forward thrust is generated by the tail
alone. A double-jointed caudal peduncle is almost undoubtedly essential to main-
tain a constant angle of attack of the tail fin. Examples, the fish, Thunnus thynnus,
white shark Carcharodon carcharias, bottlenose dolphin, Tursiops truncatus and
extinct Jurassic ichthyosaur, Stenopterygius quadricissus (Fig. 1.37).

Fig. 1.37  Gradation of
BCF swimming movements
from a Anguilliform,
through b Subcarangiform
and c carangiform to
d thunniform mode
(Lindsey 1978)
1.6  Aquatic Locomotion 45

We will start our discussion with the archetypal form of undulatory locomotion
as represented by the eel, A. anguilla.

1.6.1 Axial Undulatory Swimming (Anguilla)

James Gray (1933) traced successive frames of a cine film outlines of a young
eel swimming and superimposed them as if the eel were not moving forward. It
showed a series of sinuous waves passing from head to tail. In this type of move-
ment, which is called anguilliform (eel-like, from the generic name Anguilla for
eel), the waves cause each segment of the body to oscillate laterally across the axis
of movement. Each oscillating segment describes a figure-eight loop, the center of
which is along the axis of locomotion. It is these oscillations and the associated
orientation of each body segment that produce the propulsive thrust. The actual
propulsive thrust can be seen in Fig. 1.38.

Fig. 1.38  Outlines traced
from successive frames
of a cine film of a young
eel, Anguilla, swimming,
superimposed as if the eel
were not moving forward.
Numbers show outlines
at different points of the
forward undulatory motions
imposed at a single point.
From Gray (1933)
46 1  Swimming and Flying in Vertebrates

In the left side for instance, outline 3 is labelled at the crest of a wave and this
wave can be followed down the body till it reaches the tip of the tail in outline 9. As
the wave travels backward along the body each part of the body moves from side
to side. As any short segment moves to the left, its left side is inclined posteriorly.
The region where one side of the body is given a thick black outline is meant to
draw attention to this. Whether it is travelling to the left or the right, the body is
inclined in such a way that it deflects water posteriorly and tends to drive the fish
forwards (Newton’s third law), i.e., it moves sideways through the water at an angle
of attack, and a forward lift acts on it (James Gray 1933) (Figs. 1.37a and 1.38).
Azuma (2006) looked at the hydrodynamic forces and moments on a flexible
and deformable body from a mathematical perspective by simultaneously solving

Fig. 1.39  Swimming mode of eel, Anguilla. a Real mode. b Mathematical model based on

Eq. 5.22 (see Azuma 2006). Modified from Azuma (2006)
1.6  Aquatic Locomotion 47

the elastic equation and equations of motions at every part of the body. He noted
that usually by assuming nondeformable cross-sections the elastic equations can be
discarded. To introduce the effects of change of body configuration in the hydrody-
namic forces and moments, the velocity and acceleration of the fluid around every
part of the body must be known. This is done by dividing the body into n segments
along the longitudinal axis of the elongate body. Azuma found that by summarizing
and integrating the friction and reaction forces acting on the body segments dur-
ing linear and angular acceleration of the respective segments themselves and the
added masses of the fluid surrounding them, the total (inertial and hydrodynamic)
forces of the whole body can be mathematically calculated, and is comparable with
the real swimming mode of, e.g., the eel (see Azuma 2006; Fig. 1.39).

1.6.2 Axial Subundulatory to Axial Suboscillatory

Swimming (Most Fishes)

Particular attention is given in this section to the heterocercal tail because of a set
of peculiar hydrodynamic problems connected with it. The tail of most sharks has
an elongated upper lobe that differs from the externally symmetrical tail structure
common among bony fishes (Fig. 1.40).
A common interpretation for the unique morphology of the shark tail is that
the force such tails generate has components pointed in both anterior and dorsal
directions (Alexander 1965; Thomson 1976). The dorsal component of the force
is considered important in preventing fore-aft pitching of the animal, a phenome-
non which arises from the awkward position of the center of gravity relative to the
center of fluid forces acting on the body. The upward component was proposed to
be a consequence solely of the tilt of the lift force generated by the tail (Alexander
1965). The tilt requires a slight lateral bend to the tail. Daniel et al. (1990) note
that an alternative method that can yield sufficient upward force is leading-edge
suction, which acts perpendicular to the line of the leading edge, always maintain-
ing an upward component by pushing the back end of the animal up (Fig. 1.41).
The hydrodynamic purpose of this asymmetric tail shape has been a source of
much debate and will be considered in the light of new investigative techniques
below. Much of the design of the heterocercal tail involves the rate of momen-
tum ejected from the trailing edges of the tail and consequently the total thrust.
Understanding fish locomotion has in a similar way to understanding bird flight
been transformed through analyses of vortex production. Workers such as George
Lauder and colleagues have been at the forefront of attempts to quantify the three-
dimensional motion of the caudal fin, which they view as a critical component to
understanding caudal fin functions and to evaluate the impact that movement of
the fin has on the fluid (Figs. 1.42 and 1.43).
To quantify water flow patterns in the wakes of the caudal fin they used a
method called digital particle image velocimetry (DPIV) which involves small
48 1  Swimming and Flying in Vertebrates

Fig. 1.40  Heterocercal
caudal fin in the
suboscillatory-swimming
tiger shark, Galeocerdo
cuvier

Fig. 1.41  Diagram of flows
and forces associated with
leading-edge suction acting
of the heterocercal tail of
some elasmobranch. The
suction force arises from the
large pressure associated with
flows around sharp leading
edges. Redrawn from Daniel
et al. (1990)

reflective particles that are placed in the water and light from a laser is focused
into a light sheet which reflects off individual particles and is imaged by high-
speed video photography (similar to work by Spedding 1984, 1987). Wilga and
Lauder (2002, 2004) used DPIV analysis to investigate the vortex patterns of
leopard sharks, Triakis semifasciata and bamboo sharks, Chiloscyllium punctatum
swimming at 1.0 Ls−1, where L is total body length. They found that these sharks
generate strongly tilted vortex rings with a mean jet angle of approximately 30°
below horizontal during steady horizontal swimming. The corresponding angle
of the reaction force is much greater than body angle (mean 11°) and the angle
of the path of motion of the center of mass (mean, approximately 0°), here too,
strongly supporting the classical model of heterocercal tail function for steady
horizontal locomotion (Fig. 1.42). Vortex jet angle varies significantly with body
angle changes during vertical maneuvering, but sharks show no evidence of active
reorientation of jet angle relative to body angle, as was seen in the authors’ previ-
ous study on the function of the sturgeon tail. Hence, it is expected to generate lift
1.6  Aquatic Locomotion 49

Fig. 1.42  Schematic summary of two alternative models illustrating the forces acting on the
body of a shark during steady horizontal swimming. a Modified version of the classical model
(with data on body angle and pectoral fin function incorporated from Wilga and Lauder 2000) in
which the beating of the tail is proposed to generate an upward lift force (Ftail) that generates a
torque around the center of mass (shaded circle). Force on the water is directed posteroventrally
(Fwater), and an equal and opposite reaction force is directed anterodorsally, dorsal to the center
of mass (Freaction). Torques generated by the tail are countered by equal and opposite torques
resulting from lift forces produced by the body (Fbody), which has a positive angle of attack dur-
ing horizontal locomotion. The net upward lift forces are balanced by the weight (Fweight) of the
negatively buoyant shark. The pectoral fins do not generate lift during steady horizontal locomo-
tion (Wilga and Lauder 2000) and, hence, no forces are shown acting on these fins. b Modified
version of the model of Thomson (1976) (to include the authors’ previously published data on
shark body angle and pectoral fin function) in which the tail generates a reaction force that is
directed anteriorly through the center of mass. Modified after Wilga and Lauder (2002)

forces and torques which must be counteracted anteriorly by the body and pecto-
ral fins. In the lamnid sharks such as the white shark, Carcharodon carcharias,
given a conical head rather than highly flattened as in most sharks (body flatten-
ing is minimal), very large pectoral fins (Thomson and Simanek 1977) are reason-
ably considered to be the main source of lift and balance anteriorly.
The above method was extended to steady swimming analyses in chondrich-
thyians and ray-fined fishes (sturgeon and bluegill sunfish) with homocercal fin
morphologies (Lauder 2000) (Fig. 1.43). A functional analysis of the homocercal
tail of bluegill shows that the dorsal and ventral lobes do not function symmet-
rically as expected. Rather, the dorsal lobe undergoes greater lateral excursions
and moves at higher velocities than the ventral lobe. The surface of the dorsal
lobe also achieves a significantly acute angle to the horizontal plane suggest-
ing that the homocercal tail of bluegill generates lift during steady swimming.
50 1  Swimming and Flying in Vertebrates

Fig. 1.43  Schematic illustration of the vortex wake behind a bluegill sunfish swimming steadily.
Oscillatory motion of the tail is hypothesized to produce a linked chain of vortex rings (depicted
for simplicity as circular and enlarged relative to tail height) which are tilted to form an acute
angle to the XZ plane so that the central fluid jet through the ring has a posteroventral inclination.
The outside diameter of vortex rings measured using DPIV closely approximates the height of the
tail. The reactive force on the fish (FR) is thus oriented anterodorsally. Under this hypothesis, the
homocercal tail does not function in a manner consistent with the classical model, and generates
lift forces and torques that must be balanced by anterior forces generated by the orientation and/or
movement of the body and pectoral or pelvic fins. Modified after Linden and Turner (2004)

These movements are actively generated by the hypochordal longitudinalis mus-

cle within the tail. Based on this result, combined with DPIV flow visualization
data, the authors proposed a new hypothesis for the function of the homocercal
tail, i.e., generation of tilted and linked vortex rings with a central jet inclined
posteroventrally, producing an anterodorsal reactive force on the body which gen-
erates lift and torque in the manner expected of a heterocercal tail (Fig. 1.43).
The authors suggest that the application of new techniques to the study of caudal
fin function in fishes reveals a previously unknown diversity of homocercal and
heterocercal tail function, and that morphological characterizations of caudal fins
may not always accurately reflect in vivo function.
One unusual gain to the consequences of vortex shedding, not seen, e.g., in
birds, is that the caudal fin in sharks (many fishes) lies in the vortex wake gener-
ated by the dorsal fins and the energy lost in their shed vortices can be recovered
by the caudal fin and used to create more lift than if the caudal fin were oscillated
in an undisturbed flow (Yates 1983, citation in Daniel et al. 1990).

1.6.3 Oscillatory Swimming (Thunniform)

The oscillatory mode of swimming, hereafter thunniform, is the most specialized

and highly efficient method of swimming (Fig. 1.44). Most fishes move by gener-
ating an undulating wave along their bodies that extends to the tail fin that pushes
water backwards. However, we saw in Volume 1, that thunniform swimmers iso-
late this movement to the crescent-moon-shaped or lunate tail, which is much
1.6  Aquatic Locomotion 51

Fig. 1.44  Four thunniform
swimmers. a Large white
shark, Carcharodon
carcharias, based on
specimen TRA 92004 [fork
length (FL) 4.15 m]. Inset
shows photo of the enormous
liver of another large white
shark specimen RBDS 42
(FL 4.23 m; both Natal
Sharks Board); shark
outline drawn from
photograph. b Dolphin,
Delphinuscapensis. c Tuna,
Euthynnus affinis (Froese and
Pauly 2002). d Ichthyosaur,
Stenopterygius quadricissus,
SMF 457. Scale: a, inset
a, b = 50 cm; c = 10 cm;
d = 25 cm

taller, narrower and stiffer than that of other fish. This form of locomotion, thunni-
form, is quite exclusive and found in just four, phylogenetically unrelated, groups
of animals, tuna, lamnid sharks, a number of cetaceans and the extinct Jurassic
ichthyosaurs (mentioned in Volume 1). In all four groups the skin plays a signifi-
cant part in their locomotion, which will be discussed in Chap. 2.
Thunniform locomotion is a lift-based swimming mode as opposed to drag-
based and the principles of flight are very much as discussed in aerial locomotion
in the preceding sections. Here, we will briefly describe some of the distinctions
with respect to the fluid dynamics involved in thunniform locomotion.
The lunate tail of a thunniform swimmer looks like an aerofoil and it generates
lift the same way as an aeroplane wing does. Lift is created perpendicular to the
direction of fluid flow around the aerofoil shape, so in the thunniform swimmer,
the force produces forward thrust instead of upward lift. The fin is oriented at a
less oblique angle than the path the fin follows, and this difference is called alpha
(α), the angle of attack. The result is asymmetrical water flow over the fin, with
less pressure at the rear-facing surface than the forward-facing surface, producing
a forward lift force (Shadwick 2005).
The heterocercal tail of most sharks has been transformed to a near homocer-
cercal, lunate-shaped tail in tunniform sharks, perhaps most advanced in the mako,
Isurus oxyrinchus (Fig. 1.45a), and slightly less so in the white shark, Carcharodon
52 1  Swimming and Flying in Vertebrates

Fig. 1.45  Caudal fin of thunniform sharks. a Mako, Isurus oxyrinchus. b Characteristics based

on the tail of the white shark, Carcharodon carcharias, including pitching axis and sweepback
angle. c, d (Drawn from serial cross-sections of the dorsal and ventral caudal fin in the white
shark) Sections show consistent elliptical shape. Authors unpublished data

carcharias (Fig. 1.45b–d). In addition, the stiff caudal fin possesses a curved leading
edge and a sharp trailing edge (Fig. 1.45b–d). The caudal fin performs a combina-
tion of pitching and heaving motions, tracing an oscillating path as the fish moves
forward. There are very small lateral movements of the body, mainly concentrated
near the tail (Fig. 1.46). According to finite amplitude theory, thunniform swim-
ming characteristics do not differ significantly from the caudal fin small-amplitude
approximation in their implications—mean thrust is still produced only by the
downstream edge of the caudal fin, and in order to achieve maximum efficiency at
high speeds, the fish should minimize lateral excursions, reducing the problem to
1.6  Aquatic Locomotion 53

Fig. 1.46  Thunniform swimming. a Lateral view of caudal fin shape for thunniform swimmers,
showing span b, chord c, pitching axis position d, sweepback angle Λ and surface area Sc. b Trail
of an oscillating caudal fin showing amplitude A, wavelength λ, feather angle ψ, and attack angle
α of the fin. Modified after Sfakiotakis et al. (1999)

small-amplitude swimming. In addition to thrust obtained by the lift force there is

leading-edge suction, i.e., the action of the reduced pressure in the water moving
around the rounded leading edge of the caudal fin (Daniel et al. 1990).
The developed thrust and the propulsive efficiency in thunniform swimming
generally depend on the following parameters:
(1) The aspect ratio (AR) of the caudal fin AR = b2/Sc. High aspect ratio fins lead
to improved efficiency, because they induce less drag per unit of lift or thrust
produced. In thunniform swimmers, AR values range from 4.5 to about 7.2
(see Lingham-Soliar 2005c).
(2) The shape of the caudal fin, as it is defined by the sweepback angle and the cur-
vature of its leading edge. A curved leading edge is beneficial, because it reduces
the relative contribution of leading-edge suction to the total thrust, avoiding
boundary layer separation for high thrust values (Daniel et al. 1990) (Fig. 1.41).
(3) Fin stiffness. The benefit of a higher degree of stiffness is increased thrust
generation capability, with only a relatively small drop in efficiency
(Lingham-Soliar 2005b, c) (this will be discussed in detail in Chap. 2).
(4) The oscillatory motions of the fin. Most fast swimming fish swim with a fre-
quency and amplitude of tail motion that are within the optimal range of Strouhal
number of 0.25–0.4 fin (reviewed, Sfakiotakis et al. 1999) (see Fig. 1.14).
(5) A constant angle of attack of the caudal fin during oscillations, achieved by a
double-jointed or flattened (opposite to direction of caudal fin motions) caudal
peduncle (Fig. 1.47). This feature isolates the caudal fin from the anteriorly
placed locomotory musculature, necessitating connectivity with the caudal
fin via tendons that pass through the caudal peduncle and enter the caudal
(Fierstine and Walters 1968, reference in Chap. 2 (Fig. 1.47); Lingham-Soliar
2005b; Shadwick 2005).
In cetaceans, it is easier to see how lift is achieved in comparisons with birds
because of vertical heaving and pitching motions of the flukes comparable to the
54 1  Swimming and Flying in Vertebrates

Fig. 1.47  Caudal peduncles.
a White shark, Carcharadon
carcarias (dorso-ventrally
compressed). b Bottlenose
dolphin, Tursiops truncatus
(laterally compressed)

flapping motions of birds. On the downstroke flow over the fluke moves faster
over the top than the bottom. This velocity gradient develops some generation of
vorticity over the fluke which, when integrated over the length of the fluke, yields
some sectional circulation. Because the fluke has ends to it (it has finite span) the
circulation tends to roll off the tips yielding a “tip vortex” as found in birds and
aeroplanes (above). The very ends of the fluke therefore contribute little to the
overall forces that are generated. As we saw in birds, flukes of greater span have
proportionally less of their surface associated with the loss of circulation and pro-
duce, therefore, proportionally more force, i.e., greater span yields better lift per-
formance (Daniel et al. 1990).
An influential analysis of swimming in dolphins by Gray in (1936) revealed
that reported speeds of dolphins and then-known estimates of muscle power were
inconsistent. Gray estimated that energy levels appeared much less than that
needed for a fast swimming dolphin. This was dubbed Gray’s Paradox which
triggered numerous studies to determine swimming and energy reducing mecha-
nisms. It was instrumental in my own studies in the white shark to find energy
saving mechanisms, which will be discussed in Chap. 2. Research on the integu-
ment and control structures of marine mammals by Ann Pabst and colleagues have
prompted proposals that swimming animals such as dolphins may possess elastic
1.6  Aquatic Locomotion 55

mechanisms that might reduce energy expenditure. For instance she suggested that
collagen fibers in the caudal peduncles of dolphins (Pabst 1996), describe helical
angles greater than 60°, and may act to store and release strain energy when these
vertebrate cylinders bend in swimming. Perhaps more controversial, Pabst pro-
posed that if dolphins possessed appropriately tuned springs, elastic strain energy,
they could double their force output with no increase in the rate of oxygen con-
sumption and decrease their metabolic cost with increased speed and force out-
put. Findings, thus far have been inconclusive given opposing results by different
groups of workers and different analytical methods. However, one form of pos-
sible drag reducing method among some species of thunniform dolphins involves
a form of swimming known as porpoising, which will be briefly mentioned below.

1.7 Energy Saving Devices in Vertebrate Swimming

1.7.1 Reverse Von Karman Vortex Street

We mentioned earlier in the discussion on vortex flow that the frequency f is

referred to as the “unsteadiness” of the system. Generally, the periodic effect is
enforced by the boundary conditions or the initial conditions. In other situations,
the physics itself initiates or forces periodic instability. We saw above that the
flow around a cylinder at first looks like a symmetrical situation. And indeed in a
low Reynolds number it is a steady state (Lissaman 1983). However after a cer-
tain value of Reynolds number, vortices are created in an infinite parade and this
phenomenon is called Von Karman vortex street (see Figs. 1.20 and 1.48). These
vortices are created in a nonsymmetrical way and hence create an unsteady situ-
ation. In BCF swimmers, as in bird flight, there is an interesting array of vorti-
ces that conform to the observed phenomenon, named reverse von Kármán street,
which appears to be tightly associated with thrust generation (Cheng and Chahine
2001). Bergmann et al. (2005) found in rotary sinusoidal control for the circular
cylinder wake in the laminar region (Reynolds number = 200), that partial con-
trol restricted to an upstream part of the cylinder surface may increase consider-
ably the effectiveness of the control. Indeed, a maximum value of relative mean
drag reduction equal to 30 % is obtained and the significant thrust force that is

Fig. 1.48  The Karman street generates a drag force in a Bluff body (or streamlined, see
Fig. 1.18b). b The wake of a swimming fish has reverse rotational direction, associated with thrust
generation
56 1  Swimming and Flying in Vertebrates

locally generated in the near wake corresponds to a reverse Kármán vortex street
as commonly observed in fish-like locomotion or flapping wing flight.
Research shows that a variety of fish and cetaceans swim with a frequency
and amplitude of tail motion that are within a narrow range of Strouhal numbers
(Fig.  1.14; discussed above in unsteady, oscillating flow problems in aerial flight
in which the frequency of the oscillation is important) minimizing energy lost in
the wake for a given momentum and increasing efficiency. A more detailed three-
dimensional analysis reveals that the vorticity in the wake is actually concentrated
in a series of strong counter-rotating elliptical vortices, linked together as vortex
loops, (Nauen and Lauder 2002), consistent with findings by mechanical engineers.
Experimental studies and numerical simulations suggest that fish can actively
manipulate vortices encountered in their environment or produced by themselves,
to reduce energy losses in steady swimming, increase thrust when accelerating
and achieve high agility in maneuvering. Research shows free vortices forming
well ahead of the tail and travelling along the body to reach the caudal fin, which
manipulates them and repositions them in the wake (Zhu et al. 2002). It has been
demonstrated, that fish use two different modes of vorticity control in straight-line
swimming to optimize performance by utilizing body-generated vortices (Fig. 1.48).
(1) The constructive mode employs a vortex reinforcement scheme, whereby the
oncoming body-generated vortices are repositioned and then paired with tail-
generated same-sign vortices, resulting in a strong reverse Kármán street, and
hence increased thrust force (see Fig. 1.48).
(2) The destructive mode, in contrast, employs a destructive interference scheme,
whereby the body-generated vortices are repositioned and then paired with
tail-generated opposite sign vortices, resulting in a weakened reverse Kármán
street, thus extracting energy from the oncoming body-shed vorticity and
increasing swimming efficiency.

1.7.2 Diamond-Shaped Shoals

Birds utilize the vortex flow from other birds in a flock by flying in V formation
(also see Chap. 5). Similar effects can be observed in schools of fish, where fish
organize themselves in an elongated diamond-shaped pattern (Fig. 1.49) to exploit
each-other’s vortex wake. The advantage is greater when the fish in the same col-
umn swim in antiphase with their neighbors. Estimates show that schooling can
save up to 20 % of energy (Sfakiotakis 1999).

1.7.3 Porpoising

Porpoising is the popular name for the high-speed motion of dolphin schools in
which long, ballistic jumps are alternated with sections of swimming close to the sur-
face (Weihs 2002). Azuma (2006; Figs. 1.50 and 1.51) assumed that if the dolphin
1.7  Energy Saving Devices in Vertebrate Swimming 57

Fig. 1.49  Plan view of a horizontal layer of a fish school, showing its diamond-shaped building
block structure. The configuration is described by the wake width A, the vortex spacing L, and
the lateral distance H amongst fish of the same column. Adapted from Weihs and Webb (1983)

Fig. 1.50  Porpoising. Acceleration in the water initiates with the minimum speed Vmin at time
t = 0 and ends with a maximum speed Vmax at time t = rT where T is a time period of this pro-
cess, Vo is steady velocity, and sT the minimum value of Vmin within the time, r is time in the
water with constant forward acceleration. Modified from Azuma (2006)

swims with a constant forward acceleration α during time fraction r and spends
the rest of the time by jumping into and flying through the air, which is much less
dense than water and by penetrating the water (added mass) for acceleration follow-
ing deceleration, then it is possible to save power (two-phase model). He based this
largely according to Au and Weihs (1980). Azuma specified in general terms (1) the
time fraction for the acceleration r should be small as rmin, (2) the body shape must
be slender in order to make the added mass and drag area small, and (3) the dissi-
pated energy for the splash must also be small (Fig. 1.50).
Weihs (2002), since the earlier publication (Au and Weihs 1980), found as a
consequence of several later studies that documented porpoising behavior at high
speeds, that the porpoising behavior was more complex than previously assumed.
He considered that that dolphin leaps were interspersed with relatively long
58 1  Swimming and Flying in Vertebrates

Fig. 1.51  Dolphins porpoising. Photo permission of Lloyd Edwards

swimming bouts, of about twice the leap length. The hypothesis is that dolphins
use a combination of leaping and burst and coast swimming. He consequently
proposed a three-phase model for porpoising. The first phase is when the dolphin
leaps out of the water at a speed Uf, which is the final speed obtained at the end of
the burst phase of burst and coast swimming. The leap is at constant speed and so
the animal returns to the water at Uf, goes to a shallow depth and starts horizontal
coasting while losing speed, till it reaches Ui. At that point it starts active swim-
ming, accelerating to Uf. It then starts the next leap. Energy saving, given different
swimming potentials (speed) in individuals, can be as high as 33 % and as low as
18 %. So the expected saving due to porpoising at 7 m/s (14 knots) was considered
to be somewhere between these two values, i.e., around 25 %.
The next chapter leads directly on from here with the role of the integument in
vertebrate aquatic locomotion. Aerial flight will continue in Chaps. 3–5.

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Chapter 2
Vertebrate Swimming

As we saw in the chapter on fishes in Volume 1, their success is reflected by the

fact that the total number of fish species comprises more than half of the total
number of approximately 55,000 recognized living vertebrate species. We ended
Chap. 1 with a brief look at certain advances in our understanding of the hydrody-
namics involved in vertebrate swimming. We will now look at the role the integu-
ment plays in the different swimming categories mentioned in Chap. 1 (Fig. 2.1)
including special reference to the outer and inner dermis of sharks, a group with
which we will start this chapter because it saw the first seminal research in this
area among vertebrates. This will also be a suitable prequel to the group of fast
swimming marine vertebrates, the thunniform swimmers.
Most sharks use what may be described as an in-between mode of axial undula-
tory (anguilliform) and sub-oscillatory swimming. Some of the important devel-
opments with respect to the swimming dynamics were discussed in Chap. 1 and
will not be dealt with any further here other than by way of comparison. Instead,
we will stick to the two extreme swimming modes below, anguilliform and thun-
niform locomotion, and the crucial role that the superficial dermis and the deeper
underlying dermis plays in them. We will start with the role of the superficial der-
mis, i.e., that region that gives rise to the scales in fishes (Volume 1). The scala-
tion of sharks is an advanced example of how fish scales contribute to locomotion
as seen through important research in the last 30 plus years. Further on we will
see how the underlying dermis plays a similarly critical role in some of the fastest
marine vertebrates in the oceans, albeit not involving scales, but rather a crossed-
fiber collagenous architecture.
As shown in Volume 1, fish scales afford protection and help in hydrodynamic
streamlining. However, during the last quarter of the 20th Century it was found that
placoid scales may play a very specific role in the locomotion of sharks in control-
ling turbulence (discussed in Chap. 1). Here we look at the morphological character-
istics that enable this function.

© Springer-Verlag Berlin Heidelberg 2015 61

T. Lingham-Soliar, The Vertebrate Integument Volume 2,
DOI 10.1007/978-3-662-46005-4_2
62 2  Vertebrate Swimming

Fig. 2.1  Differences in body profiles in an eel and three shark species reflecting different
­lifestyles and swimming potentials. a Eel, anguilliform. b Carcharias taurus, sub-anguilliform.
c Galeocerdo cuvier, sub-carangiform or sub-oscillatory. d Carcharodon carcharias, thunniform
or oscillatory

The scale crown has a very distinctive morphology that varies considerably,
not only across the body but also among species (Fig. 2.2). The majority of scales
on faster swimming sharks such as the shortfin mako, Isurus oxyrinchus, black-
tip shark C. limbatus, and silky shark Carcharhinus falciformis have a series of
parallel riblets (also termed micro-ridges, ridges, or keels) that run in an anterior–
posterior direction, often terminating in cusps on the trailing edge of the scale
(Motta et al. 2012). As mentioned in Chap. 1, Wolf-Ernst Reif and colleagues first
proposed in the early 1980s that the highly specific orientation of these riblets and
2  Vertebrate Swimming 63

Fig. 2.2  A placoid scale. a Lateral, dorsal, and ventral views of a placoid scale (dermal denticle)
from a 135.5 cm TL (total length) female blacktip shark Carcharhinus limbatus. Morphometric
measures are indicated on each view (magnification 200X). Dorsal and anterior is indicated for
the upper, lateral view. B base; BL base length; BW base width; C crown; CL crown length; CW
crown width; N neck; RS riblet spacing. b and c From the B2 regions of the body respectively
(see d). d Flank region (oval) and other parts tested. Modified from Motta et al. (2012)

consistent height and spacing especially in fast swimming sharks have a hydro-
dynamic role, the understanding of which has since been supported by the use
of supercomputers. The longitudinal riblets reduce drag because they impede the
fluctuating turbulent crossflow near the wall, and in this way reduce momentum
transfer and shear stress. Moin and Bewley (1994) and Moin and Kim (1997)
showed by simulations of trajectories of marker particles in a turbulent water
flow between parallel plates exactly how they work. The riblets appear to inhibit
the motion of eddies by preventing them from coming very close to the surface
(within about 50 μm). By keeping the eddies this tiny distance away, the riblets
64 2  Vertebrate Swimming

prevent the eddies from transporting high-speed fluid close to the surface, where it
would decelerate and sap the animals momentum (Chap. 1, Fig. 1.36).
In a morphological study of shark scales, Philip Motto and colleagues (2012)
have shown specialization of scale morphology and patterns in the flanks of the fast
thunniform shark, the short fin mako, Isurus oxyrinchus and the non-thunniform
black tip shark, C. limbatus, which enables a new hypothesis on how reduction of
drag might be achieved.
Motta et al. (2012) sampled scales in regions along the flanks of both sharks
(Fig.  2.3). The placoid scales of the shortfin mako and blacktip sharks were
anchored in the stratum laxum of the dermis with no obvious direct connection to
the fibers of the stratum compactum. The attachment fibers of the scales in both
species were almost exclusively collagen.
The authors found that the shortfin mako shark has shorter scales than the
blacktip shark. The majority of the shortfin mako shark scales have three longi-
tudinal riblets with narrow spacing and shallow grooves (Fig. 2.2b, c). In com-
parison, the blacktip shark scales have five to seven longitudinal riblets with wider
spacing and deeper grooves (Fig. 2.2a). The relative riblet heights in the black tip
were similar to those of the shortfin mako shark. The most significant finding is
that I. oxyrinchus, one of the fastest swimming marine vertebrates, has a region of
highly flexible scales along the flank with erection angles equal to or greater than
50°. This is in contrast to the scales on the other regions of the shortfin mako’s
body as well as all the scales of the black tip shark C. limbatus, which are not
as erectable. The authors propose that the combination of a long crown length to
short base length in I. oxyrinchus facilitates pivoting and erection of flank scales,
which plays a key role in drag reduction that they hypothesize is passively driven
by localized flow patterns over the skin.

Fig. 2.3  The cuticle of the worm, Ascaris lumbricoides, showing collagen fiber layers. After
Clark (1964)
2.1  The Deeper Dermis of Marine Vertebrates 65

2.1 The Deeper Dermis of Marine Vertebrates

2.1.1 Non-thunniform Sharks

With respect to the next section on the dermal fibers, although seemingly incon-
gruous we will start with the more advanced form of locomotion, the thunni-
form mode, first, given that in the modern groups they evolved last. This can be
explained by the chronology of the history of research and discoveries and, to a
lesser extent, by the fact that the thunniform mode of swimming is in fact very old,
having first evolved in the ichthyosaurs over 200 million years ago (Lingham-Soliar
1999, 2001; see Volume 1).
Perhaps the most significant study, which enabled much of the work in the area
that followed, was that by Philip Motto. Motta (1977) investigated the dermis of
a number of shark species by dissections and light microscopy. What he discov-
ered was seminal—in several regions of the shark he found that the skin was com-
prised of multiple layers of oppositely oriented collagen fibers (Motta 1977), in
some shark species as many as 45 layers of the dermis. While Motta thought that
these layers of stiff collagen fibers served, at least in part, for protection and as
an anchor for the musculature, he nevertheless asked some critical questions as
to why the skin tension remains constant during each stroke of the tail and why
the fibers do not buckle on the concave size of the bending. In fact he had touched
upon the most important role of the fibers, which had never been described in a
vertebrate animal before and so their function was very much a mystery. To under-
stand the function of these cross-helically wound fibers one needs to go back in
time to the late 1950s to a study by RB Clark and JB Cowey on perhaps the most
unlikely of animals for an answer to our mystery, the humble nemertean and tur-
bellarian worms. So important and influential was that study that we will break
with the objective of this book of describing purely vertebrates, and in particular
their integumentary systems, to describing the structure and biomechanics of the
integument of these invertebrate animals.
In an elegant study incorporating both the biological and mathematical sci-
ences, Clark and Cowey (1958) described how fibers that were largely inextensible
in nemertean (from Greek myth, Nemertes, a sea nymph) and turbellarian worms,
yet enabled the animals to extend and compress at will. The authors saw a com-
plex problem that had to be resolved in these animals—the fibers enabled the body
maximum stiffness and yet at the same time allowed the body all the flexibility
necessary for the animal’s vital movements in their locomotion. Put another way
the inextensible fibers in the integument of animals enabled both stiffness and flex-
ibility. This sounds like the stuff of which riddles are made. Indeed, in Greek myth
the classic riddle was posed by a foul creature, the Sphinx, with a terrible death to
those who failed to answer it. It might have fared better and had a very different
result had it asked Oedipus instead, “What fibers are at once both extensible and
inextensible?” Oedipus would undoubtedly have failed to answer it and have been
promptly throttled and devoured by the creature and it would have saved a whole
66 2  Vertebrate Swimming

lot of the messy business that followed. Instead Oedipus did answer the riddle
posed by the Sphinx, resulting in its own destruction (see Sophocles’ play (~430
BC)).
Yet, it was the answer that Clark and Cowey (1958) discovered and it involved
a beautiful combination of biology and mathematics. The idea that hydrostatic
pressure in many worms plays a role in invertebrate support and locomotor sys-
tems had been explored by many other researchers but it was not until the study by
Clark and Cowey that the actual mechanism of how this was incorporated into the
animal’s locomotion was discovered. They found that the integument in turbellar-
ian and nemertean worms was composed of regularly disposed inextensible fibers
arranged in layers in alternate left- and right-handed geodesic helices extending
around the body of the animal (Fig. 2.3 and Frontispiece).
The model shows the worm as a fluid-filled tube stiffened by helical wrappings
of inextensible fibers (Fig. 2.4a). Figure 2.4b show the section cut along the top
and laid open, with just a single fiber represented. Although the fibers themselves
are inextensible, changes of length of the body or parts of the body are permitted
by a change in the angle of the crossed fibers exactly as the intersecting elements
in a lattice or trellis. They demonstrated that in considering the fiber system alone
there is a simple relationship between the inclination of the fibers to the longitu-
dinal axis and the length of the system (Fig. 2.4c). In a cylindrical worm, e.g., as
the inclination of the fibers changes so does the total volume the system can hold
change, i.e., the volume varies according to the formula
V = D3 sin2 ϑ cos ϑ/4πr
With extension, the segment’s diameter and fiber angle both decrease; conversely,
with segment shortening the fiber angle and diameter increase. If the segment
maintains a circular cross-section, its volume, V, will vary, according to the curve
in Fig. 2.4c. V decreases toward zero as θ goes to 0° (a long, thin thread) or 90° (a
flat disc), and it peaks at an intermediate angle of 54.74°. But an extensible worm,
in most cases, does not change volume, so it cannot follow the curve. However,
according to Clark and Cowey, “The system can always contain less than this vol-
ume if the cross-section is elliptical instead of circular” allowing a worm to adopt
a flattened, elliptical cross-section as it changes length along a horizontal line of
constant volume, as shown in Fig. 2.4c. The extremes of shortening and length-
ening occur where this line intersects the V versus θ curve and only here will the
worm be circular. The greatest degree of flattening occurs when θ = 54.74°, also
the angle where circumferential and longitudinal stresses in a pressurized cylin-
der balance (Wainwright et al. 1976). This is probably the reason why Clark and
Cowey observed that a worm fully relaxed by anesthesia adopts a length where
θ  ≈ 55°. In theory, a flatter worm should have a higher range of extensibility,
because of its lower position on the plot in Fig. 2.4c, i.e., there is a greater range of
lengths possible between the extremes bounded by the V curve.
Clark and Cowey (1958) stated that the helical bounding systems might
be “widespread, if not general, in soft bodied, worm-like animals” but at the
time even they had no way of anticipating the impact their findings would have
2.1  The Deeper Dermis of Marine Vertebrates 67

Fig. 2.4  The cuticle of the worm, Amphiporus lactifloreus. a A unit length segment of a model
worm, represented as a cylinder (radius r, length l) wrapped by one full turn of an inextensible
fiber having length D; fibers with the opposite sense are omitted. The fibers follow the course of
geodesics (i.e., the shortest line between two points on a curved surface). b The unit length in A
cut along the top and laid open. c A curve representing the volume contained θ by the cylindrical
fiber system at different fiber angles θ, showing the maximum occurring at 54.74°. Segments at
low θ are long and thin; at high θ they are short and fat. The horizontal line represents the con-
stant volume of the nemertean Amphiporus lactifloreus. It intersects the curve at F and G, which
represent the maximum and minimum lengths, respectively. After Clark and Cowey (1958)

in biology, which extends to vertebrates as we will see in studies below (see

Frontispiece).
In their book Mechanical design in organisms, Wainwright et al. (1976) pro-
moted Clark and Cowey’s (1958) model as a design principle in engineering and
in nature, although solely in invertebrates. They recorded a number of studies that
demonstrated the mechanical importance of the integument in a variety of inver-
tebrates from insects to arthropods and mollusks. But it was not until soon after
68 2  Vertebrate Swimming

Philip Motta’s (1977) study on the cross-fiber structure in the dermis of sharks was
published that Wainwright and colleagues (1978) were able to see that the design
principle discovered in worms and thus far confined to invertebrates, might be
equally relevant to large vertebrate animals.
Wainwright et al.’s (1978) study published in the journal Science showed that
during slow swimming the shark bent its body in left- and right-handed bends
of 38 cm radius whereas during bouts of fast swimming tighter bends of 20 cm
radius were produced and concomitantly the pressure rose from about 20 and
35–200 kN m−2 during each tail beat, on both the concave and convex sides of
the fish. The body stiffness achieved coincided with the angles made by the alter-
nating left- and right-handed fibers with the long axis of the shark as seen in
Philip Motta’s study (Fig. 2.5a). This in fact could now be seen to conform with
a common engineering principle with respect to thin-walled cylinders in which
torsional stiffness can be enhanced by struts aligned at 45° to the cylinder’s long
axis (see Chap. 1) and that this was exactly how torsional stiffness was achieved in
the sharks, i.e., collagen fibers in the skin wrapped at 45° to the body’s long axis
(Motta 1977).
The authors tested the shark skin in a biaxial testing machine and found that
while pulling it longitudinally and holding a constant circumferential stress of
0.3 MN m−2, a great longitudinal extension of the skin occurred (Fig. 2.5b, lower
curve). When they held circumferential stress at the fast swimming value of
2.8 MN m−2 the stress in the unstretched skin at zero extension increased 13-fold
and a given longitudinal extension required very much more stress than it does in
the lower pressured slower swimming situation (Fig. 2.5b, upper curve).
To assess the torsional stiffness conveyed to the shark’s body by the skin the
authors performed load tests on the caudal peduncle with the skin intact and cut.
They showed that the skin accounts for half the passive resistance to twisting
despite the small percentage thickness (6 %) compared to the muscles. In ­addition,
and this is important, unlike in the experiments on worms, this resistance was
obtained in a dead shark, i.e., without hydrostatic pressure. Clearly, as the authors
stated, the values obtained would be even higher in a living pressurized shark but
nonetheless a high degree of resistance was possible without hydrostatic pressure
(we will see situations with reduced internal pressure in Chap. 5). Wainwright
et al.’s (1978) findings are extremely important and set the bench mark for future
studies (including my own) on the biomechanics of the fiber structure of the
­vertebrate integument. The functional findings of their study may be summed up as:
(1) Skin stiffness and the energy stored in shark skin depend on the amount by
which the skin is prestressed by internal hydrostatic pressure at the time that it
is extended.
(2) The locomotory muscles of sharks as well as each muscle segment attaches to
the skin over an area similar to that by which it attaches to the backbone and
thus the skin acts as a tendon that increases the mechanical advantage of the
locomotory muscle.
2.1  The Deeper Dermis of Marine Vertebrates 69

Fig. 2.5  Helical fiber system. a Outline of a lemon shark (139 cm long) with some helical fiber
angles indicated. b Longitudinal stress-extension behavior of skin from the lemon shark shown in
Fig. 2.1. (Lower curve) The specimen was first stressed to 0.3 MN m−2 to simulate conditions in
slow swimming. The crosses (x) are longitudinal stresses predicted by the relation: the square of
the tangent of the fiber angle is equal to the ratio of the circumferential stress to the longitudinal
stress. (Upper curve) The specimen was first stressed to 2.8 MN m2 to simulate conditions in
fast swimming. Rising and falling arrows indicate loading and unloading, respectively. Modified
from Wainwright et al. (1978)

(3) If the shark’s skin is to transmit forces of contracting muscles to the tail, at rest
the muscles have the same length and cross-sectional area, and the fibers in the
skin make a 60° angle with the fish’s long axis. Internal pressure is low and
so is skin stiffness. To bend sharply as in fast swimming, the muscle on one
side shortens and increases in cross-sectional area and girth. This causes fib-
ers in the skin overlying the contracting muscles to increase their angle. The
fiber angle controls the change in girth per unit change in length of the skin in
concert with the surface of the contracting muscle. The changes in fiber angle
imposed by the muscle cause the skin to remain taut in containing the muscle
volume and to avoid wrinkling or loss of tension on the concave side of the fish.
70 2  Vertebrate Swimming

(4) Since skin stiffness is high, tensile forces applied to it are transmitted by it
from the head to the tail. Since the backbone resists compressive changes in
the fish’s body length, contracting muscles pull on one side of the head and
tail causing the fish to bend rather than to shorten.
The studies on shark dermal fiber structure paved the way for studies on the fastest
swimmers in the oceans, the thunniforms.

2.1.2 Thunniform Swimmers

The mathematician Sir James Lighthill (1975) categorized four groups of marine
vertebrates as thunniform swimmers, tuna, lamnid sharks, dolphins and the extinct
ichthyosaurs. Despite their disparate phylogenies, i.e., tuna and lamnid sharks are
bony and cartilaginous fishes respectively, dolphins are mammals and ichthyosaurs
are reptiles (see Chap. 1 and Volume 1), their apparent similarities have fascinated
biologists and engineers alike for many years both in terms of biomechanics as
well as the power of convergent evolution. However, convergent evolution in these
animals was initially based on one criterion alone, body shape (including the cau-
dal fin). It was through morphological investigations that at first were somewhat
removed from questions of convergent evolution that we began to see deeper sim-
ilarities in these animals. Among the four thunniform groups we will start with
tuna.

2.1.2.1 Tuna Dermis

Following from Motta (1977) and Wainwright et al. (1978), the next breakthrough
with respect to dermal fibers among fast vertebrate swimmers was in tuna, from
which the thunniform swimming mode takes its name. Tuna arose some 40–60
million years ago at about the same time as the two other groups of extant
thunniform swimmers, lamnid sharks and dolphins, possibly as a consequence of
­selection pressures for fast swimming as an effective part of predation at this time.
Mary and John Hebrank (1986) investigated the skin of two species of tuna-like
fishes belonging to the family Scombridae, the Norfolk spot, Leiostomus xanthu-
rus, and the skipjack tuna, Katsuwonus pelamis (officially these do not belong
to the genus of tuna, i.e., Thunnus, although they are commonly referred to as
tunas (the skipjack most resembling them), they are scombrids. These are highly
streamlined fish with a teardrop-shaped body and high aspect ratio tail (Fig. 2.6).
The muscle forces that are anteriorly located are transmitted via the extremely
­narrowed caudal peduncle via a system of tendons (Fig. 2.7).
They found that in the Norfolk spot the skin is composed largely of a crossed-
helical array of collagen fibers. Over most of the body of the fish these are ori-
ented at angles of 45–80° with the long axis of the fish. The skin of K. pelamis
2.1  The Deeper Dermis of Marine Vertebrates 71

Fig. 2.6  Scombrids. a Skipjack tuna, Katsuwonus pelamis. b Norfolk spot, Leiostomus xanthurus

Fig. 2.7  The tendons connecting to the caudal fin has arisen convergently in the mako shark and
tuna from the backward-pointing cone of connective tissue. Modified from Donley et al. (2004)
72 2  Vertebrate Swimming

also contains a crossed-helical array of collagen fibers, although fewer fiber lay-
ers are present and fiber angles are generally in the range of 55–75°. To test the
function of the fiber structures the authors performed uniaxial stress-strain tests on
both species of tuna. They show that for both species the skin is most extensible
in the longitudinal direction. For the Norfolk spot, the skin is stiffer in the direc-
tion of the fibers than in the circumferential direction, but for the skipjack tuna,
the skin is of about the same stiffness in the circumferential direction as it is in the
direction of the fibers.
The authors’ results of biaxial tests of Norfolk spot and skipjack demonstrated
that contraction of one side of the skin does not occur concomitant with extension
of the orthogonal direction. Without this contraction tension cannot be transmitted
by the skin down the length of the fish during swimming movements. This demon-
strates that the skin of the spot and the skipjack do not behave as simple crossed-
fiber systems, and are therefore incapable of transmitting forces down the lengths
of these fishes or of acting as “external” tendons as found in sharks (above). The
latter function is because a force applied to the skin can generate a greater bending
moment than the same force applied near the backbone, the mechanical advan-
tage of the axial musculature can be enhanced by pulling on skin that is capable of
transmitting forces down the length of the fish (Wainwright et al. 1978). Hebrank
and Hebrank suggested that this might be because sharks and eels (Hebrank 1980;
see further on) are considered to be relatively primitive fishes and that both swim
using fairly large amplitude waves of lateral undulation, whereas in their study of
the structural features and mechanical properties of the integuments of two more
advanced teleosts, the Norfolk spot and the skipjack tuna, they exhibit relatively
small amplitude waves of lateral undulation and therefore the skin does not func-
tion as a giant tendon. Instead, for the spot and the skipjack, the crossed-fiber
array of collagen seems to function primarily to keep the tough exterior surface of
the fish smooth and free of kinks during swimming movements. A smooth surface
is an important factor promoting hydrodynamic performance.
Hebrank and Hebrank (1986) also showed that the skin overlying the caudal
peduncle (the very narrow region just anterior to the caudal fin) of the skipjack
tuna is wrapped by dermal fibers at very steep fiber angles. This reinforcement is
not seen in fishes that lack terminal tendons, such as Norfolk spot and eel (Hebrank
1980). Deep to the dermis, the tuna peduncle is also reinforced with a thick subder-
mal sheath, formed by myoseptal collagen fibers of caudal posterior pointing arms.
We will consider this function further in the other thunniform swimmers.

2.1.2.2 Dolphin Dermis

Our understanding of the role the skin plays in dolphin locomotion has been
largely due to Ann Pabst at the University of North Carolina at Wilmington (Pabst
1996a, 2000). As mentioned, dolphins show the classic case of convergent evolu-
tion with tuna, lamnid sharks and ichthyosaurs. However, unlike tuna and sharks,
but like ichthyosaurs (see further on), dolphins are secondarily adapted to aquatic
2.1  The Deeper Dermis of Marine Vertebrates 73

locomotion. As cetaceans (whales, dolphins and porpoises) they are distinctive

from the other three groups in having arisen from terrestrial mammals. Part of that
distinctiveness is reflected in their propulsion through the water—their caudal tail-
stock and caudal flukes oscillate dorsoventrally, reflecting their terrestrial origins
and locomotion, rather than laterally (side-to-side) as in the other three groups
(even early land reptiles employed the side-to-side locomotion). Historically it
was shown that the axial muscles, arranged in longitudinal tracts transmit forces
via connective tissue ‘‘fabrics’’ of aponeurotic tendon sheets, and horizontal septa.
Ann Pabst demonstrated that the skin played an important role in force transmis-
sion, i.e., that surrounding the axial musculature is a robust collagenous membrane
which she named the subdermal connective tissue sheath (SDS). The SDS lies just
deep to the blubber layer, is firmly anchored to the vertebral column and is formed
by layers of collagen fibers that describe alternating right- and left-handed oblique
angles relative to the long axis of the body, just as in the other animals described
above (Figs. 2.8, 2.9).
Significantly, Ann Pabst found that the dolphin was modeled along the lines of
a fiber-wound, thin-walled pressurized cylinder. With respect to mechanical func-
tions, it was based on its cylindrical shape, a wall less than one tenth the radius in
thickness, reinforced by two sets of fibers describing equal left- and right-handed
fibers in alternating layers and, uniformly loaded by internal pressure. While elas-
tin fibers were found associated with the SDS the predominant protein fibers were
collagen. It was also found that fiber orientations, fiber diameters, and fiber lay-
ers and sheath thickness vary as a function of their position along the longitudinal

Fig. 2.8  A scombrid myomere is a block of muscle, complexly folded into anterior pointing
arms (APA), posterior pointing cones (PPC), and anterior pointing cones (APC). Each myosep-
tum is reinforced by two populations of collagen fibers—one wrapped circumferentially, the
other longitudinally. Both populations of fibers coalesce in the main horizontal septum (the
connective tissue structure that lies along the lateral midline and that connects the skin to the
vertebral centra; not pictured here) to form obliquely oriented tendons. The circumferential fib-
ers form anterior oblique tendons (AOTs), the longitudinal fibers form posterior oblique tendons
(POTs). (BB represents backbone; TAA represents the triangular attachment area, the connection
between the myomere and skin). Modified from Pabst (2000)
74 2  Vertebrate Swimming

Fig. 2.9  The dolphin longissimus muscle and the superficial tendon. Skeletal elements are
shown as a series of cross-sections. a the longissimus, and its caudal extension, the extensor cau-
dae lateralis. Cross-sectional shape of the muscle is indicated at various points, and arrows indi-
cate the approximate angle of muscle fascicles. b The superficial tendon. Thick transverse lines
indicate cross-sectional shape of the tendon. These tendon fibers change their orientation as they
enter the subdermal connective tissue sheath (SDS); only the tendons that join the SDS on the
ipsilateral side of the body are pictured here. These fibers approach the dorsal midline, become
woven into the SDS and change their trajectories to insert on more caudal vertebrae. By permis-
sion of Ann Pabst (2000)

axis of the dolphin body. With respect to fiber angle, for instance, the forward and
backward leaning fibers at the thorax are approximately equal but as one moves
caudally the forward leaning fibers remain fairly constant but the backward lean-
ing fibers become progressively steeper till near the insertion of the flukes they
approach 90°. The sheath also becomes thicker caudally with an increase in the
number of fiber layers. She also found that although there is a critical angle of 60°
(McNeill Alexander (1987) demonstrated the functional role of the different fiber
angles) at which the fibers may be strained and store energy, that when the animal
bends this may differ in dolphins and that the vast majority of fibers may strain
when the dolphin bends. Consistent with other animals, she found that the fiber
morphology of the SDS resists torsion, prevents aneurysms and limits wrinkling
when the dolphin bends. On the other hand her new model more accurately rep-
resents specific morphological features of the dolphin tapering cylinder. She pre-
dicted that the SDS also acts as a retinaculum for the terminal tendons of the axial
locomotor muscles, and plays a role in maintaining the laterally flattened cross-
sectional shape of the caudal peduncle (Chap. 1, Fig. 1.47b). The retinaculum is
extremely important in marine animals with long tendons that have a tendency
to ‘‘bowstring’’, i.e., to lift away from the joints when they are pulled on by their
muscles and when joints bend. A connective tissue band, reinforced with fibers at
high angles (often perpendicular to) the direction of the tendon, as in the dolphin
peduncle, is an ideal retinaculum. Pabst (2000) hypothesized that the body walls of
vertebrate swimmers with narrow-necked caudal tailstocks would have to be rein-
forced against tendon bowstringing (this was investigated in the white shark, as we
will see later (Lingham-Soliar 2005b)).
2.1  The Deeper Dermis of Marine Vertebrates 75

Pabst (2000) wondered if characters previously identified as convergent

between cetaceans and tunas were predominantly external features. Her findings
showed they were not and that comparisons extended much deeper such as the pat-
tern of force transmission through the bodies of cetaceans and tunas and the mus-
culoskeletal system with respect to: (1) Connections between axial muscles and
peripheral, helically wound, connective tissue membranes that function to increase
locomotor muscle performance. (2) A pattern of caudal intervertebral joint flex-
ibility that controls caudal tailstock/peduncle movement. (3) Long, terminal ten-
dons that function to control the angle of attack of the propulsive caudal fin/flukes.
(4) A peripheral connective tissue membrane in the region of the caudal tailstock/
peduncle, which is thickened and reinforced with steeply angled connective tissue
fibers that function as a retinaculum.
Based on her findings, Pabst proposed that these convergent characters are
‘‘functionally significant design features’’ of steady swimming vertebrates. She
looked at how the evolution of axial muscles involved changes in morphology,
activation pattern and function as vertebrates made the transition from axially-
powered (body) swimming to appendicularly-powered (limbs), terrestrial loco-
motion and vice versa. Interestingly, she found that dolphins and scombrid fishes
do not share similar axial muscle morphologies. Although the design of the col-
lagenous force transmitting structures are convergent, the morphology of the force
generating axial muscle does not appear to be a functionally uniform design. In
contrast to fish myomeres, the axial locomotor muscles of dolphins are organ-
ized into longitudinal tracts as is typical of mammals (reviewed in Pabst 1990)
(Figs. 2.9, 2.10). On the other hand, regional patterns of vertebral flexibility in the
common dolphin (Long et al. 1997) are similar to those described for tunas.
Long and colleagues (1997) found that the lumbo-caudal region appears to
function as a rigid base of support for the muscles that act on the caudal tailstock
and that caudal vertebrae 20 and 21 appear to function as a base for the highly
flexible insertion of the caudal flukes. From these studies it is clear that tunas and
dolphins possess convergent patterns of caudal vertebral flexibility. The serial
arrangement of a stiff tail-base, intervening flexible spine, stiff caudal fin base,
and compliant joint at the caudal fin insertion, appears to be a functionally signifi-
cant design that controls the pattern of body bending in steady swimming verte-
brates. In scombrid fishes, the five to six caudal-most myosepta form two sets of
long, terminal tendons (Fierstine and Walters 1968; Westneat et al. 1993; Donley
and Dickson 2000; Donley et al. 2004; Shadwick 2005). The great lateral tendon
(GLT), which inserts on the caudal fin, is formed by the longitudinally oriented
collagen fibers of the myosepta of anterior pointing cones. Likewise, the medial
caudal tendon, which also inserts on the caudal fin, is formed by the longitudinally
oriented collagen fibers of the myosepta of posterior pointing cones. The tendons
transmit muscular force across the compliant joint at the base of the caudal fin
and aid in controlling its angle of attack. Long, terminal, myoseptal-tendons are an
apparently derived character for scombrids (Katz and Jordon 1997). In dolphins,
the caudal extension of the longissimus, the extensor caudae lateralis, inserts onto
the dorsal surfaces of the caudal-most vertebrae in the flukes, by way of seven
76 2  Vertebrate Swimming

Fig. 2.10  Evolution of epaxial muscles in vertebrates. a Fish axial muscles are organized into
myomeres—a series of discrete, complexly folded units, separated by connective tissue membranes
called myosepta. The shaded area represents a single myomere. Myomeres and myosepta con-
nect directly to the skin as well as to the vertebral column, and function to produce lateral bend-
ing of the axial skeleton. b The epaxial muscles of most anamniotic tetrapods, as represented by
salamanders, are myomeric in their organization, and most maintain their connections to the skin.
The shaded area represents a single, block-shaped myomere. During both swimming and walking,
the epaxial muscles function to produce lateral bending of the axial skeleton. c In amniotes, both
the function and morphology of the epaxial muscles are changed. As is seen in the crocodile, the
epaxial muscles are organized into three longitudinal tracts, most have lost their connection to the
skin, and they function to stabilize the longitudinal body axis during appendicular locomotion. The
shaded area represents the longissimus muscle. Adapted from Pabst (2000; see references therein)
2.1  The Deeper Dermis of Marine Vertebrates 77

Fig. 2.11  Caudal peduncle of humpback dolphin dissected to show some of the muscle tendons
as they enter the caudal fluke. Author’s unpublished data

long, terminal tendons that are serially homologous to the superficial tendons
(Pabst 1990). The extensor caudal lateralis is the only epaxial muscle to insert on
fluke vertebrae, and aids in controlling the flukes’ angle of attack. Thus, tunas and
dolphins have converged upon a pattern of long terminal tendons that insert upon
the propulsive caudal fin/flukes (Fig. 2.11).
This tendon morphology permits forces that are generated by large cross-sec-
tional areas of more cranially-placed muscle (large anteriorly located muscle mass),
to be transmitted and focused through the narrow-necked caudal peduncle—a func-
tionally significant design feature of steady swimming vertebrates recognized as
an adaptation to reduce drag. Fortuitously, it was possible to discover this design
feature in the extinct member of thunniform swimmers, the 200 million-year-old
ichthyosaur, Stenopterygius, which will be mentioned further on. We will con-
sider these conditions in further detail later but first we will look at the lamnid or
thunniform sharks with particular respect to structures that may reflect yet more
instances of evolutionary convergence in the biology and biomechanics of the four
groups of thunniform swimmers.

2.1.2.3 Lamnid Shark Dermis

Attention among thunniform vertebrates was next turned to the control surfaces
of the white shark, Carcharodon carcharias, and the role of the dermal fibers in
their mechanical performance (Lingham-Soliar 2005a, b). C. carcharias, along
with the mako shark, Isurus oxyrinchus, belongs to a family of sharks (Lamnidae)
using the fast, thunniform mode of locomotion (Donley et al. 2004), shared with
as shown earlier just three other phylogenetically unrelated groups of large marine
78 2  Vertebrate Swimming

Fig. 2.12  Shortfin mako shark, I. oxyrinchus photographed from above as it swam close to the
boat. Both the angle of photography and refraction of the water gives a more flattened impression
of the animal but serve to emphasize the flattened plate-like caudal peduncle relative to the rest of
the body. Photo permission of Lloyd Edwards

vertebrates, tuna (Scombridae), dolphins (Delphinidae), and the extinct ichthyo-

saurs (Ichthyosauridae; see below). Evolutionary constraints in the three extant
groups of phylogenetically unrelated thunniform swimmers have imposed notable
differences in the anatomy and biomechanics of the dorsal and caudal fins, princi-
pally connected with how stiffness is achieved. However, even a superficial exami-
nation in lamnid sharks shows the presence of a large, highly stiffened dorsal fin
and a highly stiffened, high-aspect ratio (AR) caudal fin (and dorso-ventrally flat-
tened caudal peduncle; Fig. 2.12), as opposed to all other sharks, with implications
of very similar functions.

Dorsal Fin

Despite significant work on the tail mechanics of sharks (Alexander 1965;

Thompson 1976; Thompson and Simanek 1977; Wainwright et al. 1978; Graham
et al. 1990; Ferry and Lauder 1996; Wilga and Lauder 2002, 2004), there are few
studies that have examined the control structures of thunniform swimmers in any
real depth, other than whether or not there was some kind of internal support sys-
tem. Presence of a large, similarly shaped and similarly located dorsal fin in phy-
logenetically unrelated groups of cruising marine vertebrates (tuna, lamnid sharks,
dolphins, and the extinct ichthyosaurs) underscores its apparent importance as a
stabilizer. Evolutionary constraints, however, have imposed notable differences in
the anatomy and structure of the dorsal fin in these groups. For instance, within
2.1  The Deeper Dermis of Marine Vertebrates 79

Teleostei, the dorsal fin in its derived condition, e.g., in fast-swimming perciforms,
comprises two anatomically distinct portions: an anterior section supported by
spines and a posterior section supported by soft rays (Drucker and Lauder 2001).
In dolphins it is a de novo dermal structure, formed and supported only by connec-
tive tissue (Pabst 1996a) and in sharks it consists of soft, cartilaginous radials and
highly flexible fin rays or ceratotrichia (Gans and Parson 1964).
Because little was known of the control structures in one of the most formi-
dable predators in the oceans, the white shark, the possession of simple flexible,
cartilaginous radials intuitively felt quite inadequate for maintaining a stiff dorsal
fin comparable to that of the other extant thunniform swimmers. There had to be
some other stiffening mechanism. Did the crossed-fiber structure discovered in the
body of non-lamnid sharks extend into the control structures of the white shark?
However, Moss (personal communication in Motta (1977)) had earlier stated that
only a basement membrane was present in the control structure of sharks and that
the dermis was absent.
It is important to note that in studies such as this (Lingham-Soliar 2005a, b),
before freezing for storage, that the carcasses are of freshly caught sharks (Cliff
et al. 1996). Freezing has been found to have no effect on the tissue quality (Mann
et al. 1990; Micozzi 1986; Gill-King 1997). Studies have investigated and dis-
missed the effect of freeze-thaw cycles on skeletal muscle including collagen fib-
ers (Van Ee et al. 1998), articular cartilage (Tordonato 2003) and ligament tissue
(Woo et al. 1986).
The internal anatomy of the dorsal fin in C. carcharias showed that the radial
muscles extend less than half way up the dorsal fin and attach to the cartilaginous
radials (Fig. 2.13) by perimysial connective tissue (PCT).
Contrary to Moss’ (1972) findings in non-lamnid sharks, transverse histologi-
cal sections in the dermis in the dorsal fin of C. carcharias showed large numbers
of dermal fiber bundles that extended from the body into the dorsal fin. However,
they differed from those shown before in the body of sharks (Motta 1977). Here,
they were organized in extremely elongated bundles (in cross-section, Fig. 2.13b,
arrow 1) packed tightly together and became progressively more elongated deeper
into the dermis. Most striking was the staggered formation of the adjacent bundles
in the vertical plane, i.e., in a straight line from the fin surface to its interior. What
this means is that they were not in distinct, well-organized layers of uniform depth,
rather adjacent fiber bundles were staggered through the depth of the dermis, like
a vertical brick work, some popping up and others down. This was in contrast to
bundles of uniform cross-section occurring in neat rows (frequently demarcated
by septa) as revealed in the dermis overlying the body of non-lamnid sharks
(Motta 1977). The close association of these tall bundles meant that the fiber bun-
dles of the dorsal fin were packed to capacity in the dorsal fin of C. carcharias.
Because Moss’ findings were on non-lamnid sharks, I also investigated two spe-
cies of non-lamnids, the tiger shark, Galeocerdo cuvier, a fairly competent swim-
mer (Fig. 2.1c), and the spotted ragged tooth shark, Carcharias taurus, (Fig. 2.1b),
a relatively slow swimming species with two fairly low aspect ratio dorsal fins.
80 2  Vertebrate Swimming

Fig. 2.13  Schematic representation of the dorsal fin of Carcharodon carcharias. a The rectangle

inserts A–E show sites from which transverse sections of the skin were taken. Note, sites A–E
appear in this figure for convenience and represent only the locations of the dermal sections and
are not intended to represent different orientations, levels, etc. Tangential sections were taken
from sites A–C. Arrow 3 shows fibers in tangential view. b Representative transverse sections
of the dermis taken identically in all five sites (A–E). Arrow 1 shows the plane of the transverse
sections and arrow 2 the plane of the tangential sections. Lingham-Soliar (2005a), courtesy of
Journal of Morphology, Wiley and Sons

First, both non-lamnid species possessed significant amounts of dermal fibers,

again contrary to Moss (1972) and, second, they were significantly different from
those in the white shark. The findings in the three species examined were:
1. In all species the fiber arrangements of the dorsal fin occur in staggered for-
mation, generally contrasting with the well-ordered rows previously found in the
dermis overlying the body of the sharks. 2. Fibers are grouped in bundles of vary-
ing sizes, somewhat resembling skeletal muscle fasciculi. 3. Variations were found
in stratum compactum fiber bundle profiles and densities in the three species with
the most impressive concentration, distribution, and number of fiber bundle layers
occurring in C. carcharias. 4. Fiber angles in the dorsal fin in the three species are
60°+ to the long axis. 5. In the dorsal fin in all three species an orthogonal mesh-
work is formed by some layers of fibers but not by others. 6. Fiber bundles at the
boundary just below the base of the dorsal fin are smaller in diameter and form an
orthogonal meshwork. 7. In the caudal fin in C. carcharias fibers extend in parallel
formation along the length of the dorsal fin in a number of clearly demarcated lay-
ers or rows. 8. In C. carcharias the fiber bundles in the caudal peduncle (close to the
2.1  The Deeper Dermis of Marine Vertebrates 81

caudal fin) occur at angles in excess of 60° to the long axis of the animal. Fibers in
layers are alternately left- and right-hand oriented and form an orthogonal mesh-
work. 9. In the stratum spongiosum the fiber bundle profile (small size, sparse, and
not grouped in larger bundles) is generally similar in all three species (Fig. 2.14).
With hindsight wisdom the fiber organization in the dorsal fin of C. carcharias
shows exactly what one would expect of a dynamic stabilizer. Based on the fiber
directions and close aggregations the indications are that they work like the rig-
gings that stabilize a ship’s mast. This means they have to allow an increase in
tensile strength but without impeding the transfer of fiber tension from the body
(Fig. 2.15). This is achieved principally in two ways: first fiber bundles are tightly
packed in transverse section in more or less staggered formation but without being
interwoven either as bundles or layers; and second fiber bundles are steeply ori-
ented (in excess of 60°) and strained (or pre-stressed), facilitating rapid transfer of
tension from the body (see below). During fast swimming, when the problems of
yaw and roll are greatest, hydrostatic pressure within the shark increases and the
fibers around the body, including in the dorsal fin, become taut, thereby stiffening
the fin. During slow swimming and feeding the hydrostatic pressure is reduced,
the fibers are slackened, and the muscles are able to exert greater bending forces
on the fin via the radials and ceratotrichia. In C. carcharias there is a trade-off for
greater stiffness of the dorsal fin against flexibility.
How critical are the fiber structure and mechanical characteristics of the dorsal
fin to the lifestyle of Charcarodon carcharias? In a high speed swimming thunni-
form animal such as C. carcharias the powerful oscillations of the tail may induce
recoil or lateral oscillations at the head. The latter could potentially diminish the net
thrust by increasing viscous drag as the organism deviates from a rigid body (Nauen
and Lauder 2002; Fish et al. 2003). In C. carcharias there are two ways in which
the anterior recoil forces are reduced. First, by narrow necking and streamlining of
the caudal peduncle (Lingham-Soliar 2005b; here, Chap. 1, Fig. 1.47a) this reduces
the mass effect posteriorly during caudal fin oscillation and the corresponding recoil
forces anteriorly (Blake 1983; Webb 1984; Reif and Weishample 1986; Fish et al.
2003). Second, by increasing the surface area around the center of mass by means of
a tall and broad dorsal fin), this increases the added mass and inertia at the anterior
end of the animal. The high angles of the fiber bundles act as reinforcement of the
dorsal fin, comparable to the high angles of the fiber bundles in the caudal pedun-
cle of dolphins (Pabst 1996a). In the lemon shark, tension on the shark’s skin due
to internal hydrostatic pressure was shown to increase with speed from ~20–35 kN
m−2 to 200 kN m−2 (Wainwright et al. 1978). It led to the hypothesis that this ten-
sion is transferred to the fibers on either side of the dorsal fin, which results in the
fin becoming rigid (Lingham-Soliar 2005a). Thus, maximum stiffness occurs with
maximum speed, and it is no coincidence that this also occurs when the problems of
yaw and roll are most serious.
A highly stiffened dorsal fin is necessitated by the lifestyle of C. carcharias,
a pelagic, high-speed swimmer at the top of the marine food chain (Randall
1983; Boustany et al. 2002; Froese and Pauly 2002). This lifestyle contrasts with
that of C. taurus and G. cuvier. The more posterior position of the dorsal fins in
82 2  Vertebrate Swimming

Fig. 2.14  Representative transverse sections of the skin from the dorsal fin of Carcharodon
carcharias, Galeocerdo cuvier, and Carcharias taurus. All sections are taken from the skin sur-
face downward. Arrows at the upper and lower parts of the figure show top and craniad direc-
tions of the sections, respectively (refer to Fig. 2.13 for site locations). a Section from site A
of C. ­carcharias RB 02057 (female) in which approximately nine distinct rows of dermal fiber
bundles are present. Just visible above is the stratum spongiosum and at the bottom the connec-
tive tissue layer in which collagen fiber bundles are absent. b Site A of C. carcharias ZIN 02029
(male) in which the dense fiber bundles are staggered in formation. c Part of the stratum compac-
tum of C. carcharias RBDS42 at site C in which numerous layers of fiber bundles are present.
d About four rows of stratum compactum fibers are seen at site E in C. carcharias RBDS42.
The fiber bundles have oriented with the long axis along the horizontal plane. Above is the stra-
tum spongiosum and at the bottom connective tissue. e Site B in Galeocerdo cuvier in which the
fiber bundles of the stratum compactum are already reduced. The upper half of the picture shows
the stratum spongiosum in which small bundles of fibers occur within a collagenous matrix. The
large yellow inclusions toward the bottom are ceratotrichia. f A major part of the stratum compac-
tum fibers of C. taurus RB 02061 at site A showing densely aggregated fiber bundles in staggered
arrangement. g By site B the stratum compactum fibers have dwindled to 2–3 rows. Above is the
stratum spongiosum and below connective tissue with ceratotrichia just in view. h At site C there
are no stratum compactum fibers in C. taurus RB 02061; only small fiber bundles may be seen
in the stratum spongiosum. Scale bar in all figures except d, 0.25 mm. Scale bar in d, 0.5 mm.
Lingham-Soliar (2005a), courtesy of Journal of Morphology, Wiley and Sons
2.1  The Deeper Dermis of Marine Vertebrates 83

Fig. 2.15  A schematic
view of the dermal fibers
extending from the body into
the dorsal fin of Carcharodon
carcharias. The angles
become much steeper in
the dorsal fin (60°+) and
the crossed-fiber meshwork
is not always as evident
as depicted in the scheme
(see text). Lingham-Soliar
(2005a), courtesy of Journal
of Morphology, Wiley and
Sons

C. taurus compared with C. carcharias and G. cuvier (see Fig. 2.1), exempli-

fied in fish such as the northern pike, Esox lucius (Webb 1983; Webb and Weihs
1983), may enable more rapid acceleration from a stationary position, com-
pared with slower starts in thunniform sharks (McGowan 1999), the former use-
ful in ambush predation. A special ability to control its buoyancy and remain
motionless by gulping air into the stomach (Bass and Ballard 1972) may also
contribute to predation by stealth. Among sharks, G. cuvier spends considerable
time swimming slowly in habitats that are varied (Tricas et al. 1981; Tricas and
McCoscer 1984; Heithaus et al. 2001; Heithaus and Dill 2002). Its dorsal fin is
closely similar in shape and size to that of C. carcharias, but the dermal fiber
structure suggests greater flexibility, which, in my view, may create less resist-
ance during the strong lateral movements involved in underwater shake feeding
(Frazzetta and Prange 1987; Frazzetta 1988, 1994), while stability is maintained
by the pectoral fins (Springer 1961).
84 2  Vertebrate Swimming

Caudal Fin Dermal Fibers

The complex fiber organization in the dorsal fin of C. carcharias and the critical
functional implications in a high-speed swimmer paved the way for a similar anal-
ysis of the caudal fin. We saw in Chap. 1 that the classic model of heterocercal tail
function in sharks asserts that the tail produces a forward thrust directed in a line
that would produce a turning movement around the center of balance: this would
tend to raise the tail and drive the head downward in forward movement, the lat-
ter countered by lift generated by the pectoral fins (Alexander 1965) contrasting
with Thomson (1976) and Thomson and Simanek’s (1977) model, that hypothe-
sized that the tail generates a reaction force directed through the center of mass.
We also saw that recent studies using, e.g., digital particle image velocimetry
(DPIV) on wake vortices in juvenile, benthic sharks, support the classic interpre-
tation of heterocercal caudal fin function (Ferry and Lauder 1996; Lauder 2000;
Wilga and Lauder 2002, 2004; Nauen and Lauder 2002; see Chap. 1) which was
also at variance with the interpretations on how anterior balance is achieved (Fish
and Shannon 2000).
The above studies involved relatively slow swimming sharks and certainly can-
not be used as a model for fast swimming thunniform sharks, which Wilga and
Lauder (2002) acknowledge. The white shark is almost impossible to keep in
captivity and hence upon which it is clearly impossible to perform DPIV analy-
sis. Given such constraints, anatomical and biomechanical studies were per-
formed on the control structures of the thunniform shark Carcharodon carcarias
in an attempt to understand their locomotory potential (Lingham-Soliar 2005a, b)
(Fig. 2.16).
Wainwright et al. (1978) investigated the role of the skin in swimming dynam-
ics by twisting the entire tail and measuring the torque with the skin intact and
excised and found that despite the thinness of the skin it contributed about 50 %
of the tensile stiffness. However, because of significant differences in the lobe size
and anatomy in the heterocercal tail of sharks it was considered important to test
the two lobes in Carcharodon carcharias individually as well as the caudal pedun-
cle (Lingham-Soliar 2005b).
The caudal peduncle in thunniform sharks such as C. carcharias is very different
from that of other sharks. It is a highly modified, dorsoventrally compressed and
rigid structure that facilitates the oscillations of the caudal fin (Fig. 2.12). Its stiff-
ness appears to be principally achieved by a thick layer of adipose tissue ranging
from 28 to 37 % of its cross-sectional area, reinforced by cross-fibered collagen
fibers. Numerous overlying layers of collagen fibers of the stratum compactum,
oriented in steep left- and right-handed helices (65° to the shark’s long axis), pre-
vent bowstringing of the muscle tendons, which lie just below the dermal layer
(exactly as in dolphins) (Lingham-Soliar 2005b) (Fig. 2.16b).
With respect to gross structure, the bulk of the mass of the dorsal lobe of the
caudal fin comprises the notochord (not present in the ventral lobe), perimysial
fibers, muscles, and adipose tissue. The adipose tissue reinforces the leading edge
of the dorsal lobe and contributes to an ideal cross-sectional geometry (tear-drop)
2.1  The Deeper Dermis of Marine Vertebrates 85

Fig. 2.16  Carcharodon carcharias. Schematic representation of the caudal fin and caudal

peduncle based on dissections. a Dissection showing, perimysial fibers, muscle, and notochord.
Note, the caudal peduncle has been twisted ventrally to show the broad dorsal view. The hemal
spines just intrude into the ventral lobe. Numbers indicate the sites from which transverse and
tangential sections were taken. b Caudal peduncle transverse section taken from a point just ante-
rior to the mid-length showing the adipose tissue, muscle, and notochord. c Schematic 3D block
cut from the fin showing principally transverse (1) and tangential (2) views of the stratum com-
pactum fibers. Lingham-Soliar (2005b), courtesy of Journal of Morphology, Wiley and Sons

consistent with an advanced hydrofoil (Figs. 2.16, 2.17a, b). In contrast most of the
mass of the ventral lobe consists of the ceratotrichia or fin rays separated by thin
partitions of connective tissue. At the core is a pith of gas-filled cells (Fig. 2.17c, d).
The dermal fibers of the stratum compactum of the caudal fin of sharks had not
been investigated previously (Lingham-Soliar 2005b). Consistent with findings in
the dermis overlying the body of other sharks (Motta 1977) the fibers of dorsal
lobe of C. carcharias were found to occur in numerous distinct layers. However,
the layers are more complex than in other sharks and reflect a hierarchical devel-
opment, i.e., the fiber layers comprise thick fiber bundles with the thickest occur-
ring deepest in the stratum compactum and diminishing in size toward the surface.
Each of these layers alternates with and is separated by a single layer of fiber bun-
dles, a formation thought to give stability to the stratum compactum and to enable
freer movements of the fiber system. In tangential sections of the stratum compac-
tum the fiber bundles in the dorsal lobe can be seen oriented with respect to the
long axis of the shark at ~55–60° in left- and right-handed helices. Because of the
backward sweep of the dorsal lobe (55° to the shark’s long axis) the right-handed
fibers also parallel the lobe’s long axis. In the dorsal lobe, ceratotrichia are present
only along the leading edge (embedded within connective tissue), apparently as
reinforcement (Fig. 2.18).
86 2  Vertebrate Swimming

Fig. 2.17  Carcharodon carcharias. Caudal fin cross-sections. a Approximate two-thirds span

dorsal lobe. b Base dorsal lobe. c Base ventral lobe (hemal spines from dorsal lobe just intrud-
ing). d Approximate two-thirds span ventral lobe. Lingham-Soliar (2005b), courtesy of Journal
of Morphology, Wiley and Sons

The dermal fiber bundles of the ventral lobe, viewed in transverse section, lack
the well-ordered distinctive layers of the dorsal lobe, but rather occur as irregu-
larly arranged masses of tightly compacted fiber bundles of various sizes, more
resembling those of the dorsal fin. In tangential sections the fiber bundles are ori-
ented at angles of ~60°, generally in one direction, i.e., lacking the left- and right
handed helical pattern. Below these layers of the dermis, dense layers of cera-
totrichia extend virtually to the core of the fin and comprise a ‘honeycomb’ of air
pockets (Fig. 2.19).
Tensile load tests on the skin of the caudal fin [by testing with skin intact
and then with skin excised (see Wainwright et al. 1978)] indicate high passive
2.1  The Deeper Dermis of Marine Vertebrates 87

Fig. 2.18  Dermal fibers of Carcharodon carcharias. a Transverse section. Eight layers of

fiber bundles; four thick layers alternating with 4 thin layers (numbered 1–4) at one-third span.
A further layer at the base is less organized and with a higher proportion of connective tissue.
Arrow = vertical direction of section to the surface. b Similar section as a by scanning electron
microscopy. a Modified from Lingham-Soliar (2005b) and b Authors unpublished data

resistance to bending. The shear modulus G showed that the skin’s contribution
to stiffness (average values from three specimens at radians 0.52 and 1.05) is
33.5 % for the dorsal lobe and 41.8 % for the ventral. The load tests also indicate
greater bending stiffness of the ventral lobe compared to the dorsal. Overall, the
anatomy and mechanics of the dorsal lobe of C. carcharias facilitate greater con-
trol of movement compared to the ventral lobe. However, I anticipate that with
increasing speed and increased hydrostatic pressure in the dorsal lobe (the ventral
lobe, unlike the dorsal, lacks a muscle and blood vascular system) the dorsal lobe
88 2  Vertebrate Swimming

Fig. 2.19  Carcharodon carcharias. Vertical section of the ventral lobe at one-third span under
dichromatic light. Ceratotrichia. a Part of the dense layer of ceratotrichia (below the dermis) that
extends virtually to the core of the fin. All white/bluish shapes are thin sections of ceratotrichia.
The black shapes are where the thin sections have fallen out. b Scheme of vertical section of the
ventral lobe, from the stratum spongiosum to the core, which is composed of a dense, irregular
mass of connective tissues; only the upper part of the ceratotrichia layer is shown as indicated by
stippled lines. Scale bar ~1 mm. Lingham-Soliar (2005b), courtesy of Journal of Morphology,
Wiley and Sons

will match the static stiffness of the ventral lobe. The helical fiber architecture near
the surface of the caudal fin is analogous to strengthening of a thin cylinder in
­engineering (see Chap. 1).
The detailed anatomical and morphological descriptions (Lingham-Soliar
2005b) were vital to the functional interpretations. High fiber angles along the
span of the dorsal lobe are considered ideal for resisting the bending stresses that
the lobe is subjected to during the locomotory beat cycle. They are also ideal for
2.1  The Deeper Dermis of Marine Vertebrates 89

Fig. 2.20  Schematic
interpretation of the stratum
compactum fibers of the
dorsal lobe of Carcharodon
carcharias showing the fiber
helices. Arrows show the two
axes along which the fibers
were examined and fiber
angles based upon. Lingham-
Soliar (2005b), courtesy
of Journal of Morphology,
Wiley and Sons

storing strain energy during bending of the lobe and consequently may be of value
in facilitating the recovery stroke. The higher shear modulus in the ventral lobe
may be explained by absence of vertebral support. The air filled cells in the middle
of the ventral lobe may also be of functional significance (Fig. 2.19). For instance
Dawson and Gibson (2006) who investigated the biomechanics of hedgehog and
porcupine quills, which have compliant cores found optimization or improvement
in the load ratio and moment ratio in shells with a honeycomb or foam core over
an equivalent hollow shell. Overall both the compliant core (ventral lobe) and
complex fiber structure of the dorsal and ventral lobes of the caudal fin and cau-
dal peduncle of C. carcharias provides a realistic potential for an elastic mecha-
nism in the animal’s swimming motions and consequently for energy conservation
(Alexander 1988; Pabst 1996b) (Fig. 2.20).

2.1.2.4 Ichthyosaur Dermis

Modern studies on the extant thunniform swimmers, lamnid sharks, dolphins, and
tuna help explain many of the complexities of structure and mechanics connected
with high speed aquatic locomotion that were previously unknown. However, one
group of extinct marine vertebrates, included as we said earlier among the thun-
niform swimmers, were the ichthyosaurs, albeit based purely on external charac-
teristics, body and tail shape (Lighthill 1975). According to the modern studies
that showed the importance of internal anatomical characteristics, particularly
with respect to the dermal fiber structure and chemistry, no more than speculation
on similarity of swimming locomotion with extant thunniform swimmers could
90 2  Vertebrate Swimming

now be made. Hence, similar definitive evidence as found in modern-day thun-

niform swimmers was needed if more conclusive comparisons were to be made.
A search for ichthyosaur soft tissue, which might hold some of these answers, was
necessary.
The first problem that required an answer to the question referred to earlier,
was there direct muscular control of the caudal fin in Jurassic ichthyosaurs or were
nearly all the muscle fibers lost and the cones almost completely tendinous as in
tuna and dolphins? Among the numerous ichthyosaur specimens examined, one
appeared to provide some of the answers, a specimen of Stenopterygius, housed
in the Geology Museum at Tubingen University (Fig. 2.21). It was possible to
identify in the preserved soft tissue, structures that were near spindle-shaped in
the region just anterior to the caudal fin and to reasonably conclude that these
cone-shaped structures formed part of a tendinous sheath, which was apparently
derived from myosepta (associated with the myomeres) and that it provided the
basis in ichthyosaurs for a caudal tendon system (Lingham-Soliar and Reif 1998)
(Fig. 2.22a, b), as demonstrated by Fierstine and Walters (1968) in tuna.
The next question, closely associated with narrow-necking of the region ante-
rior to the caudal fin was whether or not a caudal peduncle, as in the white shark
and dolphins, was present so as to enable a constant, high angle of attack of the
caudal fin during the beating cycle. In a lateral beating cycle as in ichthyosaurs,
the caudal peduncle if present would have been flattened dorsoventrally as in the
white shark (Fig. 1.47a) and mako shark (Fig. 2.12). The odds were against identi-
fying such a structure because virtually all Jurassic ichthyosaurs are laterally com-
pressed during preservation. However one specimen that I was able to examine,
Stenopterygius R 457 (Senckenberg Museum, Germany) showed a hint of dorsally
displaced soft tissue in the peduncular region suggesting strong circumstantial evi-
dence of a thickened lateral keel that had been twisted slightly vertically during
lateral compression and apparently in consequence had displaced the vertebrae
ventrally (Lingham-Soliar and Reif 1998; here Fig. 2.23).
Probably the most significant investigation involved whether or not Jurassic
ichthyosaurs had a crossed-fiber architecture of the dermis comparable with that of
the extant thunniform swimmers. The first clue to the possibility of a crossed-fiber

Fig. 2.21  Stenopterygius quadricissus Re 1297/1 (Department of Geology, Tubingen Uni-

versity). Preparation is of the right side shows the lateral and part of dorsal surface. Scale
bar = 25 cm. Lingham-Soliar and Reif (1998), courtesy of Neues Jarbuch (abh)
2.1  The Deeper Dermis of Marine Vertebrates 91

Fig. 2.22  Stenopterygius quadricissus Re 1297/1 (Department of Geology, Tubingen Univer-

sity). a Part of exposed layer of tissue above vertebral ‘peduncle’ showing phosphatized fibers
and a further layer of fibers is also visible below the vertebrae. b Detail of phosphatized fib-
ers. Lower part of figure shows ruptured overlying tissue that is folded back (arrowed). Scale
bar = 1 cm. Lingham-Soliar and Reif (1998), courtesy of Neues Jarbuch (abh)

architecture came from an ichthyosaur specimen, GLAHM V1180a, housed in the

Hunterian Museum of the University of Glasgow. This specimen was identified
as Ichthyosaurus, from the Lower Lias of England, which lived about 200 MYA
(Lingham-Soliar 1999). Only the skull was preserved in a mudstone nodule but,
fortuitously, this specimen showed traces of preserved skin (Fig. 2.24). This is not
to be confused with many other ichthyosaur specimens from the world famous
lower Jurassic Posidonia shale of southern Germany with so-called soft tissue
preserved. Frequently, they are no more than decayed and transformed soft tissue
92 2  Vertebrate Swimming

Fig. 2.23  Stenopterygius quadricissus SMF R457. Dorsolateral view of meshwork of filamen-

tous fibers over dorsolateral surfaces of the body. Because of slight dorso-lateral compression
the fleshy outline of the caudal peduncle is visible. Scale bar = 25 cm. Lingham-Soliar and Reif
(1998), courtesy of Neues Jarbuch (abh)

that may simply outline the body as a black carbon-like film, with little organic
matter preserved including skin fibers. The Hunterian specimen shows actual pre-
served skin fibers overlying the jaws. Significantly, two layers of dermal fibers are
revealed, which, despite erosion, show a crossed-fibered arrangement (Fig. 2.24b,
white arrows) strikingly similar to that of tunas, dolphins, and sharks (Lingham-Soliar
1999). Note, the black arrows show patches of tissue (not individual fibers) that in
an earlier study (Delair 1966) had mistakenly been identified as thick fibers.
However, because the fibers were found solely on the jaws it was not possible to
state other than by speculation that they were found over other parts of the body as
in the modern thunniform swimmers. This was critically important, because of the
functional significance with respect to high-speed swimming (also see Volume 1).
Many specimens were examined in some of the best collections in the world,
among which two ichthyosaurs specimens showed potentially viable soft tis-
sue preservation over the body. They both belonged to the late Jurassic species
Stenopterygius quadricissus and both were fossilized in the Posidonia Shales of
southern Germany. Specimen PMU R435 was housed in the Uppsala Museum
in Sweden and the other was specimen SMF R457, mentioned above. They were
both coincidentally prepared by one of the finest fossil preparators in the world at
the time, Bernard Hauff. These findings were described in Volume 1. Figure 2.23
shows some of the best preserved crossed-fiber architecture over large areas of
the body in SMF R457 (the largest of which, up to 1 mm thick, are visible to the
naked eye).
Fibers were identified in three size classes based on thickness and in different
levels of the integument over virtually the entire surface of the body of the three
ichthyosaur specimens named above (Lingham-Soliar 1999, 2001). The thick-
est fibers were located deepest in the skin and the thinnest in the outermost layers.
However, this was the first such record of a hierarchical fiber architecture seen in
2.1  The Deeper Dermis of Marine Vertebrates 93

Fig. 2.24  Ichthyosaurus GLAHM V1180a housed in the Hunterian Museum of the University of

Glasgow. The specimen shows crossed-fiber architecture in the lower jaws. a The head preserved
in a mudstone nodule. b A section of two layers of oppositely oriented fibers, fairly decomposed/
eroded. Lingham-Soliar (1999) courtesy of the Royal Society of London

the integument of any vertebrate extinct or extant (Lingham-Soliar 2001). It was not
until a few years later that a similar hierarchical structure of fibers in the dermis of
the white shark, C. carcharias, as shown above, was found (Lingham-Soliar 2005b).
The system comprised an architecture of oppositely oriented fibers in alternative
layers just as they are in extant thunniform swimmers. The fiber angles varied over
the body from between 25° and 70° to the long axis of the animals, which coin-
cided with different amounts of stress in different regions of the body. Thus the fiber
structure in Jurassic ichthyosaurs strongly suggested another important criterion
of thunniform locomotion, namely a means for a highly stiffened body as demon-
strated in extant thunniform swimmers (Lingham-Soliar 1999, 2001).
94 2  Vertebrate Swimming

The next task was to examine the dermis overlying the dorsal and caudal fins
and determine whether or not the ichthyosaur dermis aided in their biomechanics
as established in sharks. The tail in both groups of animals had particular signifi-
cance, given that ichthyosaurs, like sharks have vertebral support in just one of the
caudal fin lobes, the lower (the upper in sharks).
Stenopterygius SMF 457 again proved invaluable, this time in resolving the
fiber architecture in the dermis of the dorsal and caudal fins (2.25). Three major
types of fiber orientations were shown in the dorsal fin of Stenopterygius of SMF
R457 (Lingham-Soliar and Plodowski 2007) (Fig. 2.25a, b). In the first, alternat-
ing oppositely oriented fibers at the lower posterior part of the fin were oriented at
low fiber angles that apparently allowed greater freedom of fiber movements and
facilitated reorientation toward a stress axis (Naresh et al. 1997). This fiber pattern
is similar to that observed in the white shark dermis (Lingham-Soliar 2005a, b). In
the second, stiffness in the lateral plane is achieved by fibers that parallel or orient

Fig. 2.25  Dorsal and caudal fin crossed-fibers in Stenopterygius quadricissus SMF 457 in the
Senckenberg Museum in Germany. Dorsal fin. a High-tensile fibers near the fin base in three
to four layers, two show low fiber angles and one, high. b Left- and right hand-oriented fibers
toward the midpoint of the dorsal fin. Fibers occur in steeply angled right- and left-hand helices
in several layers (arrows show main fiber directions). c Fibers in the caudal fin dorsal lobe (lack-
ing vertebral support), exposed in transverse section (almost 90° to the surface) but also sheared
in places at about 45° to the surface, occur as a unique 3-D image. About eight layers of fibers
oriented at about 45° (right-handed) to the ichthyosaur’s long axis can be seen. Scale bar in a,
c = 1 cm (see Lingham-Soliar and Plodowski 2007 for figures on all seven zones investigated)
2.1  The Deeper Dermis of Marine Vertebrates 95

at steep angles to the long axis of the ichthyosaur (Fig. 2.25b). This orientation was
found toward the middle and tip of the dorsal fin of Stenopterygius where torsional
stresses were probably greatest as again shown in the white shark (Lingham-Soliar
2005a, b). Also toward the anterior of the dorsal fin the fibers are predominantly in
a single orientation, oriented at 50–60° to the long axis, in numerous layers before
a reversal in orientation (again for several layers). This structural architecture of
high fiber angles oriented at the same angle over numerous layers was considered
to have functional implications connected with control surfaces dedicated to stiff-
ness and stability during locomotion (Lingham-Soliar 2005a, b).
The dorsal lobe of the caudal fin also showed a number of areas with compa-
rable fiber layers to those of the dorsal fin. However, despite more severe degra-
dation in the caudal fin, two areas of preserved fibers in the dorsal lobe occur as
rare transverse sections (cutting at near right angles to the fin’s surface), allowing
a high level of integumental information that is seldom seen in a fossil. The fibers
were preserved helically wound around the upper caudal lobe, oppositely oriented
at approximately +45° to the ichthyosaur’s long axis. In the 3-D images from the
unsupported dorsal lobe of the caudal fin, fibers follow the same orientation in
about eight layers (right-handed) before a reversal (Fig. 2.25c) in orientation (left-
handed). This is comparable to the anterior-midpoint of the dorsal fin and with the
same functional implications, dedicated to stiffness and stability during locomo-
tion (Lingham-Soliar 2005a, b).
A system of fibers with diagonal or bias arrangement of alternating left- and
right-hand-oriented fibers at ~45° to the long axis of a structure such as a fin pro-
vides stiffness in shear that functions to reinforce the fin in the same way that that
it does in fiber-reinforced thin cylinders (Lingham-Soliar 2005b; Clark and Cowey
1958; Wainwright et al. 1976). On the other hand, we find modifications of that
system in living animals such as sharks and ichthyosaurs where external condi-
tions may change and where fiber patterns may vary in different parts of the body
or organ to deal with different or changing conditions and stresses. This allows a
mechanical explanation for the fiber architecture at the base and tip of the dorsal
fin where torsional stresses are probably greatest, and for the central part where
bending stresses are greatest, as shown schematically in Fig. 2.26.
Findings of a highly organized cross-fiber architecture in the body and fins of
thunniform ichthyosaurs such as Ichthyosaurus and Stenopterygius are important
because it is now possible to tie them closely with respect to this crucial design
strategy with that of the other three groups of extant thunniform swimmers.
We mentioned briefly in Volume 1 the need to resolve the physico-chemistry of
the cross-fiber architecture in ichthyosaurs, which was more-or-less assumed to be
collagenous. A little more detail is added here.
The triple helical structure of the amino acids plays a major role in the molecu-
lar conformation of collagen in living animals. This gives collagen a unique nano-
physical structure or “fingerprint” ,i.e., the molecules of collagen types I, II, III,
V, and XI are packed into D-periodic cross-striated fibrils (D-bands), typically
D-67 nm, the characteristic axial periodicity of collagen, sometimes referred to
as the quarter-stagger structure because adjacent molecules are transposed just
96 2  Vertebrate Swimming

Fig. 2.26  Schematic views of major fiber constructions in the control surfaces of Stenopteryg-

ius. Dorsal fin. a Exploded view of fibers in alternate layers of left- and right-handed orienta-
tions. Fiber angles differ from steep to shallow angles in the layers (range shown 25–70°). b At
the base of the fin and at the tip, fiber layers show fibers oriented at low angles with the occa-
sional layer with fibers at high angles. Caudal fin (upper Lobe). c Numerous layers with fibers
oriented in the same direction before a reversal in direction

under one-quarter of their length in the axial direction (Smith 1968). However, this
method requires valuable material for examination by SEM. Although I was under-
standably turned down in a request for a small sample of GLAHM V1180a for
SEM analysis, the curator of the museum, Dr Neill Clark sent me some minute
fragments that had come of the specimen during its relocating in the Hunterian
Museum in Glasgow.
We were fortunately able to use the most advanced Zeiss electron microscope
in South Africa at the time and fortuitously, two fibers of approximately 20–30 µm
length, with rounded cross sections of approximately 4 µm in diameter (Fig. 2.27c)
were identified (~5,000 magnification). However, it was at a much higher resolu-
tion (~30,000 times) that the most significant discovery was made (Lingham-
Soliar and Wesley-Smith 2008). The SEM revealed numerous component fibrils
(Fig.  2.27a, b) with the distinctive axial band periodicity of 66.12 nm (mean
from numerous fibrils) consistent with the repeat D-band ultrastructure of type 1
2.1  The Deeper Dermis of Marine Vertebrates 97

Fig. 2.27  Ichthyosaurus (GLAHM V1180a). a Part of a 30 µm long fiber packed with fibrils
in remarkably good preservation. b Well-preserved D-bands or 67 nm repeat axial bands. c The
sheared tip of a fiber. The fiber is eroded but shows an angled cross-sectional view. Fibers can
be seen all the way to the fiber center. Lingham-Soliar and Wesley-Smith (2008), courtesy of the
Royal Society of London

collagen (Smith 1968; Kadler et al. 1996; Reichlin et al. 2005). The findings dem-
onstrated conclusively that the fibers preserved in the ichthyosaur integument were
collagenous.
The question that remains is why did such a wonderfully advanced swimming
animal such as the ichthyosaur not only become extinct but was among the first of
the great marine reptiles (see Volume 1) to do so? It is a question I tried to answer
a few years ago (Lingham-Soliar 2003).
During the early Jurassic monopoly of the swimming mode would have made
them highly competitive as pursuit predators of fish and squid. As fast efficient
predators they would have been secondary consumers in the food chain compara-
ble to present day dolphins. So, why were ichthyosaurs the first of the four main
groups of marine reptiles (the others being plesiosaurs, marine crocodiles, and
mosasaurs) to go extinct toward the end of the Cretaceous? Ironically, extreme spe-
cialization as high-speed pursuit predators, as seen in some modern-day predators
such as the cheetah, places a great strain on their feeding behavior particularly as
98 2  Vertebrate Swimming

prey become more evasive, which in some animal groups may ultimately lead to
extinction (Lingham-Soliar 2003). By the end of the Jurassic/early Cretaceous ich-
thyosaur monopoly of thunniform locomotion had come to an end. For instance the
Late Jurassic saw the emergence of high-speed swimming fishes (if not thunniform,
but fast) of the order Clupeiformes (herrings, anchovies, and allies) with a signifi-
cant peak in the Lower Cretaceous and the greatest radiation of teleost fishes, which
was so rapid that by the Upper Cretaceous 40 % of the families had appeared. The
radiation of chondrichthian fishes paralleled that of the bony fishes and reached
its greatest peak in the Upper Cretaceous. This invasion of fast-swimming fishes
would have placed great energetic costs on ichthyosaurs, both as predators and prey,
and may have played a significant part in ichthyosaur extinction (Lingham-Soliar
2003) (Fig. 2.28).

Fig. 2.28  The rise of four major fish groups over time, condrichthyans (Cy), chondrosteans
(Co), holosteans (H) and teleosteans (T). O Ordovician; S Silurian; D Devonian; C Carbonifer-
ous; P Permian; Tr Triassic; J Jurassic; K Cretaceous; T Tertiary. Graph from Lingham-Soliar
(2003), redrawn from Thomson (1976), courtesy of Neues Jarbuch (abh)
2.1  The Deeper Dermis of Marine Vertebrates 99

On a lighter note, ichthyosaurs may well feel aggrieved that the thunniform
swimming mode takes its name from Thunnus (tuna) given that Jurassic ichthyo-
saurs had evolved the swimming mode about 150 million years before tuna even
came into existence (almost certainly a class A litigation). Yet if the name ichthy-
osauriform did take precedence, think of the added burden of having to say and
spell it. One is reminded of Isabel Frances Bellous children’s poem.
There once was an ichthyosaurus,
Who lived when the earth was all porous,
But he fainted with shame
When he first heard his name,
And departed a long time before us.

2.1.3 Anguilliform Swimmers

We have come full circle since discussing the eel, Anguilla, in Chap. 1, and now
we briefly look at how the dermis might aid in the locomotion of the slowest of
vertebrate swimmers discussed in this volume.

2.1.3.1 Eel Dermis

Mary Hebrank (1980) notes the functions of fish skin are numerous, and are gen-
erally categorized as forms of protection from or adjustment to the environment
and eel skin particularly performs these functions admirably. She mentions an
interesting fact on a practical aspect of its toughness, in the service of humans—in
Scandinavia it is used as door hinges. With its ability to produce copious quanti-
ties of mucus the skin can also assist the animal in adjusting to rather extreme
environmental conditions—eels are not only euryhaline (capable of tolerating a
wide range of salinity down to freshwater) but are also capable of aerial cutaneous
respiration.
We saw above that sharks are constructed with the bulk of their musculature
far anterior to its primary propulsive organ, the caudal fin, reaching an extreme
in this evolutionary development in lamnid sharks. At the opposite end, the eel
has its musculature distributed more evenly along its length, and uses nearly this
whole length as its propulsive surface, lacking a distinct caudal fin (see Chap. 1;
Fig. 2.1a).
While an external tendon might be of less benefit to an eel than it would be to a
shark it should be kept in mind that both the eel and the shark (excluding Lamnid
sharks) swim by undulatory propulsion, and in both cases the amplitude of the
waves of bending increases as these waves travel backwards (Gray 1933). It is also
interesting that in both Motta (1977) and Wainwright et al. (1978), the sharks studied
were not thunniform but slower swimming sub-undulatory forms. Mary Hebrank’s
(1980) study was the first to investigate the anatomy of the dermal crossed-fiber
100 2  Vertebrate Swimming

system since Wainwright et al.’s (1978) study and, in the archetypal undulatory
swimmer. Thus, despite the morphological differences between sharks and eels,
Hebrank (1980) wondered whether or not presence of a similar fiber system to that
of sharks might contribute structural and mechanical properties to the locomotor
behavior of eels.
Mary Hebrank showed through morphological examination and tensile tests that
eel skin behaves very much as described in sharks including acting as an exotendon.
In addition, she pointed out that the eel exhibits another type of locomotor behavior
in certain feeding situations. When the eel feeds on something which is too large to
swallow, it bites into the food and then rotates about its own long axis several times,
with great speed, in order to tear off the mouthful. This motion can sometimes be
seen when an eel is caught on a hook and line, and it has been witnessed in eels
in aquaria. When this “corkscrew” motion occurs, the eel’s skin must be stressed
in torsion. As we know, a cylinder wrapped with inextensible fibers resists torsion
most rigidly when the fibers are wound at an angle of 45° with the long axis (the
direction of maximum tensile stress during torsion). Thus, when the eel performs
its corkscrew motion, the collagen fibers of one helical set (either the right- or left-
helical set, depending on the direction of the motion) are being pulled along their
long axes. Since the fibers behave as though they are continuous, the tensile force
is transmitted along the length of the fish. In this way it is possible that the eel need
only generate a twisting moment about the head in order to rotate the whole body. It
appears that a fiber angle of 45° is uniquely suited to this corkscrew motion.
Once we discovered that the invertebrate threshold for the crossed-fiber archi-
tecture had crossed over to vertebrates it now seems no surprise that the cross-fiber
helically wound fiber structure can be regarded as a biomechanical design prin-
ciple in many animals (and plants) and materials perhaps comparable in impor-
tance to, e.g., other design principles such as beams and thin-walled cylinders and
indeed frequently a part of them. In vertebrates its chemistry has been restricted to
collagen, unlike in invertebrates where, e.g., it includes collagen and chitin, and
in plants, cellulose (Gibson 2012). However, the story does not end there. We will
see in Chap. 5 the latest group of animals to join this structural design club, birds,
and with them a new material to incorporate the design in vertebrates, β-keratin.

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Chapter 3
Vertebrates Make Their Flight Reservations

In Chap. 1 some general principles of mechanics and flight were introduced.

Here we look at those aerodynamical principles that are involved in gliding
both as an end result in some animals and in others as a potential stage in the
­evolution of flapping flight. We will not consider pterosaurs and bats here but in
Chap. 4 because they use flapping or powered flight. We will also not consider
Archaeopteryx here which may or not have been confined solely to gliding but in
Chap. 5 as an introduction to birds where we will also look at advanced forms of
gliding among birds (soaring).

3.1 Gliding: Economy Class Air Travel

Why glide? Gliding flight is cheap and may be defined as passive or unpowered
flight in which little or no energy is consumed. For instance compared to active
flight, gliding in the herring gull (Larus argentatus) costs only 2.17 times the basal
metabolic rate (BMR; Norberg 1990). The forest or woodland canopy, in which
present-day gliders are found, makes gliding an energetically inexpensive means
of travel, i.e., of bridging the gap between one tree and the next or descent to the
ground. For some animals gliding is frequently used as a means of escape from
predators. Dudley and colleagues (2007) in considering its origins in reptiles, pro-
posed that aerial behaviors, including gliding, are natural extensions of arboreal-
ity and of the consequent selection for avoiding injury during falls (dealt with in
greater detail below). Just as in powered flight, gravitational gliding evolved inde-
pendently in three distinctive vertebrate groups, amphibians, reptiles, and mam-
mals. In all three groups the wing is membranous, formed by an extension of the
skin, i.e., in all types of vertebrate flight, whether powered (as in birds and bats
for example) or unpowered, the crucial component is the integumentary system
(Fig. 3.1).

© Springer-Verlag Berlin Heidelberg 2015 105

T. Lingham-Soliar, The Vertebrate Integument Volume 2,
DOI 10.1007/978-3-662-46005-4_3
106 3  Vertebrates Make Their Flight Reservations

Fig. 3.1  Diversity of aerial behaviors and a diagrammatic scenario for the evolution of flight.
Parachuting (left), directed aerial descent at steep angles (center), and classical gliding at shallow
angles (right) represent different stages of aerodynamic control and force production that charac-
terize a broad diversity of arboreal taxa. Flapping flight (top) is hypothesized to derive from con-
trolled aerial behaviors that phylogenetically precede fully articulated wings mg, force of gravity.
Modified from Dudley et al. (2007)

3.1.1 Exploiting the Laws of Physics

The idealized observation of Galileo that all bodies in free-fall accelerate equally
implies that the gravitational force causing acceleration bears a constant relation
to the inertial mass. The critical problem therefore for an animal that is under-
going free-fall is to introduce changes to its form compared to another animal
with a constant mass. At its simplest it would involve, e.g., a change in form that
would increase its drag and consequently reduce its speed of descent. Other more
involved methods will be considered below.
Ulla M. Lindhe (Norberg 1985) stated “a gliding animal needs good control and
stability to be able to retain or adjust flight direction and gliding angle to reach
a particular destination. Even poor gliders have some control and stability. The
selection pressure for control and stability in a gliding proto-bird, proto-bat, and
proto-pterosaur must have been high, probably tremendously higher than for a
proto-bird jumping on the ground after insects, and may have evolved stepwise
and simultaneously with the ability to glide. The evolution of control and stabil-
ity includes the evolution of larger wings and also the ability to coordinate wing
movements (twisting, retraction, etc.). Good control and stability were probably
achieved before true flight evolved” (we will return to flight coordination in Chap. 5).
She proposed that stationary aerodynamic theory could be used to explain passive
3.1  Gliding: Economy Class Air Travel 107

Fig. 3.2  Aerodynamics of gliding. Lift-to-drag ratio, L/D, determines the descent angle θ. R is the
resultant of L and D and must balance the body weight, Mg. Vg and Vs, are gliding and sinking speeds,
respectively. b An increase of the L/D ratio following an increase in wingspan results in a smaller
gliding angle and lower sinking speed than in (a). Starting from a given height, the animal will cover
more ground in a glide as L/D (glide) ratio improves. Decrease of wing loading following increased
wingspan and area will reduce minimum gliding speed, Vg.min. Modified from Norberg (1990)

flight (Fig. 3.2). She found that in passive gliding when an animal takes off from
some elevation, the glide path steepens first and the speed increases to the equilib-
rium speed and that the glide path flattens as equilibrium speed is approached until
the force F (now vertical) becomes equal to the weight, Mg. The resultant force
can be resolved by two components, the drag component D, backward along the
glide path and lift component, L, perpendicular to it. The calculations below are
after Norberg (1985, 1990).
In equilibrium gliding (stable or steady state) the lift and drag equal
L = F cos θ = Mg cos θ , and
D = F sin θ = Mg sin θ
The total drag D is the sum of the wing drag Dw (induced and profile drags) and
the body drag Db (parasite drag). The L/D ratio for the wings alone is better than
that determining the glide angle θ, because the wings’ L/D ratio depends on the
relative magnitudes of the wing and body drag. In equilibrium gliding, the hori-
zontal component of the body drag Db,h equals the horizontal thrust component
T of the wings’ resultant force Rw. In steady gliding at small angles and in level
powered flight with no vertical acceleration, the lift force as averaged over a whole
wing and wing stroke equals the weight, L ≈ F = Mg. Gliding speed Vprop.(Mg/S)

Vg = (2Mg/pSCL )1/2

The lift results from downward deflection of the air passing over the wings and is
defined as
108 3  Vertebrates Make Their Flight Reservations

L = 1/2pCL V 2 S
where p is air density; CL, lift coefficient; V, speed; and S, flight surface. CL is
related to the aspect ratio of the wings and to the wing-profile angle of attack. The
maximum value of CL is obtained just before stall and determines the minimum
gliding speed (see below).
With higher lift coefficients you have lower gliding speeds as well as lower stall in a
gliding animal. The minimum gliding speed, Vg.min, occurs at the maximum obtainable
lift coefficient, CL.max, which means that the minimum stalling speed is approximately

Vg.min = (2Mg/pCL.max S)1/ 2

Hence, proportional to the square root of the wing loading (Mg/S)1/2 (Pennycuick
1975).
The total drag experienced by body and wings during stable gliding is the sum
of the induced drag, Di, and frictional drag, Df (on wings and body combined),
D = Di + Df. In straight unaccelerated glide, the induced drag is
 
Di = 2c(Mg)2 / πpV 2 b2

where c is a constant (=1.1 – 1.2 for airplane wings). This drag component is very
high at slow speeds but becomes smaller when speed increases. The frictional drag is

Df = 1 2pV 2 SCDf ,


where CDf is the frictional drag coefficient. This drag component can be lessened
by smoothing the surface and by streamlining. Di is much higher than Df at slow
speeds, whereas the relative importance of Df increases with speed. An increase of
wingspan, b, reduces Di, and the simultaneous increase of wing area, S, increases
L but also Df. The lower wing loading resulting from the enlarged area also results
in a lower minimum gliding speed. A 25 % increase of wing area would reduce the
gliding speed by about 11 % if the lift coefficient remains constant. An increase
of aspect ratio and, hence, area is very likely to increase the overall lift coefficient
because the gliding animal will then consist of relatively more airfoil and less
body (with poor lift capacity). The potential speed reduction therefore should be
larger still. At low and medium speeds, an increase of span would also increase lift
more than drag, because of the increase of the overall lift coefficient and because
of the overriding importance of induced drag at these speeds. The result is an
increase of L/D and, hence, a flattening of the glide path and increase of its length.
Also noted, during stable gliding at speed Vg the animal loses height at a verti-
cal sinking speed (or rate of sink) Vs,
Vs = Vg sinθ
Norberg (1990) thus suggested that an increase in aspect ratio usually will increase
the overall lift coefficient, resulting in larger potential speed reduction. At low and
medium speeds an increase of span increases lift more than drag because of the
3.1  Gliding: Economy Class Air Travel 109

increase of overall lift coefficient and the overall importance of induced drag at
these speeds, which produces an increase of L/D and a flattening of the glide path.
Norberg (1990, 1985) avoided the rhetoric and emotive arguments that had plagued
the complex questions of vertebrate flight origins by addressing them in mathematical
terms. As it happens, her conclusions support the ‘trees down’ hypothesis of bird flight
and complex question of gliding/partially powered flight origins.
Azuma (2006), however, suggested that wing shape and function might not
always be obvious and predictable in gliding potential. He showed the lift coeffi-
cient of three wings with different planforms, two rectangular and one triangular (a
type of Rogallo wing; Fig. 3.3) as a function of (a) angle of attack and (b) the polar
curve (by plotting drag coefficient against lift coefficient) of these wings. The figure
shows that (1) the low aspect rectangular wing as the lowest lift slope but the high-
est maximum lift coefficient; (2) the flow separation (shaded area) starts early at the
middle part of the low-aspect-ratio rectangular wing, whereas it begins later at the
wing tips of the triangular wing; (3) the triangular wing has the highest lift slope but
the lowest maximum lift coefficient; (4) as the aspect ratio increases, the drag rise in
high angle of attack is reduced; (5) the full stall of the low-aspect-ratio rectangular
wing is milder than that of the medium-aspect-ratio rectangular wing. Thus the very

Fig. 3.3  Aerodynamic conditions of three wings with different planforms, two rectangular and
one triangular (A type of Rogallo wing) as a function of a angle of attack and b polar curves of
these wings. a Lift coefficient. b Polar curve. c Rolled-up vortices. After Azuma (2006)
110 3  Vertebrates Make Their Flight Reservations

low aspect ratio wings as we see had very high drag. For lizards and squirrels, e.g.,
such wing characteristics would allow flight at unexpectedly low speeds as well as
a high angle of attack, which is particularly pronounced as they decelerate sharply
as they land on the vertical surface of the tree at the end of a flight for softer land-
ings. The giant flying squirrel, Petaurista leucogenys, e.g., upon alighting on a tree
flares its body to assume a large angle of attack and reduce its speed so as to land on
the vertical surface of the tree. The low aspect ratio of the wing enables the squirrel
to maintain a high aerodynamic force at slow speed with high angle of attack. The
low aspect wings enable greater stability, reduce the need for complex control and
behavioral mechanisms, are more effective as parachutes and in negotiating their
glides in dense forest canopies (Alexander 2002).
David Alexander (2002) emphasized the relationships among the resultant force,
weight, glide ratio and flight speed. He notes, for any given wing, the lift-to-drag ratio
is controlled by the angle of attack, α (see Chap. 1). Because the glide ratio and the
lift-to-drag ratio are identical, the angle of attack also controls the glide ratio, and
hence the glide angle (Fig. 3.4). What would happen if a glider became heavier, e.g.,
a vulture after a big meal, without changing anything else? If the glider became heav-
ier but the glide angle stays constant it will come down to earth in less time but will
cover the same distance because of the increase of speed. As observed in a number of
flying animals and machines, the lift-to-drag may be related to size—small animals
have low lift-drag-ratios and large animals higher (see RE NO in Chap. 1) (Fig. 3.4b).
The membranous wings of the animals discussed below are all low aspect ratio and
relatively rigid and quite unlike the membranous wings of bats and pterosaurs. In rep-
tiles the aspect ratio of the patagium is about 2 (see below). David Alexander (2002)
raised a number of questions with respect to the low aspect ratio wing in terrestrial
gliders (see aspect ratio and fluid dynamics in Chap. 1). Specifically he asked, given
that the lift-to-drag ratio should be higher for animals with wings of high aspect ratio,
was there a benefit to these animals in having such stubby surfaces or, were such seem-
ingly poor characteristics connected with an early evolutionary stage of flight abilities?
He saw a possible answer to his questions in a study in the early 1930s on aeroplanes
by C.H. Zimmerman and in particular a peculiar property of wings with low aspect
ratio (between 1 and 3), i.e., they could operate at extremely high angles of attack,
which gives them a surprisingly high coefficient of lift and, in addition, greater stability
(a point made by Azuma above). We will return to this important question of stability
in low aspect ratio wings during the course of this chapter. First we will look at the
dramatis personae of gliders living and extinct below, a few in some detail particularly
in the context of interesting recent research, which gives a much better, and sometimes
surprising, understanding of gliding as a locomotory strategy.

3.1.1.1 Amphibians

Frogs are among the earliest tetrapods to adapt to a terrestrial environment. They
may use parachuting to avoid injuries when leaping from trees to escape preda-
tors. All amphibian gliders are able to increase the relative width of their bodies,
3.1  Gliding: Economy Class Air Travel 111

Fig. 3.4  Airfoil section of a wing in horizontal motion and steady gliding, to show relationships
among forces, angles, and speeds. a Steady horizontal motion at angle of attack α, showing lift
(L), drag (D) and the vector sum of lift and drag, called the resultant force (R). Angle θ is the
angle between lift and R. This wing is moving horizontally, so it must be under power, not gliding.
b Tilting the path of movement downward by angle θ makes R exactly vertical, which is the orienta-
tion in a steady glide RH is the resultant force direction in horizontal flight and RG is the resultant
force direction when gliding. c Forces on a wing in a steady glide. The aero dynamic forces sum
to give R, which is exactly equal and opposite to the weight (W). d The distance moved hori-
zontally, dH, divided by the distance moved vertically, dv, in a given time is the glide ratio. The
trigonometric relationship between these distances and the glide angle θ is cotangent (θ) = dH/dv.
This ratio turns out to be the same as the lift-drag ratio, L/D. Dividing dv by the time it took to
descend that distance gives the sinking speed (A.P.). Modified after Alexander (2002)

thereby increasing the surface area exposed to wind resistance. Several Southeast
Asian gliding frogs are true gliders that launch themselves, spread their limbs out-
ward, flatten their bodies dorsoventrally, and control their orientation so that the flat
ventral surface faces the airstream. Other tree frogs have no obvious way of slow-
ing the descent other than by controlling the angle of descent. One species in the
family Hylidae can achieve an angle of descent of about 60° while several other
tree frogs, e.g., Rhacophorus dulitensis in the family Rhacophoridae may achieve
an angle of descent of 45° (Hildebrand 1995). Despite names such as flying frogs,
these amphibians are actually parachuters. As David Alexander (2002) points out,
to make a useful operational distinction between gliding and parachuting, biologists
often use the glide angle: if the glide angle is less than 45°, the lift-to-drag ratio is
greater than 1, so anything with a glide angle less than 45° is considered gliding.
112 3  Vertebrates Make Their Flight Reservations

If the glide angle is greater than 45°, the lift-to-drag ratio is less than 1, and this is
considered parachuting. This is a somewhat arbitrary rule since under some circum-
stances it is perfectly possible to produce lift in, e.g., high glide angles but neverthe-
less provides a practical distinction.

3.1.1.2 Reptiles

Snakes

In gliding snakes the potential lift is generated along the widening body from the
head to the middle. They are capable of gliding some distance when they wish to
move quickly from one tree branch to another or down to the ground. For some
time they were considered as simple parachuters and one species, the ribbon-flat
paradise tree snake, Chrysopelea paradisi, in its natural form was thought to be
permanently adapted to gliding, with an extremely thin and flattened body, which
enables it to ‘fly’ through the jungle canopy airspace. Recent research shows that
the body shape and gliding mechanisms are far more complex.
Members of the genus Chrysopelea inhabit lowland tropical forests in
Southeast and South Asia and have a peculiar behavior: they jump from tree
branches to start a glide to the ground or other vegetation, possibly as a way to
escape a threat or to travel more efficiently. In the flight, the potential lift is gener-
ated along the widening body from the head to the middle where its width is the
maximum. The potential lift is further strengthened when the body takes a snak-
ing form. Azuma (2006) notably indicated the adeptness of C. paradisi at aerial
maneuvers, with maximum upward accelerations and, horizontal velocity at take-
off and lateral undulations during the mid-glide. The glide angle in the last part of
the trajectory was found to be quite shallow at 31° and the best glide ratio (range-
to-height ratio) was an amazingly high 3.7. Azuma interestingly considered that
the normal forces caused by the drag due to the perpendicular flow component
is also generated along the entire length of the body and that the drag is further
increased by the separated flow at the sharp opposite (trailing) edges of the body
resulting in a vortex lift (discussed in Chaps. 1 and 5). This is very interesting in
the context of the latest research on C. paradisi.
Contrary to earlier impressions that suggest that it has a naturally flattened rib-
bon-like body, like all snakes C. paradisi has a cylindrical body with roughly cir-
cular cross-section. But when it glides, this snake reconfigures its body to assume
a flatter profile. Krishnan and colleagues (2014) study on the gliding aerodynam-
ics in C. paradisi shows how the shape of its body cross-section during the glide
plays an important role in generating lift. C. paradisi and other gliding snakes
make use of unique kinematics. The glide begins with a ballistic dive from a tree
branch: the snake launches itself with a horizontal velocity and falls with a rela-
tively straight posture (Fig. 3.5). Immediately after the jump, it spreads its ribs
apart and nearly doubles the width of its body, changing its cross-section from the
cylindrical shape to a flattened shape (Fig. 3.6). Krishnan et al. (2014) present a
3.1  Gliding: Economy Class Air Travel 113

Fig. 3.5  Paradise tree snake, Chrysopelia paradisi. a The paradise tree snake. b Different stages
in a typical glide trajectory of the paradise tree snake. From Krishnan et al. (2014), free access

Fig. 3.6  Artistic impression
of the mechanism that
changes the snake’s body
cross-section for gliding.
a The rib movement is
hypothesized to be directed
both anteriorly (toward the
head) and dorsally (toward
the spine). The sketch is not
to scale and was adapted
from an illustration by
Tara Dalton Bensen in
collaboration with Jake
Socha. b Cross-section of
a typical adult Chrysopelia
paradisi during glide,
modified from a previous
study. From Krishnan et al.
(2014), free access
114 3  Vertebrates Make Their Flight Reservations

Fig. 3.7  Chrysopelia paradisi. a As it moves through the air, the snake undulates laterally, send-
ing traveling waves down the body. The body dimensions have been exaggerated for the sake of
clarity. b Sketch on the right for a proportionally more accurate plan-view of the snake in flight.
After Krishnan et al. (2014), free access

computational investigation of the aerodynamics of the cross-sectional shape. When

it glides, it reconfigures its body to assume a flatter profile. During the glide, the
snake undulates laterally and the parts of the body that are perpendicular to the
direction of motion act as lift-generating wings (Fig. 3.7). To achieve this, they ran
two-dimensional simulations of flow over the anatomical cross-section of the snake
and computed the flow at various angles of attack at low Reynolds numbers start-
ing from Re = 500 and increasing. They found that the incompressible flow past
the anatomically correct cross-section of the species C. paradisi showed a signifi-
cant enhancement in lift at a 35° angle of attack, above Reynolds numbers 2,000
(Fig.  3.8). Thus, they were able to capture some of the unique lift characteristics
observed in the physical experiments of earlier workers. Their primary aim there-
fore was to explain the enhanced lift mechanism by analyzing vorticity visualiza-
tions of the wake, time-averaged pressure fields, surface pressure distributions,
swirling strength, and wake-vortex trajectories (Fig. 3.9). They found the flow is
inherently three-dimensional in physical experiments, due to fluid instabilities,
and it is thus intriguing that the enhanced lift also appears in the two-dimensional
simulations. The simulations point to the lift enhancement arising from the early
separation of the boundary layer on the dorsal surface of the snake profile, without
stall. The separated shear layer rolls up and interacts with secondary vorticity in the
near-wake, inducing the primary vortex to remain closer to the body and thus cause
enhanced suction, resulting in higher lift (Figs. 3.8 and 3.9).
Krishnan et al. (2014) note that at least thirty independent animal lineages
have evolved gliding flight but only one animal glides through the air without any
3.1  Gliding: Economy Class Air Travel 115

Fig. 3.8  Pathlines of the centers of the coherent vortices in the wake at different AOA and Re
No. Clockwise vortices have been represented by blue dots and counter-clockwise vortices by
red dots. Points of the same darkness and size represent the positions of the vortices at the same
instant in time. Consecutive points are separated by the same periods of time (0.256 units). More
than one point with the same color indicates the presence of more than one vortex at that instant.
Note that the dorsal vortex stays closer to the body for a longer period of time at AOA 35° and
Re = 2,000. From Krishnan et al. (2014), Free access. a Re = 1000, AOA 30°, b Re = 1000,
AOA 35°, c Re = 2000, AOA 30°, d Re = 2000, AOA 35°

appendages, the gliding snake. They believe that such diverse solutions in animal
locomotion as that of C. paradisi are encouraging engineers to turn toward nature
for inspiration and promote the fields of biomimetics and bioinspired design.

Lizards

Lizards among the south-east Asian genus Draco have unusually adapted ‘wings’.
The best-adapted gliding lizards have an extensive skin membrane or patagium
extending on either side of the body from the thorax to the base of the hind leg
that opens laterally like a fan. Because the expanded lateral surface of the body
increases the wind resistance against the body, the speed of falling is reduced. The
directions of gliding can be controlled by adjusting the surface area—to curve to
the right, the right patagium is relaxed. These lizards are capable of low gliding
angles of 20–30° and may even gain elevation if they move into an updraft, with
glides of 24 m being observed (Hildebrand 1995). Gliders can land on vertical sur-
faces by suddenly turning the anterior end of the body up as it reaches the sur-
face. Mechanically, this stalls the flight—i.e., the horizontal component of flight is
eliminated.
116 3  Vertebrates Make Their Flight Reservations

Fig. 3.9  Vorticity in
Chrysopelia paradisi in
Re = 2,000, AOA = 35°.
a A single vorticity contour
a series from −25 to +25 in
steps of 2 (Krishnan et al.
2014). Contour lines of
negative values of vorticity
are blue and the contours
of positive values are red.
b A summary of the major
features found in the near-
body wake. Modified from
Krishnan et al. (2014), free
access

Russell et al. (2001) made a detailed study of the patagial morphology of

Draco volans. They showed that the Draco patagium is unique among living ani-
mals in that it is an actively controlled structure supported by elongated thoracic
ribs and a specialized musculature. The musculature that controls the patagium
is composed of highly modified external and internal intercostal muscles, exter-
nal oblique muscles, and a system of ligaments spanning the individual elongated
thoracic ribs. This type of patagium is able to be erected and folded at will, and its
configuration can be adjusted in flight, giving a much more controllable combi-
nation of aerodynamic surfaces, differing significantly in these respects from the
patagium in the parachuting geckos Ptychozoon and Cosymbotus. The recruitment
of intercostal muscles for patagial control resulted in a profound reorganization of
the respiratory apparatus. Whereas all other lizards ventilate their lungs primar-
ily through expansion and contraction of the rib cage via the intercostal muscles,
the provisioning of power for ventilation by Draco has been shifted to the pecto-
ralis muscles (McGuire and Dudley 2011, and references therein). McGuire and
Dudley show a number of additional and less familiar features that add to the func-
tional sophistication of gliding in the genus Draco such as elongated and mobile
3.1  Gliding: Economy Class Air Travel 117

ceratohyal cartilages in their hyoid apparatus (present in most lizards) that support
laterally extensible throat lappets, which is thought to function as a smaller and
secondary anterior airfoil to generate extra lift and enhance balance and stability.
In addition all species of Draco also have modified streamlined hind limbs and
elongated fringing scales on the base of the tail that serve to further increase the
effective aerodynamic surfaces (Fig. 3.10).
McGuire and Dudley (2011) note, among lizards, patagial structures are not
unique to Draco. For example, a patagium is also present in at least two other
extant lizard assemblages, the flying geckos of the genus Ptychozoon, and the
geckos Hemidactylus craspedotus and H. platyurus. However, the patagium
in Ptychozoon and Hemidactylus is relatively small and is unsupported by an
underlying skeleton or by sophisticated musculature, and thus must open pas-
sively as it catches air during controlled aerial descent. As we will see further on,
although unique to modern reptiles, structures similar to the patagium of Draco
evolved repeatedly and convergently in other extinct gliding reptiles including
Kuehneosaurus, Icarosaurus, Coelurosauravus as early as the Late Triassic period.

Fig. 3.10  The relationship between wing loading and height lost over the course of a standard
glide length of 9.3 m (from McGuire and Dudley 2005). Black dots represent the original empiri-
cal observations of Draco on which the regression analysis was based. Last and penultimate dots
represent the inferred points along the Draco-specific regression for Kuehneosaurus sp. and C.
elivensis, respectively, based on published estimates of wing loading. Gray dots represent three
alternative positions along the regression for I. seifkeri depending on whether wing loading is
based on estimates of body mass obtained from (A) a published regression of SVL on body mass
across a diversity of lizard species, (B) a regression of SVL on body mass for female Draco, or
(C) a regression for male Draco. Modified from McGuire and Dudley (2011)
118 3  Vertebrates Make Their Flight Reservations

Surprisingly, flying lizards exhibit isometry (i.e., geometrical similarity) in

their wing area—body mass relationships (as opposed to functional similarity
see Chap. 1). Wing loadings of larger species are consequently substantially
higher than those of smaller species, suggesting higher equilibrium glide speeds
(Fig.  3.10). McGuire and Dudley (2011) hypothesized, on the basis of known
area-mass scaling relationships and aerodynamic theory, that large Draco spe-
cies are relatively poor gliders relative to their smaller congeners. More spe-
cifically, they predicted, first, that larger species require greater absolute glide
velocities in order to generate sufficient lift, given that their wings must support
greater mass per unit area; second, that the need for greater velocities conse-
quently requires longer ballistic dives such that larger species lose more height
over the course of standard glide distances; and third, that longer ballistic dives
result in increased glide angles for larger species. Their expectation was that
there would be positive correlations between wing loading and each of these
performance parameters. Comparative analysis confirmed that larger species
are relatively poor gliders and do not compensate substantially for their higher
wing loadings via either behavioral or physiological mechanisms. Flying lizards
were found to exhibit substantial context-dependent variation in glide perfor-
mance, with smaller species often exhibiting extensive variation in height lost
and glide angle between trials. The authors emphasized that the most important
performance parameters evaluated in their study—height lost over the course
of a standard glide distance and the correlated total glide angle—are generally
not considered in theoretical treatments of animal gliding. Rather, steady state
aerodynamics are emphasized, with the glide angle generally considered only
from the standpoint of the equilibrium phase of a glide (the equilibrium glide
velocity is a theoretical expectation under steady state aerodynamics that maxi-
mizes the lift-to-drag ratio and minimizes the glide angle; see Norberg (1990)
and above). From an ecological perspective they argue that the total height lost
over the course of a glide (and the corresponding total glide angle, including the
ballistic dive component) may have more direct fitness consequences than the
more restricted parameter of total height lost during the equilibrium portion of a
glide. The overall conclusion is that larger species have not evolved compensa-
tory biomechanical or morphological mechanisms that might have allowed them
to overcome their substantially greater wing loadings.

3.1.1.3 Mammals

Squirrels

There are 43 recorded species of gliding squirrels. Two species are North
American, two live in northern Eurasia, and all others are found in the temperate
and tropical forests of India and Asia. In “flying” squirrels a considerable range of
body size exists among the 14 genera. Some giant flying squirrels of tropical India
and southeastern Asia weigh 1–2.5 kg and have a body length of about 30–60 cm
3.1  Gliding: Economy Class Air Travel 119

and a tail 35–64 cm long. The smallest are the dwarf flying squirrels (Petaurillus)
of northern Borneo and the Malay Peninsula; their bodies are just 7–9 cm long and
their tails 6–10 cm. In some forms of the giant oriental flying squirrels (Petaurista)
glides of up to 450 m (almost 1,500 ft) have been recorded (Enc. Brit. 2005).
In some members of the scaly tailed squirrels (family Anomaluridae) the very
large membranes are supported in part by long cartilaginous struts, or calcars,
from the elbows. Some “flying” squirrels (family Sciuridae) have shorter struts
from the wrists that support the front part of each membrane alongside the body
(these will be discussed further below). Usual glides are 6–10 m in length at angles
of 30–60° to the ground although an American species was seen to glide 50 m with
a drop of only 18 m (Hildebrand 1995), however as Milton Hildebrand points out,
such figures mean little as all gliders within reason seem able to glide as far as they
“want” to, perceptively underscoring the idea that there is perhaps more control in
these activities than previously considered. This idea we will see developed further
in a number of studies below.
David Alexander notes, at first glance the low aspect ratio wings of reptiles
(calculated ~1.7–2.3) and squirrels would not seem to be particularly effective
wings. One possible answer he suggests is that a significant amount of lift may
be generated by the rest of the body. Also we have seen above (e.g., in early work
by Zimmerman and later work in Azuma (2006)) that other factors such as high
angle of attack may compensate for the low aspect ratio. The important question
of steady-state versus unsteady-state aerodynamics involved in low aspect ratio
wings will be explored further below (Fig. 3.11).

Fig. 3.11  Flying squirrel, Petaurista leucogenys. Wiki Commons photo

120 3  Vertebrates Make Their Flight Reservations

Bahlman et al. (2013) in their study on northern flying squirrels questioned the
frequent use of a gliding model advocating an equilibrium (steady-state) in which
aerodynamic forces exactly balance body weight resulting in constant velocity.
They suggest that while the model is relevant for long-distance gliding, such as
soaring by birds, it may not be realistic for shorter distances between trees. To
understand the aerodynamics of inter-tree gliding, they used direct observation,
videography (60–125 fps) to track and reconstruct the three-dimensional trajecto-
ries of northern flying squirrels (Glaucomys sabrinus) in nature and mathematical
modeling. From their trajectories, they calculated velocities, aerodynamic forces
and force coefficients. The authors were able to determine that flying squirrels do
not glide at equilibrium but instead they showed continuously changing velocities,
forces and force coefficients, and generate more lift than needed to balance body
weight (see below).

Culugos

The colugo, a cat-sized Asiatic glider Cynocephalus constitutes the primitive mam-
malian order Dermoptera, of which perhaps only two species exist. They are lemur-
like (not lemurs), gliding mammals closely related to primates, and nocturnal in
habit. They are found only in the East Indies and certain of the Philippine Islands.
Colugos resemble large flying squirrels, with lateral skin membranes that form
the largest “flight” membranes of all: it extends from the throat to the wrists to the
ankles to the tip of the tail. Even the large feet have webbed toes. They have been
observed to sail 136 m at only 5° to the horizontal (Hildebrand 1995). One form
(Cynocephalus) beats the tail up and down in a fanning motion, a locomotory tech-
nique effective in reducing drag or improving gliding performance (Azuma 2006).
A study by Byrnes and colleagues (2008) presents interesting results on how glid-
ing mammals such as the colugo avoid a significant risk of injury during long-dis-
tance leaps (below) (Fig. 3.12).
Byrnes et al. (2008) examined the locomotor dynamics of free-ranging glid-
ing mammals, the colugo using custom-designed three-dimensional accelerometry
system. It allowed them to examine the take-off and landing forces associated with
leaps or glides covering distances ranging over two orders of magnitude (~2.5–
150 m) given that previous laboratory studies on leaping and gliding animals
revealed a discrepancy in the relative magnitudes of take-off and landing forces,
depending on the measurement technique used. Although landing forces have been
shown to increase with distance in both primates and flying squirrels (Demes et al.
1999; Paskins et al. 2007), their study, over a wider range of distances, showed
that the opposite is true in free ranging colugos. If forces were to continue to
increase linearly, the probability of injury on landing would also increase, espe-
cially over the glide lengths observed in this study. However, their results show
a negative relationship between glide duration and peak landing force over a
naturally occurring range of glide distances. Landing forces decrease rapidly as
glide distance increases from the shortest glides, then level off, suggesting that the
3.1  Gliding: Economy Class Air Travel 121

Fig. 3.12  Malayan colugo,
Galeopterus variegatus.
Relationships between glide
duration and a peak landing
force, b take-off impulse
and c landing velocity.
Line through each set of data
points is the mixed-model
regression, controlling for
individual identity. In a, the
curvilinear relationship is
shown to illustrate the rapid
decrease in peak force over
short glides as duration
increases up to 2 s. After
Byrnes et al. (2008)
122 3  Vertebrates Make Their Flight Reservations

ability to reorient the aerodynamic forces prior to landing is an important mecha-

nism to reduce velocity and thus landing forces. This ability to substantially alter
the aerodynamic forces acting on the patagial wing in order to reorient the body is
a key to the transition between leaping and gliding and allows gliding mammals
to travel long distances between trees with reduced risk of injury. We will also see
below that this kind of control, both muscular and neurological may have other
benefits in the evolution of powered flight.

3.1.1.4 Fossil Gliders

In the golden age of reptiles during the Mesozoic era some forms of lizards were
the first vertebrates to take to the air and they did it in their own unique way.
Icarosaurus siefkeri, described from the Upper Trias of New Jersey, was morpho-
logically similar to Draco in that it had patagia supported by elongated hollow
ribs. The snout-vent-length (SVL) of I. siefkeri has been estimated to be 95 mm
(Colbert 1970; McGuire and Dudley 2011), similar to that of the living “flying
lizard” Draco (Colbert 1970; Carroll 1978). Kuehneosuchus (‘Plesiodraco’) and
Kuehneosaurus from the Upper Triassic of Great Britain were two other glid-
ing lizards. Both had enormously elongated ribs, which are believed to have
supported a membrane (Halstead 1969, and references therein). Because sev-
eral fossil lineages share with Draco similar morphological features for gliding
including patagial membranes supported either by elongated ribs or, in the case of
Coelurosauravus (Frey et al. 1997) by rib-like ossified dermal structures, McGuire
and Dudley (2011) considered it possible to predict their locomotor capabilities
using morphological considerations alone and to investigate the relative gliding
performance of these individuals that represent early evolutionary experiments
in vertebrate flight. Some of these fossil gliders were substantially heavier than
Draco and have been inferred to have had much greater wing loadings. Because
the aerodynamic structures of these taxa were similar to those of Draco, the
authors were able to use associated regression analysis to predict the gliding per-
formance of these extinct taxa and because the fossil lineages differed from Draco
in having higher aspect ratio wings they therefore employed wind tunnel experi-
ments to determine the relative compensatory value that wings with high aspect
ratio might have provided for the fossil gliders and to evaluate whether predic-
tion of gliding performance using wing loading alone is justified for these fos-
sil lineages. Despite significant differences in body mass and lifting surface area
and shape within the three lizards studied the authors used the reduced major axis
(RMA) regression equation derived from the empirical study of gliding perfor-
mance of extant flying lizards (McGuire and Dudley 2005) to estimate aerodynam-
ics of the fossil taxa and estimate absolute gliding performance for each taxon by
extrapolating from Draco’s wing loading/glide performance relationship.
An important problem the authors had to address was the aerodynamic differ-
ence between fossil species and Draco i.e., how variation in aspect ratio as well
as wing loading might influence gliding performance, with relatively longer wings
3.1  Gliding: Economy Class Air Travel 123

expected to increase the lift: drag ratio and consequently improve glide perfor-
mance during the equilibrium phase of a glide (Norberg 1990). However, based
on unpublished data they were able to hypothesize that for gliders in the size range
of Draco and their fossil analogs, that wing loading will have substantially greater
influence on relative performance than would aspect ratio, especially given that the
concern is with the total height lost over a standard glide—justifying the associ-
ated regression they used to estimate the performance of the fossil gliders based
on their empirically derived relationship between wing loading and height lost by
Draco.
McGuire and Dudley’s (2011) analysis suggests that the small-bodied fossil
reptile Icarosaurus seifkeri was the best nonflapping (i.e., nonavian, nonchirop-
teran, and nonpterosaur) terrestrial vertebrate glider yet discovered. In contrast,
the large-bodied Kuehneosaurus and C. elivensis must have been relatively poor
gliders relative to Icarosaurus and modern Draco lizards. Even moderately sized
gliders pay a substantial penalty relative to smaller species given their increased
wing loadings. The large-bodied Kuehneosaurus and Coelurosauravus would have
performed shallow-trajectory glides at high velocities, consequently requiring an
extended ballistic dive and a loss of substantial height with each gliding event.
This finding suggests that these species must have occurred in very tall forests
such as those occupied today by Draco and a preponderance of other gliding line-
ages. Their findings further suggest that powered flapping flight, if indeed derived
from gliding behavior, likely originated in smaller species that later evolved larger
body size in conjunction with biomechanical innovations that overcame the physi-
cal constraints of body mass relative to wing area.
In his fascinating book Riddle of the Feathered Dragons, Alan Feduccia (2012)
writes of two other well published “flying” reptiles from the Triassic period,
Mecistotrachelos and Sharovipteryx mirabilis, which will consequently be men-
tioned only briefly here. Mecistotrachelos was a diapsid lizard-like lepidosaur
from the Late Triassic of Virginia, USA. It resembled living gliders such as Draco,
gliding on wings formed by extensions of the membranous skin supported by
elongated ribs. Sharovipteryx was a small gliding archosauromorph reptile with
short forelimbs, very long hind limbs and a long tail. More recently it has been
reconstructed with triangular shaped leathery patagial wings, which the authors
Dyke and colleagues (see references in Feduccia 2012) argue allowed it to glide in
a manner similar to a delta-winged jet (see Fig. 3.3 above for aerodynamic charac-
teristics of rectangular and triangular wings) (Fig. 3.13).
During the Jurassic and Cretaceous the experiment of non-powered reptile
flyers continued. Recently a new gliding lizard, Xianglong zhaoi was reported
from the Early Cretaceous of China by Li and colleagues (2007) (Fig. 3.13). The
authors show that Xianglong had clear gliding adaptations in a suite of rare gliding
capabilities. The most obvious is explicitly demonstrated by a patagium or loose
fold of skin internally supported by eight greatly elongated dorsal ribs. Li and
colleagues (2007) make some interesting comparisons with the patagium and the
wings of powered fliers that are critical to flight performance according to aero-
dynamic theory, such as much greater transverse width of the patagium compared
124 3  Vertebrates Make Their Flight Reservations

Fig. 3.13  Xianglong zhaoi holotype (LPM 000666). a Photograph and, b Line drawing. cv

­caudal vertebrae; ch ceratobranchial process of hyoid apparatus; dr dorsal ribs; lc left clavicle;
f left femur; lfi left fibula; lt left tibia; md I–V manual digits I–V; pd I–V pedal digits I–V; pls
pelvis; rh right humerus; rr right radius; rsc right scapulocoracoid; ru right ulna; sk skull. Scale
bar 2 cm

with the anterio-posterior length, a significantly thickened leading edge relative to

a thin trailing one, and a tapered wing tip. The latter is sporadically distributed but
not common in gliding tetrapods. Interestingly too, is Xianglong’s patagium sur-
face, which is mostly naked and as mentioned above is strengthened by tough col-
lagen fibers, that run parallel to the ribs and which are particularly well developed
along the trailing edge (Fig. 3.14) a feature otherwise known only in true fliers
such as pterosaurs and the enigmatic reptile Sharovipteryx.
An important adaptation with respect to its gliding lifestyle and differing from
the majority of the Squamata, which are ground living, Xianglong shows clear
climbing adaptations suggestive of an arboreal habit, which includes the follow-
ing: a curved manual and pedal digit I, elongate penultimate manual and pedal
phalanges, a greatly elongated pedal digit V, and strongly curved manual and pedal
claws (Li et al. 2007 and references therein).
Remarkably, Xianglong is estimated to have a wing loading of 0.24 g/cm2
(23.5 N/m2), an aspect ratio of 6.5, and an outer area proportion of 8 %. This is
quite amazing when we consider that Draco and flying squirrels both have wing
3.1  Gliding: Economy Class Air Travel 125

Fig. 3.14  Close-up of LPM 000666. a Cranial region showing skull roof scales and gular flap.
b Anterior trunk region showing scales along dorsal series, left arm, and leading edge of the pata-
gium (counterpart). c Left manus. d Left pes. e Collagen fibers along trailing edge of the pata-
gium (counterpart). Scale bars a–d, 3 mm; e, 1 mm

loadings of 40–50 N/m2 given that to a large extent wing loading controls speed
(Alexander 2002; also see the allometry of gliding performance in Draco above),
On the other hand the ratios proposed for Xianglong, according to the authors, are
close to those in fast-flying birds with great maneuverability, such as passeriformes.
Interestingly, Xianglong provides the first evidence of an Early Cretaceous ecologi-
cal diversification into an aerial niche by crown-group squamates.
Among fossil mammals, Eomys, a well preserved rodent (Family Eomidae)
discovered in the fossil laggerstatte of late Oligocene age in Bad Marienbad,
Germany was described by Storch and colleagues (1996; Fig. 3.15). It shows
126 3  Vertebrates Make Their Flight Reservations

traces of a gliding membrane on one side of the body, making it the fourth rodent
family to have developed by parallel evolution a gliding form of locomotion.
Gliding opened up many new opportunities to phylogenetically unrelated ani-
mals mentioned above, which would form a key part in their evolutionary survival

Fig. 3.15  Skeleton of Eomys quercyi. with preserved soft body outline from the late Oligocene
of Enspel, Westerwald, Germany (Naturhistorisches Museum, Mainz, specimen 5803/G3S16,
found in 1992). Length of head and body, about 10 cm; skull length, 3 cm. a The carcass shows
thick fur along its left side (above) and the sparsely haired, thin gliding membrane along the right
side. b Reconstruction of Eomys quercyi from Enspel during gliding locomotion. The distal part
of the tail is not preserved and its reconstructed length is about 10 cm. Small gliders such as
Eomys quercyi have low wing loadings, and are thus adapted to a maneuverable and slow ‘flight’
in densely forested areas where there is little air turbulence. Abundant fossils of leaves, fruits and
seeds prove the existence of a thick mesophytic forest around where the rodent was found, and
this forest type was widespread in western and central Europe during the late Oligocene. Modi-
fied after Storch et al. (1996), Courtesy of Macmillan Press Ltd
3.1  Gliding: Economy Class Air Travel 127

strategy. For others it would perhaps have started in a similar way, i.e., of contend-
ing with the forces of gravity that forced them downward by extending the fall
horizontally but they would take it a step further. It is easy to envisage how this
might have happened—perhaps in a last-ditch attempt to capture a flying insect
the gliding vertebrate desperately attempted to flap its membranous wings with
the available incipient musculature or perhaps it happened as a consequence of
misjudging the distance while attempting to land on a branch on an adjacent tree
(Dudley et al. 2007). Whatever the reasons, before the close of the Triassic period
the early gliding developments discussed above would lead to the first true fly-
ing vertebrates among the Archosauria. Initially it involved further development of
the stretched membranous skin or patagium and importantly, the development of
special sets of muscles to control its movements. These early true fliers were the
pterosaurs (Chap. 4).
These examples are the beginning of vertebrate attempts to make use of the
air either as predator or prey. But they were all unpowered, dependent entirely on
gravity. We have considered some of the aerodynamic principles that made gliding
a viable locomotory strategy among vertebrates and will look at it specifically in
birds in Chap. 5.

3.1.2 Evolution of Flapping Flight: Is a Transition

from Gliding Flight Possible?

Perhaps, it is important not to retrospectively confuse the evolution of the gliders

described above as part of the way to some greater level of aerodynamic success.
Rather, they may be perfectly adapted for what they “want.” David Alexander
(2002) summed up the evolution of these gliders well when he said: “Far from
being an early step on the way to becoming bats or pterosaurs, these animals are
actually well adapted to their lifestyles and habitats.” However, that is not to say
that in the course of evolution some gliders might not have ventured further to
powered flight. Archaeopteryx has long been regarded as the classic ‘intermedi-
ate” animal in this sense. However, opposition to a transition from a gliding-to
a powered-flight stage has in cases been quite vocal and championed, in par-
ticular, by proponents of the ground-up theory of flapping flight (see Chap. 4).
The following criticisms as noted by Ulla M. Lindhe Norberg sums up some of
the key objections. (1) It might be assumed that the first birds flew from branch
to branch, but landing on a branch would be impossible without well-developed
stability control. The landing process is critical to all the theories of the origin of
flight. (2) Animals that had lift and thrust but could not control their bodies could
not successfully evolve true flight. (3) Small increments of lift add only minute
distances to the glide-path length. (4) Powered flight could not have developed
from gliding, since flapping would dramatically reduce lift. (5) Achieving the
vortex rings produced by wing strokes must be a principal problem for animals
to solve in evolving flight. (6) A change from gliding to powered flight requires
128 3  Vertebrates Make Their Flight Reservations

extensive distal development of a lifting surface, with ensuing increase of aspect

ratio, extensive enough to overcome the effects of drag caused by the proximal
lift surface. (7) Gliders are structurally and aerodynamically different from active
fliers. (8) Gliding is a perfectly good adaptation, an adaptive plateau that need not
lead to further specialization. (9) Gliding and active flight are used for different
things (see Norberg (1990) for the above citations in her summary of the argu-
ments above).
As we saw at the beginning of the chapter, Norberg (1985, 1990) considered
these objections as unfounded and lacking in adequate explanations but that rather
the functional transition from gliding to flapping is biomechanically feasible. She
considered that when the wing-stroke speed is relatively low, the quasi-stationary
theory would be adequate to explain the transition. When flapping amplitudes and
velocities become large relative to the flight speed, nonstationary (vortex) phe-
nomena become important. Hence, based on mechanical and aerodynamic cal-
culations she found that there are no serious problems with transitions from the
stationary aerodynamics of gliding, via the quasi-stationary state of gliding with
incipient flapping, to flight with unsteady aerodynamics predominating. Her model
showed that even slight flapping in a gliding animal can produce a horizontal net
thrust force while the necessary vertical lift is still maintained, resulting in a shal-
lower glide path. Her model also showed that, regardless of the amount of flap-
ping, the various flight variables always combine in such a way that the vertical
lift produced during one complete wing stroke in partially powered flight always
equals the weight of the animal (as in gliding with no flapping).
Dudley et al. (2007) examined the full continuum of aerial behaviors and place
the origin of flight within a specific functional context relating to arboreality and
either inadvertent or intentional descent. In particular, they suggest that the numer-
ous evolutionary experiments in gliding and controlled descent may be inevitable
consequences of living within vegetational structures elevated above the ground.
The evolution of gliding can they say be cast as a multistep process initiated with
an aerial righting reflex, and then followed by behavioral adaptations such that the
falling lizard assumes a characteristic splayed posture with the body and tail ori-
ented in the horizontal plane while falling. This allows the lizard to maximize drag
and thus to parachute to the ground at a reduced velocity relative to that of a tum-
bling lizard. Once a lineage has acquired these behavioral adaptations, then any
increase in relative surface area will improve parachuting. Gliding and associated
lateral displacement of the body via lift forces, in turn, facilitate targeting of land-
ing sites off the ground, where predatory pressure may otherwise be formidable.
Although only a few species of arboreal lizards have been observed to utilize the
characteristic parachuting posture, they hypothesize that this is in fact a general
feature of arboreal lizards.
The stumbling block as far as some workers are concerned (see above) is
the transition from steady state gliding aerodynamics to unsteady state aerody-
namics of flapping flight. However, Dudley et al. (2007) propose a biomechani-
cally ­parsimonious hypothesis for the evolution of flapping flight in terrestrial
3.1  Gliding: Economy Class Air Travel 129

vertebrates suggesting progression within an arboreal context from jumping to

directed aerial descent, gliding with control via appendicular motions, and ulti-
mately to powered flight. The more than 30 phylogenetically independent line-
ages of arboreal vertebrate gliders they suggest lend strong indirect support to
the ecological feasibility of such a trajectory. They provide ample evidence in
animals that demonstrate the biomechanical capacity for directed aerial descent
in the complete absence of wings, which they say points to a critical apprecia-
tion of the role of the sensory and biomechanical mechanisms involved in extant
gliding animals to control and orient their descent—and central to deciphering
pathways involved in flight evolution. This idea is developed further in the study
by Bahlman and colleagues.
Bahlman et al. (2013), based on their findings on non-equilibrium glides in
northern squirrels, considered the question of the potential evolution of a flapping
flyer from a gliding ancestor. A fundamental problem that has beset the question
is that much of the discussion about the plausibility of this transition starts with a
passive glider at equilibrium, and focuses on changes in wing length to increase
lift and development of a downstroke to redirect lift into thrust. It has also been
suggested that a gliding to flapping transition is not mechanistically possible
because motions of a glider’s wing that increase or redirect force would reduce lift
and stability and cause the animal to fall faster. Therefore, an evolutionary transi-
tion from gliding to flapping requires sensory, motor, and behavioral capabilities
that can compensate for the instabilities in motion and airflow that reduce glide
performance. Bahlman et al. (2013) propose that the following are particularly cru-
cial for any gliding to flapping transition: the ability to detect the effect of airflow
on body accelerations and rotations; the ability to control body accelerations and
rotations in and about all three axes; and the ability to generate lift greater than
body weight. A glider with these sensory, motor, and behavioral abilities could
be a plausible intermediate between an equilibrium glider and an animal capable
of stable flapping flight, and would be exapted for powered flight (see Maynard
Smith in Chap. 5). They suggest that findings that show the ability of northern fly-
ing squirrels to perform consistent and repeatable glides in an aerodynamic regime
where unsteady forces are dominant is an indication that the squirrels have the
ability to sense and respond to their motion and surroundings allowing them to
detect body accelerations, rotations, and changes in position as well as the abil-
ity to detect changes in flow over the wings that enables rapid responses to rel-
evant aerodynamic cues. Such behavioral responses to unpredictable pressure and
flow gradients and a nervous system able to sense changes in flow and to effect
appropriate compensatory responses, the authors say would be highly advanta-
geous during gliding. The complexity of the arboreal habitat that demanded dra-
matic changes in behavior and mechanics, in particular involved in the execution
of inter-tree glides, may have been, as a number of recent studies have shown, the
ideal environment for the evolution of flapping flight.
130 3  Vertebrates Make Their Flight Reservations

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Alexander DE (2002) Nature’s flyers: birds, insects, and the biomechanics of flight. John
Hopkins University Press, Baltimore and London
Azuma A (2006) The biokinetics of flying and swimming, 2nd edn. American Institute of
Aeronautics and Astronautics Inc, Blacksburg
Bahlman JW, Swartz SM, Riskin DK, Breuer KS (2013) Glide performance and aerodynam-
ics of non-equilibrium glides in northern flying squirrels (Glaucomys sabrinus). J Roy Soc
Interface 10:10
Byrnes G, Lim NT-L, Spence AJ (2008) Take-off and landing kinetics of a free-ranging gliding
mammal, the Malayan colugo (Galeopterus variegatus). Proc Roy Soc B 275:1007–1013.
doi:10.1098/rspb.2007.1684
Carroll RL (1978) Permo-Triassic ‘‘lizards’’ from the Karoo System, Part II, a gliding reptile
from the upper Permian of Madagascar. Palaeont Afr 21:143–159
Colbert EH (1970) The Triassic gliding reptile Icarosaurus. Bull Am Mus Nat Hist 143:85–142
Demes B, Fleagle JG, Jungers WL (1999) Take-off and landing forces of leaping strepsirhine
primates. J Hum Evol 37:279–292. doi:10.1006/jhev.1999.0311
Dudley R, Byrnes G, Yanoviak SP, Borrell BJ, Brown R, McGuire JA (2007) Gliding and the
functional origins of flight: biomechanical novelty or necessity? Ann Rev Ecol Evol Syst
38:179–201
Feduccia A (2012) Riddle of the feathered dragons: hidden birds of China. Yale University Press,
New Haven
Frey E, Sues HD, Munk W (1997) Gliding mechanism in the late Permian reptile
Coelurosauravus. Science 275:1450–1452
Halstead (1969) Pattern of vertebrate evolution. Oliver and Boyd, Edinburgh
Hildebrand M (1995) Analysis of vertebrate structure, 4th edn. Wiley, New York
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McGuire J, Dudley R (2005) The cost of living large: comparative gliding performance in flying
lizards (Agamidae: Draco). Am Nat 166:93–106
McGuire J, Dudley R (2011) The bology of gliding in flying lizards (Genus Draco) and their fos-
sil and extant analogs. Integr Comp Biol 1–8 (July). doi:10.1093/icb/icr090
Norberg U (1985) Evolution of vertebrate flight: an aerodynamic model for the transition from
gliding to active flight. Am Nat 126:27–303
Norberg UM (1990) Vertebrate flight. Springer-Verlag, Berlin
Paskins KE, Bowyer A, Megill WM, Scheibe JS (2007) Take-off and landing forces and the
evolution of controlled gliding in northern flying squirrels Glaucomys sabrinus. J Exp Biol
210:1413–1423. doi:10.1242/jeb.02747
Pennycuick CJ (1975) The mechanics of flight. In: Farmer DS, King JR, Parkes KC (eds). Avian
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Storch G, Engesser B, Wuttke M (1996) Oldest fossil record of gliding rodents. Nature
379:439–441
Chapter 4
Flight by Membrane

We saw in Chap. 3 that many groups of vertebrates employed membranes or

extensions of the skin in gliding flight. However, there are only two groups of ver-
tebrates that use membranous wings in flapping or powered flight, one, the extinct
pterosaurs, and the other, extant bats.

4.1 The First True Fliers, Pterosaurs

A classic case of convergent evolution is seen in thunniform swimmers involv-

ing four phylogenetically disparate groups of vertebrates, lamnid sharks, tuna,
dolphins and ichthyosaurs (Chaps. 1 and 2). Flapping flight among vertebrates
is another classic example of convergence in which reptiles, mammals and birds
solved the problem of conquering the air in highly distinctive and innovative ways
dictated by the constraints of their different biological makeups. In this chapter we
concentrate on pterosaurs (reptiles) and bats (mammals).
Popular reports and the movies have imprinted upon our minds images of
pterosaurs as gigantic flying reptiles just as their land counterparts the dino-
saurs were for many years portrayed as enormous lumbering beasts. Most ptero-
saurs were small, about the size of seagulls but just as with the dinosaurs some
were indeed giants. Two major groups of pterosaurs have been recognized, the
Rhamphorhynchoidea from the Late Triassic Period and the later Pterodactyloidea
from the Late Jurassic to Cretaceous Periods (Fig. 4.1). Rhamphorhynchoids
differed significantly from the Pterodactyloidea. They were small, e.g.,
Rhamphorhynchus was about 50 cm long, with a long skull and large eyes and
pointed, forwardly sloped, interlocking teeth (probably adapted to feeding on fish),
short metacarpals and a long tail terminating with a rudder-like flap. Dimorphodon,
like other early pterosaurs, had a long tail that probably helped stabilize it during
flight. It also had a large breastbone and a large crest on the humerus to which

© Springer-Verlag Berlin Heidelberg 2015 131

T. Lingham-Soliar, The Vertebrate Integument Volume 2,
DOI 10.1007/978-3-662-46005-4_4
132 4  Flight by Membrane

Fig. 4.1  Pterodactylus kochi
(Wagner). Pterodactyloid
specimen from the Solnhofen
limestone in Bavaria.
Modified from Wellnhofer
(1987)

the powerful flight muscles were attached. Like all but the largest pterosaurs, it is
believed that Dimorphodon was well suited for flapping flight.
Pterodactyloids are distinguished from basal pterosaurs by their reduced
teeth, tail, and fifth toe. The metacarpals (palm bones) were more elongated
than those of earlier pterosaurs, which instead had elongated phalanges (finger
bones). Pterodactylus a Late Jurassic form from Germany, was one of the most
abundant with numerous specimens discovered in the world-famous Solnhofen
Limestone of Bavaria, Germany and is among the best known pterosaurs. Their
wingspan ranged from 50 cm (20 inches) to well over 1 m (3.3 feet) and they
are immediately recognized by a distinctive cranial crest (Fig. 4.2). Pteranodon,
a Late Cretaceous form from North America had a wingspan exceeding 7 m.
Other crested genera are found in Late Cretaceous deposits of Brazil and include
Tupuxuara, Anhanguera, and Santanadactylus and Dsungaripterus and several
other crested forms from China. A group of Late Cretaceous pterodactyloids called
azhdarchids includes Montanazhdarcho and Quetzalcoatlus from North America,
Europe, and Africa. The wingspan of these reptiles ranged from 2 to 11 m, which
makes them the largest-known flying animals. For pterosaur systematics, lifestyle
and general biology, Peter Wellnhofer’s (1991) book, The Illustrated Encyclopedia
of Pterosaurs, finely illustrated by John Sibbick, gives an excellent coverage of
pterosaurs and their fossil record. We will concentrate in this chapter on some of
the issues connected with flight in pterosaurs and with the structure and dynamics
of the flight apparatus, the patagium.
4.1  The First True Fliers, Pterosaurs 133

Fig. 4.2  Pteranodon sternbergi. Male (front) and female. Modified from a Wiki Commons image

For a long time many workers considered that pterosaurs were incapable of
powered flight but rather were passive gliders. A number of morphological and
anatomical characteristics such as a large sternum for the attachment of power-
ful flight muscles together with powerful shoulders to brace the animal in flight
and enable an effective upstroke indicate that they were capable of flapping flight
and hence were the first vertebrates to actively fly. The mechanics of pterosaur
flight has attracted much attention over the years. Despite the fact that specimens
with preserved soft anatomy from other deposits have been known for quite a long
time (Zittel 1882; Sharov 1971; Padian and Rayner 1993), there is considerable
disagreement on their interpretation. A number of issues connected with ptero-
saur flight have been the object of extensive debate. These include the idea that
they were bipedal, their feeding behavior, the nature of the patagium (the skin that
forms the soft part of the wing), the extent to which it involves the hind limbs and
the presence and nature of its structural fibers (e.g., Wellnhofer 1987; Pennycuick
1988; Padian and Rayner 1993; Bennett 2000; Peters 2002; Tischlinger and Frey
2002). Perhaps the most impressive pterosaurs were the ‘giant’ members such as
Pteranodon and Quetzalcoatlus and it is their flight capabilities in particular that
have attracted the most attention over the years.

4.1.1 The Pterosaur Wing

The wings of pterosaurs are frequently compared with those of bats. They devel-
oped to include a surface formed by a membrane of skin broadly comparable
to that of bats (more will be said later) but most obviously with highly different
134 4  Flight by Membrane

attachments to the body. In bats all of the fingers except the thumb support the
membrane. In pterosaurs, the membrane was attached solely to the elongated fourth
finger–the remaining three fingers were slender and clawed, possibly for grasping.
The modern reconstructions with respect to shape of the patagium may be
another character that suggests active flight. Active flight in pterosaurs is not a new
idea, after all bats fly and Theodore von Soemmerring’s (von Sömmerring 1812)
reconstruction of a pterosaur in the early nineteenth century, showing the animal’s
posture and shape of the wings as distinctly bat-like must surely have helped the
idea. In his reconstruction, the wings are attached from the tip of the finger bone to
the feet and are of relatively low-aspect ratio although somewhat higher than that
of the non-powered gliders described in Chap. 3. On the other hand Padian (1985)
considered that pterosaurs could do better than that. He reconstructed the pterosaur
wing with a much higher aspect ratio, resembling much more the long, narrow
wings of some birds and in particular to the wings of birds that soar in moving air
associated with bodies of water, such as gulls, terns, frigate birds, and albatrosses
(Padian 1985; Padian and Rayner 1993; see Chap. 5) (Fig. 4.3).
Padian and Rayner’s (1993) description of the patagium, in particular its attach-
ment to the body rather than the hind limbs (feet, knee or even thigh depending on
the species) was novel. Interestingly, this new reconstruction of the pterosaur pata-
gium paved the way for two of Padian and Rayner’s (1993) other strong conten-
tions first, concerning how the patagium was reinforced and second, its attachment
to the body, which would free the hind limbs for bipedal locomotion. Padian and
Rayner were unquestionably the first modern-day workers to draw wider attention
to a crucial feature of the pterosaur wing that von Zittel had first noted in a finely
preserved specimen of Ramphorhynchus way back in 1882—structural fibers.
Padian and Rayner’s (1993) attention to the structure of the patagium is impor-
tant in many respects and it is unfortunate that it was not pursued in later stud-
ies. The following description is taken from their abstract. “The membrane-which
formed the aerodynamic surface of the wing-was invested with a series of closely
spaced, parallel structural fibers on its ventral surface. These fibers are 0.05 mm
thick, and 3–8 of them typically span 1 mm, depending on the extent of stretching
of the patagium. The length of individual fibers is difficult to trace: they were at
1east 5–10 mm in length but may have been very much longer. Some of the fibers
may have been discontinuous along the wing chord. Fraying of the structural fib-
ers near the trailing edge of the wing of one specimen indicates that they were real
structures, not wrinkles, that they were quite strongly attached to the ventral side
of the patagium, but may have been detached under substantial aerodynamic or
mechanical (possibly postmortem) forces. The fibers may have been homologous
to the keratinous scales and feathers of other archosaurs. The patagium, as a com-
posite structure, had mechanical advantages over other non-composite biological
materials and was flexible yet much stronger than any of its components alone.
The arched leading edge spar spread the patagium, which formed the aerodynamic
surface. The curved, cambered spar, and the structural fibers, which ran largely
parallel to the leading edge, maintained stiffness of the patagium to longitudinal
(spanwise) and chordwise bending.”
4.1  The First True Fliers, Pterosaurs 135

Fig. 4.3  Pterosaur wing structure and flight. a Because the fiber axes are in fact equidistantly
spaced, there must be some intercalation of new fibers chordwise (see Padian and Rayner 1993).
b Anterior view. c Lateral view. The cross section of the wing forms an effective airfoil. Lift dis-
tributed over the wing results in a span wise bending moment Ms, distorting the wing out of its
plane and a chord wise bending moment Mc relative to the leading edge tending to pronate the
wing. Combined with the straight orientation of the fibers, the arched shape of the leading edge
spar maintains the shape of the wing under these loads. d Hypothetical cross section of the wing
of a typical rhamphorhynchid pterosaur, showing location of patagium in relation to the groove
in the leading edge spar. Lift L is generated across the chord and is greatest behind the leading
edge. Deformation of the patagium when the wing is outstretched is prevented by the arched
leading edge spar and the structural fibers. Pronation of the patagium relative to the leading edge
spar is prevented by tension Tin the tissues beneath the spar. Lift would impose only a serial
transverse tension attempting to detach the membrane from the spar. Modified from Padian and
Rayner (1993)
136 4  Flight by Membrane

However, in the Zurich specimen Padian and Rayner state that the patagium near
the third phalanx is preserved in several layers showing detail of fiber impressions in
the crumpled patagium adjacent to the third-phalanx of the right wing. At this point
the wing is preserved in several layers thought to represent layers of the folded pata-
gium before diagenesis. It is here that one wonders if the crumpling is real (also in
the material referred to as the Marsh specimen; see Padian and Rayner (1993 Fig. 9;
here, Figs. 4.4 and 4.5) or that crumpling is simply inferred from the differently ori-
ented fibers, with the expectation that fibers had to be uni-directionally oriented. If
such an assumption was made, as seems possible, then a major feature of the pter-
osaur wing had been missed—a crossed-fiber architecture (Figs. 4.4 and 4.5). This
may be another reason why areas of degradation at the wing trailing edges show fib-
ers crossing over. A crossed-fiber system, as we know from Clark and Cowey (1958)
and studies in the vertebrate integument since (Lingham-Soliar 2005a, b), would not
only provide the rigidity and flexibility needed in a pterosaur wing, but also a ductile
surface that would enable greater resistance to stress compared to a brittle surface.
Over the years, Padian has steadfastly held the idea of a narrow high aspect
ratio wing and effective bipedal locomotion in pterosaurs. It may be a chicken and
egg scenario—which came first the narrow wing or bipedal locomotion. However,
this is consistent with the view that the pterosaur ancestor, possibly a glider such
as Sharovipteryx, was bipedal given that in the early evolution of the forelimbs
for flight they would have to have had a reduced role in terrestrial locomotion. In
support, Padian and Rayner pointed out a striking similarity between the pterosaur
and bird foot. On the other hand evidence is mounting, perhaps the most compel-
ling being that from pterodactyl trackways, pterosaurs walked on all four limbs
(Lockley et al. 1995; Unwin 1997; Mazin et al. 2003).
The trackway data of a quadrupedal gait as well as new soft tissue specimens
that show the extent of the wing membranes that include a narrow portion in front
of the forelimb (propatagium) that continued distal to the wrist, and the main
wing membrane that was connected to the fore and hind limbs (brachiopatagium)
including the uropatagium (between the hind limbs) is more-or-less accepted by
most workers today (see Elgin et al. 2011). With such new evidence there is a
more or less general consensus that the unusually high-aspect-ratio or narrow wing
as reconstructed by Padian and Rayner (1993) is unrealistic and that the patagium
is at the very least attached to the mid-thigh region, with an extension, the uropata-
gium, occurring between the posterior limbs (Wellenhofer 1991).
One would have hoped that with scanning electron microscopy of the fiber
structure of the pterosaur wing membrane (Unwin and Bakhurina 1994) that many
of the unanswered questions would have been resolved. In many ways it seems
rather to have muddied the waters even more. On the positive side the SEM study
on the pterosaur, Sordes pilosus, found that each of the larger structural fibers
was comprised of finer fibrils. This should not come as a surprise because the-
fiber-fibril organization of structural fibers such as collagen and keratin is well
documented in the literature (e.g., Motta 1977; Filshie and Rogers 1962; and
Wainwright et al. 1976; see Chap. 5 for references) . More questionable are con-
clusions based on these authors SEM, which shows that in the outer half of the
4.1  The First True Fliers, Pterosaurs 137

Fig. 4.4  Details of the Zittel wing (BSP 1880 l I 8). a The region adjacent to the ulna and the
wrist in the Zittel wing. b The areas indicated by arrows show different fiber orientations in a
very small area not affected by folding of the patagium, confirmed by the straightness of the fib-
ers. Creases have largely unaffected the underlying fiber orientations

wing the fibers were straight and closely packed while they were bent and loosely
packed close to the body. This fibrous architecture was construed to provide
increased elasticity close to the body and greater rigidity further away. The authors
therefore proposed a non-homogenous fiber structure of non-elastic and elastic
138 4  Flight by Membrane

Fig. 4.5  Detail of the left wing of the Marsh specimen of R. muensteri (YPM 1778; Marsh
1882; Fig. 30), showing folds (F), structural fibers (f), wrinkles (W) and deformations of the
patagium surface (dotted lines). After Padian and Rayner (1993)

fibers (of unknown chemistry), contrary to Padian and Rayner (1993), which pro-
vided rigidity for much of the wing membrane and flexibility closer to the body.
This, as well as information from a new pterosaur, Jeholopterus, from the Jehol
Group of the Yixian and Jiufotang Formations in China, will be considered below
in the section on the pterosaur wing mechanics.
Many pterosaur reconstructions show the body covered in hair (e.g., see
Wellnhofer 1991). Although it was thought to have been based on an unfortunate
interpretation of Sharov’s (1971) description of hair-like structures in the pterosaur
Sordes pilosus, the idea of “Dino-fuzz” is now being proposed for a wide array
of taxa, some as yet unpublished, but particularly in Chinese pterosaurs (Ji and
Yuan 2002). In the latter paper the authors describe two pterosaur species from the
Mesozoic Daohugou Biota in the Ningcheng region of China, which they refer to
as “protofeathered.” These apparently hair-like filaments are known as pycno fibers
and are not considered homologous (sharing a common origin) with, mammalian
hair. Czerkas and Ji (2002) have speculated that pycno fibers were an antecedent of
proto-feathers, while other authors suggest pterosaur pycnofibers were structured
differently from ‘protofeathers and that they were flexible, short filaments, “only
5–7 mm in some specimens,” and rather simple, “apparently lacking any internal
detail aside from a central canal” (Witton 2013). Given the dismal accounts in the
literature of so-called protofeathers in non-avian dinosaurs, e.g., Sinosauropteryx
(see Chap. 6), the subject of pycnofibers and their alleged functions such as
thermo-regulation and warm-bloodedness will not be discussed any further here.
The principles of flight were discussed in Chap. 1 and will also be exam-
ined from the perspective of birds in Chap. 5. Here, because of a vastly different
4.1  The First True Fliers, Pterosaurs 139

skeletal support system and distinctive flight surface (wholly membranous) we

will briefly consider both conditions in pterosaurs. The reconstruction of the ptero-
saur wing membrane has come almost full circle as far as its points of attachments
are concerned. Reliable evidence shows that in some species it extended from the
fourth digit down to the toes roughly as shown by Soemmerring’s original recon-
struction but the consensus of opinion as we have seen above is that the wing was
connected to the hind limbs. Although some of the bones, particularly the fore-
limbs, were of considerable size, pterosaur bones like those of birds were hollow
and thin-walled, which kept the weight low. The puzzle of pterosaur flight has
not abated with a number of studies in recent years continuing to present interest-
ing answers to a number of questions on their flight potential. For example Matt
Wilkinson and colleagues have demonstrated that a forward-pointing pteroid (an
elongate wrist bone unique to pterosaurs) generated a high lift coefficient and that
attachment of the hind limb to the main wing membrane permitted control over
camber and wing shape, improving aerodynamic efficiency (Fig. 4.6). Thus, even
with the lower aspect ratio wing compared to that in the reconstructions by Padian
and Rayner, the lift/drag ratio is considered generally quite high. However, the
flight membrane itself and its attachment to a single digit continue to be of aerody-
namic interest and will be considered next.
Ulla M. Lindhe Norberg (1990) looked at critical mechanical principles of the
membrane-skeletal arrangement in the wings of bats and pterosaurs. In the bat wing,
which will be discussed further below, the principle forces are dissected by two ele-
ments, digits 4 and 5 and supported by them and by digit 3 and the body. In contrast
the pterosaur membrane is undivided and supported by just one skeletal element,
digit 4, and the body. Assuming a more-or-less equal trisection of the bat wing by
the elements, then the force per unit length of one of the trisected wings becomes
a third that of an undivided membrane as in pterosaurs—because force F is pro-
portional to the area of the supported membrane. Norberg (1990) drew attention to
Colin Pennycuick’s suggestion that the fourth and fifth digits of the bat wing act as
compression struts so that the distal part of the bat wing’s leading edge is relieved
of large tensional forces. This contrasts with the pterosaur wing where the leading
edge is supported by just one digit that would have to resist tensional forces trans-
formed from the aerodynamic pressure on the entire wing membrane. The resulting
tension would be much larger on the outer part of the fourth digit and much stronger
and thicker and controlled by much stronger muscles. In these respects the pterosaur
leading edge she considered superior to that of bats (Fig. 4.7).

Fig. 4.6  The pteroid bone in

pterosaurs. After Wilkinson
et al. (2006)
140 4  Flight by Membrane

Fig. 4.7  Bat (a, b) and pterosaur (c, d) wings. a The digits act to alter the direction of tension
forces (Pennycuick 1971) so that the distal part of the wing is relieved of large tension forces.
b Force diagram (on a cross section of a schematic wing extended by the body and three digits,
forming equal interjacent surfaces) showing that the distal skeletal element of the wing (the white
dot to the right; horizontal and acute arrows = angle θ) is exposed to tension forces transformed
from forces from one section only. The tension (lateral forces) on each side of the two middle
digits cancels out. c Arrows indicate presumable direction of the tension forces. By a proper
structure of the membrane, for instance occurrence of elastic strands along the paths indicated
by dotted lines, the tension forces might have deflected, relieving the distal part of the leading
edge from large forces. d Force diagram (on a cross section of a schematic wing extended by the
body and fourth digit) showing that the fourth digit had to resist the tension forces transformed
from forces from the entire wing membrane (posterior to the arm). The only supporting digit
had to resist a large part of the tension. In case (d) the lateral force on the leading edge digit (to
the right) is exposed to three times as large a force as that in ease (b). The middle digits in (b)
(fourth and fifth) are not subjected to any lateral forces, since they cancel out at these digits. The
distal digit in case b takes up only one sixth of the vertical force VF (vertical component of ten-
sion force F′), while the middle two digits take up one-third each of the vertical force. The hori-
zontal projection of the membrane areas, angle θ, and pressure per unit area in (b) and (d) are set
equal. Modified after Norberg (1990)
4.1  The First True Fliers, Pterosaurs 141

Norberg’s (1990) analysis has touched on important aspects of pterosaur wing

structure. Following shortly after was the study mentioned above, by Unwin and
Bakhurina (1994). In striking contrast these authors proposed that the pterosaur
patagium was non-homogeneous, comprised of two entirely different fiber types,
stiff, relatively inelastic fibers (outer half) and sinuous and relatively elastic fibers
(inner half, closer to the body). However, the authors failed to consider the taphon-
omy of the specimen. First that decay of the patagium is likely to have been more
severe closest to the body than distally (see Chap. 6). Second, the chemical and
biomechanical properties of structural fibers such as collagen change with decay.
In a study on integumental structures in certain fossil animals (Lingham-Soliar
2003) the proposals by Unwin and Bakhurina (1994) of non-homogenous fiber
types in Sordes pilosus was queried versus different states of collagen fibers under
different conditions (Gordon 1978)—i.e., that they show different forms, e.g.,
when taut or under tension—they may be straight under tension but bent when
relaxed (unstrained). Hence, the non-homogenous concept is probably unfounded.
Conclusions based on the data presented by Unwin and Bakhurina (1994) are
speculative and hence their proposal of a structural design strategy of the wing
not just for Sordes pilosus but, as they state, presumably other pterosaurs, must be
treated with caution.
A brief mention needs to be made on fibers in the pterosaur membrane that
were named actinofibrils by Wellnhofer (1987), a term that appears to have been
adopted by other authors, e.g., Christopher Bennett (2000). Yet, this definition
appears to be both unnecessary and misleading (actin is a protein that is largely
connected with contractile properties as, e.g., in muscles) and based rather ambig-
uously on their function, i.e., of being “little ray” rather than “actuating” fibers’.
In all probability they are collagen (even possibly keratin) structural fibers which
range in size from bundles about 20 μm to bundles about 1.0 mm thick (Lingham-
Soliar 2005a, b, c). As we saw in Volume 1, collagen is the dominant structural
protein in vertebrates and capable of numerous functions particularly involving
their high tensile properties (see Chap. 6).
The mechanics involved in the pterosaur patagium, principally with respect
to flexibility and stiffness, has been almost without exception linked with the
notion of two distinctly different types of fibers, stiff and elastic. These studies
have failed to take note of important studies on the integument in vertebrates (par-
ticularly connected with aquatic locomotion) outside of pterosaurs from approxi-
mately the last quarter of the twentieth century to the present time. While there
is no doubt that elastin fibers may form a part of dermal fiber systems in animals,
however, in instances where the dermis is involved in major biomechanical func-
tions, it is the geometric assembly of homogenous fibers (effectively producing
non-homogenous systems) rather than association with other fiber types that pro-
vide some of the critical properties of the integument (see Chap. 2).
The Zittel, Zurich and Marsh specimens, all of Ramphorhynchus, in my view
show compelling signs of cross-fibers (see Figs. in Padian and Rayner (1993)
and here, Figs. 4.4 and 4.5) and warrant further investigations. As in the ichthyo-
saur integument, the crossed-fiber architecture was not at all obvious but required
142 4  Flight by Membrane

investigations particularly in places of wear in which another fiber layer of oppo-

sitely oriented fibers might be exposed (Lingham-Soliar 1999, 2001; Lingham-
Soliar and Plodowski 2007). Frequently, poor tissue preservations, rather than
good, provide answers in such studies.
Just the impetus for further study has come from the Chinese pterosaur
Jeholopterus mentioned above. Kellner et al. (2009) describe differently oriented
fibers in at least three different layers of the wing membrane. Fortunately, these
are rather obvious and ubiquitous in the specimen. Consistent with the forego-
ing discussion, Jeholopterus may be the thin end of a much greater wedge and
closer examination of other species may almost certainly show that this crossed-
fiber architecture of the pterosaur patagium, rather than being atypical, was a com-
mon feature in the group. Also, their Fig. 4.4 shows that when the membrane is
twisted it is reflected by sinuous fibers and not the otherwise straight fibers, which
are also apparent in the Zittel specimen (Fig. 4.4b, arrows). As mentioned, from a
biomechanical perspective fibers oriented in a single direction would be vulnerable
to brittle tearing stresses (Bodde et al. 2011; Lingham-Soliar 2014). The conse-
quence of such stresses on a pterosaur membrane, given the high stresses involved
during pterosaur flight, would be catastrophic. In nature, in numerous cases where
brittle tearing stresses on the integument need to be avoided, the solution to mini-
mizing the dangers would almost certainly involve a cross-fiber architecture, pro-
viding a ductile tearing surface (Lingham-Soliar and Murugan 2013).
Bennet (2000) summed up the various theories on the functions of the pterosaur
wing fiber as:
(1) to prevent unwanted flapping of the patagium; (2) to camber the patagium,
transferring aerodynamic loads anteriorly and proximally to the metacarpus and
antebrachium; and (3) to spread the patagium chordwise. He favoured only the last
interpretation as consistent with the available data, i.e., that the fibers resisted lon-
gitudinal compression so as to spread the patagium chordwise, to redirect span-
wise tension in the proximal patagium as chordwise tension in the distal patagium,
and to permit compact folding.

4.1.2 Huge Body Size and Flight in Pterosaurs

The ‘giant’ pterosaurs Pteranodon and Quetzalcoatlus have frequently been the
subject of flight capabilities, some including the construction of realistic test models
(Fig. 4.2). In 1985, the Smithsonian Institution commissioned aeronautical engineer
Paul MacCready to build a half-scale working model of Quetzalcoatlus northropi.
The replica was launched with a ground-based winch. It flew several times in 1986
and was filmed as part of the Smithsonian’s IMAX film On the Wing. However,
the model was not anatomically correct and embodied vertical and horizontal
tail stabilizers that pterosaurs did not have. It also had a longer tail, changing the
weight distribution. We will not consider such experiments further here. One nota-
ble method that has been used in trying to understand function in fossil animals is
4.1  The First True Fliers, Pterosaurs 143

in the use of modern-day analogues. They have been used with varying degrees of
success in attempts to understand the flight capabilities of pterosaurs, particularly
with Recent birds as analogues.
Witton and Habib (2010 and references therein) on the other hand, in a reap-
praisal of giant pterosaur fossils suggest that bird and pterosaur wing structure,
gross anatomy and launch kinematics are too different to be considered mechani-
cally interchangeable. Observations on avian flight they say have also heavily
influenced research into pterosaur flight mechanics resulting in commonly held
assumptions that pterosaurs and birds would take off in a similar way. They pro-
pose a new theory on the ever-problematic question of how pterosaurs launched
themselves but first we will look at some of their criticisms.
Unwin and Bakhurina (1994) presented evidence from pterosaurs such as
Sordes pilosus that suggested a poor terrestrial ability and a ‘gravity assisted’
rather than ‘ground up’ origin of flight for pterosaurs. Other workers such as
Chatterjee and Templin (2004) concluded that giant pterosaurs required specific
environmental conditions to launch and must be atypically lightweight to reduce
the power required for flight and, ideally, employed downhill runs and headwinds
when launching. Perhaps most restricting is that Chatterjee and Templin’s study
permits flight only if they were extremely lightweight (16 kg for a 7 m span form;
70 kg for 10 m). They propose that a pterosaur massing more than 70 kg could not
launch, which essentially renders any pterosaur above this size flightless. A similar
conclusion was reached by Sato et al. (2009), who considered that birds—specifi-
cally ocean-going procellariiforms—and pterosaurs were so mechanically analo-
gous that the flight mechanics of the former could provide insights into the flight
of the latter. Regressing the masses of 7 and 10 m span pterosaurs from a procel-
lariiform mass dataset (see Chap. 5 on soaring birds), they predicted ‘heavy’ ptero-
saur masses and, by extrapolating flapping frequency against mass in albatross and
petrels, suggested that a 5.1 m span and 41 kg mass was the pterosaur flight limit.
They cast particular doubt on the flight abilities of Pteranodon and Quetzalcoatlus
northropi, the largest representatives of two pterosaur clades that achieved gigantic
size. According to Sato et al. (2009), even if these forms had narrow, albatross-like
wings, they would be incapable of flight in modern environments.
Witton and Habib (2010) counter some of these arguments with a number of
points. They estimate soaring and short-term flapping potential in giant pterosaurs
using the same general approach suggested by Pennycuick (2008) for the estima-
tion of flapping frequency and glide performance of birds (see Chap. 5) and utilized
the latest version of Colin Pennycuick’s flight program software (see Chap. 5), albeit
with program parameters altered from their defaults to account for pterosaur biology,
to make their flight calculations (it includes a wide range of data from measured,
living birds, both wild and captive specimens). They concluded that the propor-
tions, scaling and morphology of giant pterosaur fossils suggests that bird and pter-
osaur wing structure, gross anatomy and launch kinematics are too different to be
­considered mechanically interchangeable (Figs. 4.8 and 4.9).
Interesting, was Witton and Habib’s consideration of the potential of mem-
brane wings being able to provide higher maximum lift coefficients than avian
144 4  Flight by Membrane

Fig. 4.8  Albatross, azhdarchid and pteranodontian skeletons compared, a wandering albatross,

Diomedea exulans; b the azhdarchid Hatzegopteryx; c the pteranodontian Pteranodon; d func-
tional wing region dimensions compared across a standard wing length. After (Witton and Habib
2010; also see author credits for the individual figures) Images not to scale. PLos ONE Open
Access. doi:10.1371/journal.pone.0013982.g004

Fig. 4.9  Soaring animal planforms compared. a Wandering albatross Diomedea exulans. b The

giant ornithocheiroid Pteranodon. c The giant azhdarchid Quetzalcoatlus. d Shown to scale. After
(Witton and Habib 2010). PLos ONE Open Access. doi:10.1371/journal.pone.0013982.g007
4.1  The First True Fliers, Pterosaurs 145

wings, which they base, e.g., on findings by Song et al. (2008) that suggest that
compliant, membrane wings achieve greater maximum lift coefficients than rigid
wings. Given that the membranous wings of bats are expected to have a steeper
lift slope than the stiffer, less compliant wings of birds, Witton and Habib assume
that the same generalities apply to pterosaur wings. However, taking into account
the somewhat different wing structure and specifically membrane histology, their
maximum lift coefficient estimate for most pterosaur wings in excess of that meas-
ured for birds, by about 33 %, requires caution.
From their review and analysis of pterosaur flight capabilities, Witton and
Habib’s (2010) own hypothesis on how ‘giant’ pterosaurs launched themselves
into the air presents a number of imponderables and in other cases questionable
descriptions. In contrast to other ‘ground up’ hypotheses, involving bipedal loco-
motion, their theory favors a quadrupedal gait in pterosaurs. They propose that
pterosaurs launched themselves from a standing, quadrupedal start in a superfi-
cially vampire bat-like fashion, vaulting over their forelimbs and using powerful
flapping to gain altitude (Fig. 4.10). An extensive critique was posted by David
Peters (Plos One website for Readers Comments on Witton and Habib (2010))
counterpointing a number of general anatomical (and occasionally taxonomic)
descriptions by Witton and Habib, and specifically with respect to their “launch-
ing” theory, a lack of ichnite (pterosaur trackway) evidence (see Peters critique
and cited references therein). However, because of the novelty of the hypothesis
by Witton and Habib on how ‘giant’ pterosaurs launched themselves, Peters’ cri-
tique, particularly with respect to biomechanical implications, is interesting and
presented below in his own words.
Peters (2010) states, “comparisons to vampire bats (Desmodus rotundus) leave
certain doubts. In vampires (≤30 g) the pectoralis creates 85 % of the launch
power [10]. The hind limbs produce just enough thrust to keep the forelimb thrust
vector between the thumbs. The feet leave the substrate before the thumbs do. At
apogee the bat’s back is three times higher than at loading and the forelimbs trail
beneath the body. Afterwards the limbs rise and flex, creating a parachute to slow

Fig.  4.10  Skeletal reconstruction of a quadrupedally launching Pteranodon. Witton and

Habib (2010, and figure acknowledgements therein). PLos ONE Open Access. doi:10.1371/
journal.pone.0013982.g006
146 4  Flight by Membrane

the descent. The wing fingers do not deploy until the wings continue their rise
(and the body falls) for the first downstroke 0.10 of a second after becoming air-
borne and 0.20 of a second after initiating the launch sequence. In Desmodus the
humerus is longer than the femur, tibia, pelvis or skull and 22 % of the forelimb
length, which also includes an antebrachium and slender elongated digits.
By contrast an azhdarchid, such as Zheijangopterus [12], does not have a
similar morphology to Desmodus (but certain anurognathid pterosaurs do). In
Zheijangopterus, the humerus is a third the tibia, less than half the femur, shorter
than the pelvis, about 13 % of the skull length and less than 10 % of the forelimb
length. This pterosaur is a magnitude larger than Desmodus, but comparatively
underpowered. Zhejiangopterus would have found it difficult, if not impossible, to
launch to twice or thrice its standing height. Snapping open its large wings at the
apogee of its brief leap would also be daunting.
As an alternative, the relatively long hind limbs and large pelvis could have pro-
vided relatively more leverage and power for running or leaping and launch. They
were much more heavily muscled. Virtually all other tetrapod saltators, including the
pterosaur precursors Sharovipteryx, also used heavily muscled hind limbs anchored on
elongated hips for leaping. This coupled with extended wings providing lift and thrust
from the start, would appear to be the mode of launch in pterosaurs, as in birds.”
From a biomechanical perspective some further points are worth noting con-
cerning take-off in pterosaurs. Michael Habib is on record (interview with Erin
McCarthy on http://MentalFloss.com) comparing ‘giant’ pterosaur take-off with
pigeons. He states “… launch is effectively ballistic. So the launch is not initiated
with the wings. You don’t flap yourself into the air, you jump yourself into the
air. And then you engage your wings. Now, we don’t see that. It’s so fast. What it
looks like to us is that a pigeon is pulling himself into the air with his wings, but
he’s actually pushing his feet and then pulling himself higher with his wings.”
Of course the idea of a ballistic launch in flight take-off is not novel in both glid-
ers and powered flyers such as a pigeon and that it precedes the wings being brought
into action. However, what is importance is the relative force involved in the bal-
listic launch compared to that achieved by the more-or-less synchronous initial flap-
ping of the wings. Chapter 5 describes the strenuous motions of pigeon flight just
after take-off. Pennycuick’s studies over the years have shown how the profile of
parasite and induced drag increases with lower speeds in flying animals as repre-
sented by the U-shaped curve. Also the maximum power available as shown for the
pigeon (see references and figures in Chaps. 1 and 2) is amply sufficient for flight
at zero speed (hovering), which enables the pigeon to take-off from rest by jump-
ing straight into the air. It is also able to use each flight feather as a separate aero-
foil (Fig. 4.11). It is also clear that larger—and heavier—flyers invariably need a
take-off run to build up the necessary speed. Given that Witton and Habib describe
launching in ‘giant’ pterosaurs, rather oddly, they selectively choose pigeon jumping
as an analogue but ignore the run-off needed by heavier birds (perhaps the largest
bird that can take off from a jump without a run is the mallard duck).
If a pigeon is to be used as an analogue, then Witton and Habib must establish
the proportion of force achieved by its leap compared to its flapping of the wings
4.1  The First True Fliers, Pterosaurs 147

Fig. 4.11  Pigeon taking off

vertically from a body of
water with less force from
the jump than a solid surface
would provide. Photo with
permission of Clint Ralph

that helps prevent it from crashing back onto the ground (see Norberg and Norberg
below on maximum attainable size in bats). Hence, any extrapolation to a ‘giant’
pterosaur leaping into the air requires dynamic and functional similarity models.
Furthermore, we will see in Chap. 5 that short run-offs and steep take-offs, let
alone launching directly into the air, require shorter, low aspect ratio wings, as in
vultures, unlike the high aspect ratio wings of pterosaurs and seabirds (Fig. 3.8).
In marine animals too, high aspect ratio ‘wings’ are poor for ‘dead starts’
(Lingham-Soliar 2005b, c). From the scaling laws applied to bird flight, large fly-
ing animals such as swans and vultures require long runways to become airborne.
Considerable progress has been made over the years on the biology of ptero-
saurs generally and they continue to draw attention whether on the shape of the
wings, behavior, and lifestyle, mode of terrestrial locomotion or flight dynamics.
As so often the investigations have been fuelled by frequently differing views.

4.1.3 Pterosaur Feeding Behavior

We will very briefly mention pterosaur feeding behavior because it is frequently

connected with their flying capabilities and habitat. Since most remains have been
148 4  Flight by Membrane

found in marine deposits, it is assumed that they lived along ocean shores, probably
roosting on cliffs from which takeoff would have been easy. Several pterosaur taxa
are postulated to have been skim-feeders based largely on supposed convergences
of their jaw anatomy with that of the modern skimming bird, Rynchops spp.
Humphries and colleagues (2007) note that despite considerable interest
in the biomechanics of flight among pterosaurs, the feeding methods of these
animals are still poorly understood. This situation is in stark contrast to other
Mesozoic reptiles in which the feeding apparatuses have been subject to numer-
ous investigations in functional morphology and biomechanics. They make an
interesting statement namely that just because a component of an extinct ani-
mal resembles that of a living one does not necessarily imply that both were
used for the same task (Fig. 4.12). Humphries et al. (2007) focus on the postu-
lated convergence in mandible morphology with pterosaur species and the extant
“skimmers” (Aves: Rynchopidae), in which all three Rynchops species forage
almost exclusively by skim-feeding. Indeed, in their investigations they found
using physical and mathematical models of Rynchops bills and pterosaur jaws,
that skimming is considerably more energetically costly than previously thought
for Rynchops and that pterosaurs weighing more than one kilogram would not
have been able to skim at all. Furthermore, anatomical comparisons between the
highly specialized skull of Rynchops and those of postulated skimming ptero-
saurs suggest that even smaller forms were poorly adapted for skim feeding.
Their results they advocated refuted the hypothesis that some pterosaurs com-
monly used skimming as a foraging method and they underscore their findings
as cautionary with respect to paleontological extrapolations from limited mor-
phological evidence.

Fig. 4.12  Rynchops nigra. Commonly called the skimmer, it is distinguished by a unique

bladelike bill, the lower mandible of which is one-third longer than the upper. Photo with
permission of Clint Ralph
4.2  Bats, the Only Mammalian True Fliers 149

4.2 Bats, the Only Mammalian True Fliers

Bats belong to the order Chiroptera and are the only mammals to have evolved
true or powered flight. This ability, coupled with the benefits deriving from their
system of acoustic orientation (so-called bat sonar), and predominantly nocturnal
predation (including vampirism) has made the group highly successful in numbers
of species and individuals. About 900 species are currently recognized, belonging
to some 174 genera.
Flying birds span four orders of magnitude in size, from about 1.5 g to around
16 kg (Pennycuick 2008), whereas bats span only three, from 1.9 g to 1.6 kg. The
extinct giant vulture Argentavis had a wingspan of 6.5–7.5 m and weighed about
70 kg (Chatterjee and Templin 2004). Pterosaurs ranged from about 4 g to pos-
sibly as much as 100 kg (Wellnhofer 1991). The largest extant flying birds thus
weigh about 10 times more than the largest bats and the largest pterosaurs were
almost 70 times heavier. By contrast, the lower size limit is strikingly similar for
all three groups of flying vertebrates (Norberg and Norberg 2012).
Flight is the primary mode of locomotion in all bats, although the flight styles
vary. Some groups (the Molossidae, for example), adapted for flight in open
spaces and often at high altitudes, have long, narrow wings, swift flight, and a
large radius of turning. Other bats (the Nycteridae, Megadermatidae, and the
Glossophaginae), adapted for hovering as they pick prey off vegetation or feed on
flowers, have short, broad wings, slow flight, and a small radius of turning. Some
bats take flight easily from the ground: members of the genus Macrotus do so sim-
ply by flapping, vampires (Desmodus) leap into the air and then spread their wings
and fly. The molossids, however, roost well above the ground since, on take-off,
they fall before becoming airborne.
Ulla M. Lindhe Norberg and R. Åke Norberg (2012) reported new wingbeat fre-
quency data for 65 (27, their own data) morphologically diverse bat species repre-
senting nine families spanning a range from 2.0 to 870 g. For these species, wingbeat
frequency decreases with increasing body mass as M−0.26b . They filmed 25 of their 27
species in free flight outdoors, and for these the wingbeat frequency varies as M−0.30
b .
These exponents are strikingly similar to the body mass dependency M−0.27 b among
birds, but the wingbeat frequency is higher in birds than in bats for any given body
mass. The downstroke muscle mass is also a larger proportion of the body mass in
birds. Interestingly, from their observed scaling of wingbeat frequency and the pro-
portion of the body mass that is made up by flight muscles in birds and bats, Norberg
and Norberg estimated the maximum potential body mass for bats to be 1.1–2.3 kg,
which compared with the largest bats, extinct or extant, weight of 1.6 kg.
Though flight speeds in nature are hard to measure, four vespertilionid species,
carefully observed, have been timed on the average at 18.7–33.3 km (11.7–20.8
miles) per hour. In flight, the posture of each of the four fingers incorporated into
the wing is under precise and individual control. Finger and arm postures, which
determine the shape, extension, and angle of the wings, govern such actions as
turning, diving, landing, and hovering (Novick 2005).
150 4  Flight by Membrane

4.2.1 Wing Structure and Mechanics

As with the pterosaurs, in bats the front limbs are modified for flight. However,
unlike in pterosaurs where only the forefinger supports the membrane, in bats the
membrane is supported by the four greatly elongated fingers, excluding the thumb,
and bones of the forearm. The membrane extends from the posterior border of the
forearm and upper arm to the side of the body and leg as far as the ankle or foot.
Only the thumb, and occasionally the index finger, ends with a claw. When not
fully extended, the wing skin is gathered into wrinkled folds by elastic connective
tissue and muscle fibers (Fig. 4.13).
Wing shape, governed by the relative lengths of the forearm and the fingers,
varies greatly, in adaptation to flight characteristics. Most bats have a membrane,
consisting of skin like the wings, that extends between their legs (interfemoral
membrane). In the midline, the interfemoral membrane is usually supported, at
least in part, by the tail, and the distal edges are often shaped in flight by greatly
elongated heel bones. The membranous wings of bats are adjusted by muscle bun-
dles and elastic fibers and together with the support from the slender elements of
the digits, are very flexible. Bats with different types of flight have different shapes
of the wings. In general, long and narrow wings are associated with rapid and
enduring flight, while short and broad wings are associated with high maneuver-
ability in narrow spaces (Norberg 1972). The interfemoral membrane is especially
well developed in insectivorous, carnivorous, and fish-eating bats, is less well
developed or even absent in the vampires and in fruit- and flower-feeding bats.
The wings of birds and bats are moveable in different ways that permit the animal
to change the geometry and aerodynamic characteristics of the wing to control the
motion, or to improve the performance in some desired manner. Bats have the pos-
sibility to vary the camber (anteroposterior curvature) of the wing, in which ability
they highly surpass the birds (Figs. 4.13 and 4.14) (we saw in Chap. 1 how camber
affects lift). The following summary taken from Norberg (1972) gives a good idea of
how bat wing structures control rigidity and influence the wing aerodynamics:
“From comparisons between bat wing structures and aerofoils and high-lift
devices with known aerodynamic data, from the aeronautical literature, deductions
are made regarding the function of some bat wing structures. Special arrangements
in the hand wing add to rigidity and reduce the demands for powerful muscles and
thick digits, thereby reducing the mass of the wing.
1. The anterior part of the wing, formed by the membrane parts anterior to the
arm and third digit, is proportionally broad in megachiropteran bats as well as
in many broad-winged microchiropteran bats. These parts can be lowered by
the thumb and by pronation of the manus, and may together function as a lead-
ing edge flap. Leading edge flaps of aeroplanes permit, when lowered, higher
angles of attack without separation, and thus higher lift coefficients. The lead-
ing edge in bats is very sharp, which increases the effectiveness of the leading
edge flap (Figs. 4.13 and 4.14).
2. The Reynolds number of bat wings lies in an interesting range, where the lift
coefficient can be improved by induced turbulence of the boundary layer. The
4.2  Bats, the Only Mammalian True Fliers 151

Fig. 4.13  Rousettus aegyptiacus. The large wrinkles in the membrane parts between the second
and third digits and third and fourth digits indicate the location and direction of the largest ten-
sion forces between these digits. Modified to highlight wrinkles. After Norberg (1972)

Fig. 4.14  Common fruit
bat, Rousettus aegyptiacus
in flight showing the digits
(numbered) and the leading
edge flap. Modified after
Wiki Commons image

arm and digits, projecting markedly over the dorsal surface of the wing, and
hair may function as turbulence generators.
3. The tension forces of the membrane on the digits have different effects upon
the different digits, depending on the tautness of the surrounding membrane
parts. The second digit and distal phalanx of the third digit are exposed mostly
to bending in the membrane plane. The phalanges of the fourth and fifth digits
are exposed to large dorsoventral bending.
152 4  Flight by Membrane

4. Two arrangements add to relieving the distal part of the wing of large tension
forces, thereby reducing the demand for a powerful extensor muscle of the dis-
tal phalanx (-ges) of the third digit: 1. The fourth and fifth digits act to alter
the direction of tension. 2. By splitting the wing membrane in several parts by
the digits, the second and third phalanges (the second in fruit-bats) of the third
digit, which constitute the distal part of the wing’s leading edge, are exposed
to tension forces transformed from forces only from the nearest patagium. If
the wing membrane would be outstretched only by one digit, as was the case in
pterosaurs, the leading edge digit would have to resist the tension forces trans-
formed from forces from the entire membrane posterior to the arm.
5. The fourth digit is angled in such a way that the proximal part of the membrane
between the third and fourth digits is kept very taut, and the fourth metacar-
pophalangeal and interphalangeal joints are held very steady without any need
of large muscular forces” (Figs. 4.15 and 4.16).

Fig. 4.15  Diagrammatic
representation of the
distribution of the largest
tension forces between
the second and fifth digits
in the wing of Rousettus
aegyptiacus. Redrawn after
Norberg (1972)

Fig. 4.16  Diagrammatic
representation of forces
acting on digits three and
four. Since the fourth
metacarpophalangeal joint
is angled posteriorly and the
fourth interphalangeal joint
anteriorly, the proximal part
of the membrane between
the third and fourth digits
is kept very taut, and the
metacarpophalangeal and
interphalangeal joints are
very steady without any need
of large muscular forces.
Redrawn after Norberg
(1972)
4.2  Bats, the Only Mammalian True Fliers 153

We saw in Chap. 1 that by increasing the angle of attack the lift coefficient is
increased to a certain value at the cost of a higher drag coefficient. When a criti-
cal angle of attack is reached the wing may stall. Stalling can be delayed by larger
angles of attack and hence the lift coefficient increased, in several ways. In birds
the most important way is by the wing slot. The alula and the free ends of the
hand remiges prevent flow separation at the upper surface of the wing parts behind
these structures. Bats lack similar slots but can delay stalling by leading edge flaps
(Fig.  4.14), which have been developed for airplane wings as high-lift devices
(Chap. 1). These flaps, since they reduce the severity of the pressure peak ordinar-
ily associated with high angles of attack, permit higher angles of attack and higher
lift coefficients without separation (Chap. 1, Figs. 1.31 and 1.32), especially for
thin section wings with a sharp leading edge. The effectiveness of leading edge
flaps increases with a decreasing leading edge radius. Norberg (1972, 1990) pro-
posed that in bats the propatagium and dactylopatagii brevis and minus together
may function as a leading edge flap when lowered by the thumb and the second
digit (Figs. 4.15 and 4.16). These membrane areas are especially large (broad) in
pteropodid bats, for instance in Rousettus aegyptiacus (fam. Pterodidae), as well
as in many other species with broad wings (Fig. 4.13).
Norberg (1972, 1990) also proposed another unusual way in which bats may
delay stalling. Very near the wing surface the air is retarded due to friction and
this very thin layer, the boundary layer, can either be laminar, turbulent, or lam-
inar anteriorly and turbulent posteriorly on the wing. One way to delay stalling
is to make this boundary layer turbulent. Every pressure increase in the direction
of flow is unfavorable for keeping the boundary layer laminar, especially at high
Reynolds numbers [Re = (V ⋅ c/ν)], where V is the resultant air speed, c is the
wing chord, and ν is the kinematic viscosity of the air. Approximately at the loca-
tion of the pressure peak (Fig. 4.17a) (at about the highest point above the wing
chord) transition from laminar to turbulent boundary layer flow occurs at the upper
surface of the wing, or, if the pressure peak is sufficiently large, the laminar flow
may leave the surface permanently (Fig. 4.17b), separating. In a very interesting
aerodynamic range (when the Re No is less than ca. 105; Schmitz 1960, reference
in Norberg 1972) there is a critical value of the Re No, Recrit., below which (sub-
critical Re No) the laminar boundary layer is very stable, and above which (super-
critical Re No) there is a transition from laminar to turbulent flow at the pressure
peak. When the Re No lies below the critical value, which is different for different
profiles, the aerodynamic lift coefficient can be improved by induced turbulence of
the boundary layer (Fig. 4.17c) (Norberg 1972, 1990; also see Muijres et al. 2008).

4.2.1.1 New Developments in Bat Aerodynamics

John Gordon (1978) had an almost uncanny knack of putting his finger on biome-
chanical problems long before answers were forthcoming. He suggested the way in
which bat wings are constructed by stretching the membrane of very flexible skin
over a framework of long thin bones bore a striking resemblance with the sails of a
154 4  Flight by Membrane

Fig. 4.17  Air flow on a
wing. a Diagram showing
the pressure distribution
at the upper surface of a
wing profile. b Separation
of the laminar flow behind
the position of the pressure
peak. c Transition from
laminar to turbulent flow of
the boundary layer behind
a protruding structure, a
turbulence generator. d
Airflow separation at the
upper surface of the wing. e
Leading edge flap, keeping
the airflow attached to the
surface. Modified after
Norberg (1972; previously
modified after Hertel (1966))

Chinese junk. In a Chinese junk the battens which cross the sails are attached to the
mast and, “since the whole rig is constructed from flexible materials, as the wind
increases, the sail bows out between the battens … without much loss of aerody-
namic efficiency” (Gordon 1978) (Fig. 4.18). Despite very little data in this respect
being available at the time, Gordon noted in bats photographed during flight that
during the downstroke of the wing the membrane bulges outward into a form that
is roughly semi-circular thereby minimizing the mechanical load on the bones,
which themselves to reduce metabolic costs, are cut down in thickness—the entire
arrangement with apparently little or no aerodynamic loss. Norberg (1972) gave
the first real appreciation of the aerodynamics of the bat wing membrane (and dig-
its acting as compression struts) but unfortunately there was little further develop-
ment since, given the uniqueness of this structure in flight mechanisms. That is, not
until a resurgence of an interest by workers such as Tatjana Hubel and colleagues
(2010) and Sharon Swartz and colleagues (2007, 2012, reference in Chap. 5).
4.2  Bats, the Only Mammalian True Fliers 155

Fig. 4.18  A Chinese junk

showing the flexible masts
and membranous-like sails,
aerodynamically similar to
the wings of a bat (Gordon
1978)

Swartz et al. (2012, reference in Chap. 5) drew attention, in particular, to the

unique construction of bat wings which are made of quite flexible bones sup-
porting very compliant and anisotropic wing membranes, possessing many more
independently controllable joints than those of other animals, the significance of
which, as mentioned above, had been suggested by Gordon (1978). These spe-
cial structural design attributes which distinguish them from those of other flying
animals suggest a unique solution to flight mechanics. Their studies of the lesser
short-nosed fruit bats, Cynopterus brachyotis, included wind tunnel experiments
and investigations of the wings from the perspective of:
(1) more than two dozen joints which can be controlled independently to some
degree; (2) bones that deform adaptively during the characteristic motions of the
wingbeat cycle; (3) tremendously anisotropic wing membrane skin with both sub-
stantial variation and adjustable stiffness across the wing; and (4) a distributed net-
work of skin sensory organs believed to provide continuous information regarding
flows over the wing surfaces. The first three of these characteristics, the focus of
their study, together produce wing surfaces whose geometry and kinematics are
far more complex spatially and temporally than the classic literature regarding bat
flight would suggest.
The authors depart from the traditional widely accepted notion of gait in ver-
tebrate flight being rooted in the notion that the wingbeat cycle of birds and bats
can be subdivided into upstroke and downstroke. In bats they suggest these phases
are not only distinct kinematically but also differ fundamentally in aerodynamic
force production. They identify seven to eight independently controllable joints
interposed between the body axis and the wingtip, and the separate fingers of the
primitive mammalian hand structure retain significant autonomy. Moreover, wing
membrane skin is exceptionally compliant and bones may bend under aerody-
namic loading. The result was that there was no rigid way to subdivide the wing-
beat into upstroke and downstroke. The motions of the third digit, the wing’s
primary spanwise support, and the fifth digit, the chordwise support, are not
156 4  Flight by Membrane

synchronous. And, perhaps most importantly, the vertical, side to side, and for-aft
motions of any one wing joint may be nearly completely out of phase. Hence, the
terms ‘upstroke’ and ‘downstroke’ as used in the animal flight literature are rather
misleading when applied to bat flight.
Swartz et al. (2012, reference in Chap. 5) also depart from the view that most
researchers’ hold that the primary mechanical function of the bones of the verte-
brate limb is to resist and transmit loads. Their results they propose, is that wing
bones of bats achieve their mechanical functions in a more flexible and dynamic
fashion, deforming and recoiling with every wing beat. Given that bat wing bones
vary in external dimensions, cross-sectional geometry, and mineralization, and that
aerodynamic forces vary throughout any given wingbeat cycle, with velocity, etc.,
there is a large domain of possible patterns of skeletal deformation during flight.
Arguably the most important aspect of their work is that at biologically rel-
evant Reynolds numbers, even a low degree of compliance can have substantial
effects on aerodynamic performance of simple aerofoils. The skin stretching they
observed clearly varies with orientation within the plane, or more accurately,
the surface of the wing, and across specific anatomical regions. In particular, the
strains along the leading and trailing edges and in the spanwise direction away
from the wing edges are greater than those in the chordwise direction. At least two
phenomena, not mutually exclusive, may contribute to this pattern. First, the dis-
tribution of pressure on the wing surface is complex and dynamically evolving,
and could differentially stress the membrane in different directions; even a simple
pressurized cylinder will have different wall stresses in the longitudinal and cir-
cumferential directions. Second, deformations are constrained by the mechanical
characteristics of the material, and bat wing membrane skin is highly anisotropic,
with stiffness in the chordwise direction typically more than 100-fold greater than
that in the spanwise direction. The patterns of skin stretching that they observed
suggest that local curvature in the wing membrane may be highly variable. In a
sense, there is potential for camber to vary along the wing’s length and throughout
the wing beat cycle.
Tatjana Hubel and colleagues (see Hubel et al. 2010) point out that relatively
little is known about the wake structures typical of bat flight, and even less about
the correlations between wing kinematics and wake structure. To redress this they
investigated the detailed kinematics and wake structure of the lesser dog-faced
fruit bats, Cynopterus brachyotis, flying in a wind tunnel. High speed recordings
of the kinematics were conducted to obtain three-dimensional reconstructions of
wing movements. A key feature of their experiments was the synchronized acqui-
sition of both the flight kinematics and the wake velocity structure, which as the
authors demonstrate was quite a complex process. The simultaneous recording of
particle image velocimetry (PIV) and of kinematics and the subsequent correlation
between the two measurements allowed in principle to link vortex wake structures
to specific geometric features of the wingbeat cycle and conditions such as angle
of attack. The wake structure was dominated by a strong tip vortex that devel-
oped during the downstroke and remained until almost the end of the upstroke.
Among the significant findings, although the portion of the wingbeat cycle with
4.2  Bats, the Only Mammalian True Fliers 157

no tip vortex was very short, the wake structure can still be considered a closed
loop or vortex ring rather than a continuous vortex structure as, e.g., seen in fast
flying birds (Chap. 5). Highly significant in Hubel et al.’s (2010) findings was the
limited appearance of a counter-rotating vortex near the body, as well as a small
distally located vortex system at the end of the upstroke that generated negative
lift (Fig. 4.19a), again differing with the positive lift during the upstroke in birds,
which we will see more of below.
A question perhaps on many aerodynamicists’ minds is, how do bats compare
in flying efficiency with birds? This is exactly the question that Florian Muijres
and colleagues tried to answer in tests to measure the aerodynamic flight effi-
ciency in two passerine bird species, three pied flycatchers (Ficedula hypole-
uca) and one blackcap (Sylvia atricapilla) and two Pallas’ long-tongued bats
(Glossophaga soricina), and two lesser long-nosed bats (Leptonycteris yerbabue-
nae). The species studied are similar in size and thus fly at similar Re No (~104).
Muijres et al. (2012) used PIV measurements of the wake of the animals flying in
a wind tunnel. Their results showed that differences in wake dynamics between the
birds and bats during the upstroke are mainly a result of the presence of reversed
vortex loops in the bats (Fig. 4.19b, c) and tail vortices in the birds. The reversed
vortex loops in the bats are generated by moving the wing upwards at a nega-
tive angle-of-attack resulting in production of positive thrust and negative lift—
increasing with speed. The birds, on the other hand, make their wings inactive
(feathered) during the latter part of the upstroke by retracting them and by spread-
ing the primary wing feathers (see Chaps. 1 and 5). Thus Muijres et al. (2012)
found that there is a clear qualitative and quantitative difference in the function
of the upstroke between the passerine birds and the leaf-nosed bats they studied,
which could be directly related to the difference in L/D. The findings agreed with
models for flapping wings with relatively low L/D (L/D  = 5, i.e., similar to that
of the bats), the energetically optimal flapping kinematics generate thrust in com-
bination with negative lift during the upstroke (i.e., resulting in reversed vortex
loops). The results thus show in both span efficiency for generating lift, and the
lift-to-drag ratio for mechanical energetic flight efficiency, birds significantly out-
perform the bats. The wake patterns were also found to be strikingly similar to
those by Hubel et al. (2010) (Fig. 4.19a) despite considerable differences in the
morphology and flight ecology of the bats involved in the various studies.
Two styles of flight are involved in bats and birds with evolution optimizing
performance relative to the respective conditions of birds and bats, feathered avian
wing is made inactive during the upstroke and body lift is produced, while the
membranous bat wing generates significant flight forces during the upstroke. Both
sets of wingbeat kinematics are close to optimal for the relative flight performance
with the maximum performance limited by phylogenetic constraints on wing and
body morphology. Thus despite as the authors explain the ecological differences
between birds and bats being highly variable, the different aerodynamic flight effi-
ciency for the bird and bat species in their study may help explain why birds typi-
cally fly faster, migrate more frequently and migrate longer distances than bats.
Furthermore, as Norberg and Norberg (2012) remarked, the basic morphology of
158 4  Flight by Membrane

Fig. 4.19  PIV analysis of the lesser dog-faced fruit bats, Cynopterus brachyotis flying in a wind
tunnel at two speeds at 5.0 ± 0.1 and 6.7 ± 0.41 ms−1. a Reconstruction of the 3-D wake struc-
ture based on the 2-D PIV measurements. Sections (A, B and C) correspond to the 2-D vorticity
fields and 3-D isosurface reconstruction (Hubel et al. 2010, Fig. 4). Red arrows counter-clockwise
rotating vortex; blue arrows clockwise rotating vortex; gray arrows predicted vorticity shed in
the parallel plane (x–z-plane) either in the form of shear layers or starting and stopping vortices.
With permission of Tatjana Hubel (Hubel et al. 2010). Wake topologies for one wingbeat of Pal-
las’ long-tongued bats, Glossophaga soricina and lesser long-nosed bats, Leptonycteris yerbabue-
nae, flying in a wind tunnel at 7 m/s. The vorticity iso-surfaces (blue: +ωx iso; red: -ωx iso) show
the main vortex structures, while the color-coded surface shows downwash w (see color bar).
b Female Pallas’ long-tongued bat with ωx iso = ±50 s-1 and downwash scale wmax = 2.1 m/s.
c Female lesser long-nosed bat with ωx iso = ±45 s-1 and wmax = 2.4 m/s. The wind tunnel coor-
dinate system {x,y,z} is in b. Both topologies show the reversed vortex loop (see Fig. 19). After
Muijres et al. (2012). PLos ONE Open Access. e37335. doi:10.1371/journal.pone.0037335
4.2  Bats, the Only Mammalian True Fliers 159

bats may restrict their potential to adapt to terrestrial locomotion and swimming
which is clearly hindered by the wing membrane attached along the entire length
of the hindleg, down to the foot and across the tail. Birds, in short, are the ultimate
vertebrate fliers with the potential to invade a huge range of ecological niches,
which we will see more of in the next chapter.

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Chapter 5
Birds

5.1 Archaeopteryx, the First Bird or Urvogel

Fossils from the Late Jurassic Solnhofen limestones in Bavaria are treasures in
the collections of museums around the world. None more so than a specimen a
mere 35 cm at its longest in the Natural History Museum in London (Fig. 5.1).
This is the first example ever discovered, hence the holotype (serves as a basis for
description of a species), of the fossil bird, Archaeopteryx (ancient wing from f.
archaeo- + Gk pterux wing) and as Richard Fortey (2011) pertinently observes the
date of its discovery is only 2 years after the publication of the Origin of Species,
in which Charles Darwin had famously described as ‘difficulties on theory’ where
he expected a number of criticisms that his great idea would encounter. Prime
among these was ‘the rarity or absence of intermediate forms’ in the fossil record.
With a plethora of mixed characters between reptiles and birds few could fail
to notice that Archaeopteryx was probably the best example of an ­‘intermediate
form’ and that it had turned up with impeccable good timing to s­ upport Darwinian
theory.
To this day Archaeopteryx remains the iconic symbol of bird origins and bird
flight. Although the first irrefutable evidence of this ancient bird was not of the
specimen mentioned above but that of a feather, so unique a structure that it
was possible without hesitation to define the animal it belonged to—a bird. The
feather, like the holotype, was beautifully preserved between the thin fine-grained
Solnhofen limestone slabs. The holotype specimen on the other hand presented
a strange reptile-looking creature, but like nothing ever seen before. Among the
bones were the distinctive feathers of a bird. Yet, other features were typically rep-
tilian such as teeth, forelimb claws, and a long bony tail. Since then several other
specimens were discovered in the Solnhofen limestone, but almost certainly the
best was discovered in 1877, known as the Berlin Archaeopteryx (Fig. 5.1b). It

© Springer-Verlag Berlin Heidelberg 2015 163

T. Lingham-Soliar, The Vertebrate Integument Volume 2,
DOI 10.1007/978-3-662-46005-4_5
164 5 Birds

Fig. 5.1  Three specimens of Archaeopteryx. a London specimen (holotype). b Berlin specimen

before the leg feathers were removed. c Maxberg specimen. d Reconstruction of Archaeopteryx
modified after Rudolph Freund

is an evocative representation of an animal captured in stone soon after its death

(Reisdorf and Wuttke 2012)—its forelimbs stretched out replete with a magnifi-
cent display of feather impressions and the long tail no less striking also complete
with feather impressions.
5.1  Archaeopteryx, the First Bird or Urvogel 165

Fig. 5.2  The localities of all the known specimens of Archaeopteryx. Note the exact locality of
the “Solnhofen” and “Thermopolis” specimens is unknown but it is assumed they are from Eich-
statt (Achim Reisdorf, personal commun. 2014). I am grateful for this figure for the localities of
Archaeopteryx, which was specially modified for this study by Achim Reisdorf from Reisdorf
and Wuttke (2012)

To date 11 skeletal specimens of Archaeopteryx have been discovered in

Solnhofen localities (Fig. 5.2). The latest with perhaps the most complete feather
covering has recently been described (Foth et al. 2014) and will be mentioned
briefly later.
166 5 Birds

Archaeopteryx inhabited a region in what is now southern Germany during a

time when Europe was an archipelago of islands in a shallow warm tropical sea,
the Tethys, much closer to the equator than it is now. The bird is similar in size
to a European Magpie, with the largest individuals possibly attaining the size of a
raven. There are a number of characters that do not compare ideally with those of
a modern bird. For example the sternum was short and not keeled as in a modern
bird, lacking the massive ventral keel, the bones were not hollow and they were
not pneumatic and as mentioned there was a long, bony tail. Nevertheless, most
ornithologists agree that Archaeopteryx is the classic urvogel, that it was quite well
developed as a bird.
It is clear that Archaeopteryx lacked many advanced characters of mod-
ern birds yet many workers claim that these are precisely conditions that one
would expect in an early bird and in particular in an early true flier rather than a
glider. For instance, absence of a keeled sternum in Archaeopteryx may not have
impaired basic flapping flight but simply have prevented sustained flapping flight
(see below). Despite the constraints on design a general acceptance of somewhat
unpretentious flight capabilities in Archaeopteryx may be summed up in the words
of the notable Hungarian paleontologist, Baron von Nopcsa (perhaps better known
to some for his notoriety as the aristocrat who murdered his male lover), when he
described Archaeopteryx as not an altogether badly flying animal but that it could
on no account have been a soaring bird, but a bird that was yet in the first stage of
active flight (von Nopcsa 1907, 1923).

5.1.1 Ground-Up or Trees-Down Origin of Flight?

In 1979 John Ostrom presented a reconstruction of a hypothetical stage in

the early evolution of birds that shows a pre-Archaeopteryx stage and later
Archaeopteryx in which the hands evolve as nets for catching insects (Ostrom
1979) (Fig. 5.3). The running and the flapping hand maneuvers involved in catch-
ing insects would form the basis of Ostrom’s ground-up hypothesis leading to bird
flight. Archaeopteryx, according to his theory was presumably at or just past the
threshold of powered flight. Ostrom had first proposed his theory that birds had
evolved from small carnivorous dinosaurs, in 1973, contra hypotheses at the time
that birds evolved either from crocodiles or from basal archosaurs (thecodontians)
(Ostrom 1973, 1974). Yet, it is not difficult to see how John Ostrom’s discovery
in the 1960s of the early Cretaceous Dromaeosaur, Deinonychus (terrible claw), a
theropod that exhibited many similarities to birds, particularly in the structure of
the hand and wrist, could have been the basis of his ground up idea of bird flight,
an idea perpetuated by some of his students.
One such student was Robert Bakker, who published in 1986 his revolution-
ary book The Dinosaur Heresies, in which among the many controversial claims,
Archaeopteryx was portrayed as an earthbound theropod. By coincidence, just a
few years later when I was ‘tracking’ dinosaurs on the Zimbabwean-Mozambique
5.1  Archaeopteryx, the First Bird or Urvogel 167

Fig. 5.3  Part of John Ostrom’s reconstruction of the ground-up hypothesis of flight in birds

showing hypothetical stages in the use of feathered appendages as insect traps. After Ostrom
(1979)

border (see Volume 1) I met a French big-game hunter, by profession a book

publisher, who had just won the rights to publish Bakker’s book in France. He
explained to me that the laws in France prohibited the use of the word heresy in
all but religious matters and hence he was considering calling the book The Pink
Dinosaur because of its many controversial claims. Perhaps it was more prophetic
than he had realized in the light of the alleged findings of reddish-hued feathers in
the dinosaur, Sinosauropteryx (see Chaps. 6 and 7).
Another strong supporter of the ground-up or cursorial hypothesis of bird flight
is Kevin Padian, who as we saw in Chap. 4, extended the theory to pterosaurs.
Padian (1985, 2001) denounced the arboreal hypothesis of bird flight as a ‘false
one,’stating “[b]ecause theropod dinosaurs were cursorial predators, the cursorial
hypothesis is consistent with theropod phylogeny” and, “[f]or these paleontolo-
gists all speculation concerning the origin of flight must follow the cladogram that
dictates a theropod origin of birds and flight from the ground up.” The strength
of feelings on the ground-up hypothesis is encapsulated in these comments. We
will next consider the trees-down hypothesis briefly and return to some of Kevin
Padian’s views in Chap. 7.

5.1.1.1 Claws

Following on from the ‘ground-up or trees-down’ hypothesis, it seems appropriate

to begin with how well or not Archaeopteryx was adapted to an arboreal habitat by
considering the claws or perching capabilities (Fig. 5.4).
168 5 Birds

Fig. 5.4  Overview
photograph of the 11th
skeletal specimen of
Archaeopteryx. After Foth
et al. (2014), courtesy of
Macmillan Press

In a rigorous study designed to test the hypothesis above in which

Archaeopteryx was thought to have been a feathered predator adapted to run-
ning as part of a terrestrial evolutionary stage from coelurosaurian dinosaurs,
Alan Feduccia (1993) examined the claws of over 500 different types of birds
with respect their claw geometry of the foot or pes (degree of curvature) and
whether it is a useful index for arboreal versus terrestrial habits in birds. The
major separation of birds on the basis of claw arc measurements was between
ground-dwellers and others. Arboreal birds were for the most part separable
between trunk dwellers and perching birds. The pes claws of digit III of the
measurable specimens of Archaeopteryx (the London, Berlin, and Eichstatt)
were conservatively reconstructed with arcs 125°, 120°, and 115°, respectively.
The Early Cretaceous, fully volant perching bird Sinornis santensis, which is
only slightly younger than Archaeopteryx, has strongly curved claws: The curva-
ture of its digit III claw is about 130°–135°, which is at the upper end of perch-
ing birds. Feduccia found that all of the measurements of the claws of the pes of
Archaeopteryx fell within the range of the three strongest perching birds meas-
ured including the strong perching touracos. In contrast, he showed that claw
geometry of birds that are both tree- and ground-dwellers and ground dwellers
tends to reflect the terrestrial more than the arboreal adaptation. Furthermore,
the study showed that manus (hand) claws of Archaeopteryx differ markedly
from those of predatory dinosaurs in that they exhibit lateral compression in
extensor view and have needlelike points. The claws of predators, including
theropods, tend to be conical and smoothly tapered. Predatory birds have wide
pes claws with lateral cutting edges whereas the pes claws of theropods (for
example, Compsognathus) are characterized by small arc angles, like those of
ground-dwelling birds (Fig. 5.5).
5.1  Archaeopteryx, the First Bird or Urvogel 169

Fig. 5.5  Archaeopteryx. a, b Detail of foot of Archaeopteryx. c Morphology of foot of lyre bird.

Modified from Feduccia (1979)
170 5 Birds

The findings with respect to Archaeopteryx’s flight capabilities may be signifi-

cant as it “used the claws of the manus for clinging to branches because it had not
yet achieved the balance that is characteristic of modern birds…[i]t was capable of
trunk-climbing but may have done so only occasionally, after flying to the ground.
Archaeopteryx was probably incapable of taking off from the ground … climbing
would have allowed the bird to reach a suitable place from which to launch, where
it could take advantage of the cheap energy provided by gravity” (Feduccia 1993,
p. 792).
Derek Yalden (1997) also argued that the pedal claws of Archaeopteryx have a
very different shape in cross-section from those of Compsognathus and that while
the latter are those of a terrestrial animal, those of Archaeopteryx are of a climbing
animal. In addition to which, he had earlier argued (Yalden 1985) that the highly
curved, very sharp ungual phalanges and claws of the manus and the orientation of
these claws, which Ostrom suggested as indicative of a predatory function, seem
better explained as indicative of a climbing function.
However, in the 10th specimen of Archaeopteryx Mayr et al. (2005) suggested
that it lacked the fully reversed toe thereby limiting its ability to perch on branches
whereas Feduccia (2012) argues that full reversal of the hallux is not required for a
perching foot (see the 11th specimen; Fig. 5.6b).

5.1.1.2 Archaeopteryx: Powered or Unpowered Flight?

Storrs Olson and Alan Feduccia (1979) went to the heart of the two principal lines
of evidence given for regarding Archaeopteryx as flightless or at best an inept non-
flapping glider. First, interpretations of the structure of the pectoral girdle and the
frequently cited absence of an ossified sternum for attachment of flight muscles
and second, that the structure of the coracoid of Archaeopteryx would not have
permitted the supracoracoideus muscle to function as a wing elevator. These argu-
ments have often been cited in perhaps the most controversial topic with respect to
Archaeopteryx, the origin of flight, and whether it occurred in either the ‘ground
up’ or ‘trees down’ hypothesis.
Olson and Feduccia (1979) proposed that the generally held and prevalent view
that the carina of the sternum is the principal site of the origin of the massive pec-
toralis muscle, which provides the power stroke, is a misconception. In most birds,
they state, the pectoralis originates to a greater extent from the furcula and the
coraco-clavicular membrane (Fig. 5.7).
They show that in such birds as members of the Dendrocolaptidae in which the
carina is reduced to facilitate tree-trunk foraging, the pectoralis becomes thin and
broad, spreading out laterally and dorsally well past the sternum and on to the rib
cage. Importantly, they indicate that once anchored to the furcula area, the pec-
toralis could apparently extend posteriorly and attach to any underlying structure
present.
Olson and Feduccia suggested that a well-developed furcula in Archaeopteryx
has never been in doubt and is actually hypertrophied compared to modern birds
5.1  Archaeopteryx, the First Bird or Urvogel 171

Fig. 5.6  Details of the plumage of the 11th specimen of Archaeopteryx. a Right wing from dor-
sal view. b Leg feathers of the right hind limb. c Detail of leg feathers of right hind limb. d Detail
of body plumage from the belly region. e Overview of tail feathers. f Detail of asymmetrical
feathers at the lateral side of the tail. Arrow in a indicates gap in the wing caused by the overlap-
ping left foot. Scale bars, 1 cm. After Foth et al. (2014), courtesy of Macmillan Press Ltd

and best interpreted as having been the site of origin of a well-developed pectora-
lis muscle. The main function of the carina and ossified sternum in modern birds
they suggest is to provide attachment for the supracoracoideus muscle, which is
the largest of the muscles that affect the recovery stroke of the wing. They further
point out that it has been proven that the supracoracoideus is not essential for nor-
mal sustained flight and that the only capacity lost was the ability, as demonstrated
in the pigeon, to take off from level ground and that in modern birds the dorsal
elevators, principally the deltoideus major, are completely capable of effecting the
recovery stroke of the wing. These muscles originate from the scapula, which in
Archaeopteryx is apparently more than adequately developed. Rather the authors
suggest that the enlarged, ventrally situated supracoracoideus, the acrocoracoid
process and the ossified sternum with a keel, constitute a single functional com-
plex that is not a requisite of flight but merely a refinement that was superimposed
in later birds.
172 5 Birds

Fig. 5.7  Comparison of the pectoral girdles of an extant bird (a and c) and the first definite bird
(b and d) showing the differences in the relative sizes of the bones constituting the pectoral gir-
dle. a, c European Starling (Sturnus vulgaris): a Lateral view of the shoulder girdle. c Lateral
view of the entire skeleton in natural posture. b, d Archaeopteryx. b Lateral view of the shoulder
girdle. d Lateral view of the reconstructed skeleton in presumably natural posture. The two birds
are not drawn to scale. Modified from Jenkins (1993)

Bock’s (2013) study with respect to interpreting the flight musculature of

Archaeopteryx is scholarly and timely in the context of a recent revival in ques-
tions related to the flight capabilities of Archaeopteryx. To this end he performed
dissections on the American Crow, Corvus brachyrhynchos, which were used for
comparison with the presumed flight muscles in Archaeopteryx and in addition
dissections were made on the domestic chicken (Gallus gallus) and the domesti-
cated pigeon (Rock Dove, Columba livia). The study is largely critical of Olson
and Feduccia’s conclusions (1979).
Among Bock’s mains criticisms of Olson and Feduccia are that they had con-
cluded that the avian pectoralis muscle originates mainly from the furcula and the
coracoclavicular aponeurosis (=membranous ligament) and not largely from the
sternum, without reporting any dissections of this muscle in Columba livia or any
other Recent birds. Bock contested the fundamental view of Olson and Feduccia
that a “robust” furcula in Archaeopteryx equals a large pectoralis and hence active
5.1  Archaeopteryx, the First Bird or Urvogel 173

flight in this early bird and that they had presented no descriptive details of the
morphology of the furcula, which on the face of it appeared rather short compared
to that of Recent flying birds and certainly not hypertrophied as stated by Olson
and Feduccia. Bock concluded, “[t]here is no basis for postulating that the caudal
part of the pectoralis in Archaeopteryx was sufficiently large for active flapping
flight” but presumably was sufficient in size to hold the wings in a horizontal posi-
tion necessary for aerial locomotion and that the combination of features in the
pectoral system of Archaeopteryx strongly indicated that this bird was a special-
ized glider, not an active flapping flier.
Elzanowski (2002) sheds light on the structure of the furcula which he
described as, “broadly open dorsally, almost twice as wide as it is deep, and its
two rami meet at a right angle… [e]ach ramus is much wider transversely than
it is thick rostrocaudally, which makes the furcula of Archaeopteryx look sturdy
in front view, as if it were designed to resist transverse compression, but less so
in lateral view.” He adds it is not hypertrophied, contrary to Olson and Feduccia
(1979).
However, it is important to remember that Olson and Feduccia include the
coraco-clavicular membrane as an attachment site for the pectoralis muscle. They
may also be correct in stating that the principal site of the origin for the massive
pectoralis muscle on the carina of the sternum, as provision for the power stroke, is
a misconception. Colin Pennycuick (1972), whose major contributions to bird flight
are discussed in a later section, refers to the apparent function of the prominent
carina or ventral keel of the sternum in Recent birds as support for the pectoralis
in such a way that it does not exert pressure on the supracoracoideus when it con-
tracts or occlude the branch of the interclavicular air sac which lies between the
two muscles. In the later evolutionary developments of more massive flight mus-
cles this would make sense but would seem of lesser importance at early stages of
powered flight. Importantly, Pennycuick adds, “The size of the carina is not neces-
sarily related to the size of the pectoralis muscle in all flying vertebrates, and it is
wrong to conclude that pterosaurs had feeble pectoralis muscles because most of
them had only a poorly developed sternal keel.” Most bats, he indicates also have
only a small keel, “but the large pectoral muscles of the two sides have their origins
in a median ligamentous sheet which extends ventrally from the sternum, and pull
against one another” (based on Norberg 1970a, [reference in Pennycuick 1972]).
The points that Walter Bock raises are valid and cannot be ignored with respect
to powered flight capabilities of Archaeopteryx. However, the question that remains
is whether this should be viewed as an all or nothing process, i.e., active flying on
the one hand and gliding on the other, contra a middle-ground of inceptive pow-
ered flight. This has been considered from a biomechanical perspective by authors
such as Colin Pennycuick (1972) and Ulla M. Lindhe Norberg (1985, 1990), who
­suggest the viability of powered flight in Archaeopteryx.
Arguably among the most important of the factors that indicate powered flight
are the asymmetric feather vanes of Archaeopteryx. Alan Feduccia and Harrison B.
Tordoff (1979) demonstrated that “[v]anes in the primary flight ­ feathers of
Archaeopteryx conform to the asymmetric pattern in modern flying birds” and
174 5 Birds

have remained essentially unchanged for approximately 150 million years (since
late Jurassic times). They also show that even in weak fliers among Recent birds
there is a generally diminishing state from the asymmetric to symmetric charac-
ter state. Aerodynamically there seems little doubt of the flight function of the
asymmetric feather vane of Archaeopteryx, which is a defining characteristic of
airfoils (Chap. 1). This has been interpreted as evidence that it was a flyer, as
flightless birds tend to have symmetrical feathers. Nevertheless, whether asym-
metrical feathers can indiscriminately be interpreted as a condition of powered or
flapping flight as opposed to non-powered or gliding flight is moot. For instance,
Speakman and Thomson (1994) questioned this. In a short communication in
Nature they refer to their study of more than 70 families of living birds, in which
they found that some flightless types do have a range of asymmetry in their feath-
ers, and that the feathers of Archaeopteryx fall into this range. Although the iso-
lated feather (Fig. 5.8) exhibited an asymmetry of 2.2—just within the range of
modern flying birds, it is not known whether this feather is from Archaeopteryx, or
where on Archaeopteryx the feather was situated if it is an Archaeopteryx feather.
Evidence of the interest that Archaeopteryx still enlists is reflected in a paper
that rapidly followed on the heels of Thomson and Speakman. R. Åke Norberg
(1995), contrary to the latter study, showed that the degree of feather asymme-
try in Archaeopteryx, rather than occurring in flightless birds, is more typical for
slow flyers. R. Åke Norberg (1985) pointed out that the curvature of the feather
is also important in flight ability, and Archaeopteryx’s feathers exhibit significant
curvature.

Fig. 5.8  The first feather,

thought to be from
Archaeopteryx, discovered in
1860/1861 in the Solnhofen
Limestone in Bavaria
5.1  Archaeopteryx, the First Bird or Urvogel 175

A study by Robert Nudds and Gareth Dyke (2010a) was among the latest to
involve this crucial question of the flight capabilities of Archaeopteryx (and other
fossil birds) from a new and potentially decisive point of view. The authors pro-
pose the superiority of their investigation over others by their use of engineering
concepts (Nudds and Dyke 2010b). In support of the idea held by some workers
that early birds such as Archaeopteryx and Confuciusornis were incapable of pow-
ered or flapping flight, the authors presented an argument that the rachises in these
early birds were much thinner and weaker than those of modern birds, and thus
they were not capable of flight. The measurement data in Confuciusornis were
refuted by Zheng and colleagues (2010) and independently for Archaeopteryx by
Gregory Paul (2010). However, both critiques were dismissed by Nudds and Dyke
(2010b). For example, they reject Paul’s criticism of their mass estimates for these
fossil birds by stating that Paul did not present any new primary feather safety
factors based on his body mass estimates. Nudds and Dyke (2010b) rejected the
entirety of the criticisms by saying, “[i]f the feathers of early birds were too weak
to withstand the forces of flight, then we know (thanks to the laws of physics) that
they could not fly regardless of any other morphological features they might, or
might not, have possessed.” It was therefore on what they claimed was the inviola-
bility of their study (Nudds and Dyke 2010a, b), i.e., the laws of physics and their
use of engineering concepts that I challenged their study (Lingham-Soliar 2014a).
The authors’ proposition of a model on bird flight capabilities is based on Euler-
Bernoulli beam theory and the engineering principle of a thin-walled cylinder (see
Chap. 1). They calculated the feather safety factor (the point at which it would be
seriously damaged) (Corning and Biewener 1998) on the basis of an empty thin-
walled cylinder (the latter as an homogeneous shell). We know that the rachis shell
is not homogeneous (Lingham-Soliar et al. 2010; Lingham-Soliar and Murugan
2013) and that it not an empty shell but filled by a medullary foam core, which is
known to significantly increase its mechanical efficiency (Karam and Gibson 1995;
Dawson and Gibson 2006; Weiss and Kirchner 2010). Their findings were that the
feather rachis fell significantly short of the safety factor. However, Nudds and Dyke
(2010a) state that, in Archaeopteryx, ‘‘[o]nly if the primary feather rachises were
solid in crosssection (the strongest structural configuration), and not hollow as in
living birds, would flight have been possible,’’ i.e., it would have to have ‘‘…had a
feather structure that was fundamentally different from that of living birds.”
Besides the unsound aspects of their test methodology, which we will go into
below, on this comment alone they unwittingly destroy their entire argument.
Materials scientists have shown for years that the foam core is in effect a ‘cellular
solid’, because it is designed to give similar mechanical properties to a solid but
at low weight, particularly effective in buckling stress (Gibson and Ashby 1999;
Bonser 2001; Fratzl and Weinkamer 2007; Lingham-Soliar et al. 2010). As dis-
cussed above, nature adopts this advantageous strategy on numerous occasions in
biological systems like wood, bone, cork, plant stems, glass sponges, bird beaks
and feathers (see references above). Mechanical tests corroborated such findings,
i.e., that, during transverse loading of the rachis, the medullary core takes up 96 %
of the load, leaving just 4 % to the cortex (Weiss and Kirchner 2010).
176 5 Birds

Unfortunately, the claims by Nudds and Dyke (2010b) that their method over
others is ‘‘quantitative’’ rather than ‘‘subjective’’, and that they are supported by
the laws of physics, is not supported by either the feather structural data, mechani-
cal analyses or statistics. Not only do Nudds and Dyke’s investigations ignore a
major component of the feather rachis, the foam core but they also use a formula
that is inappropriate—the calculations have little quantitative basis with respect to
real feather structure and lack statistical significance—only one feather was tested.
Following my above critique (Lingham-Soliar 2014a), a response was made by
a colleague of Nudds and Dyke, Colin Palmer (2014). Because the arguments pre-
sented by Nudds and Dyke and by Palmer could potentially close the door at a
stroke on Archaeopteryx’s ability to actively fly, extracts from Palmer (2014) and
my own rebuttal (Lingham-Soliar 2014b) will be included here so that readers can
independently, without translation, form their own conclusions.
Palmer’s comments:
“L-S’s first objection to the work of Nudds and Dyke (2010a, b) is that these
authors used an ‘‘inappropriate formula’’ taken from Corning and Biewener
(1998); thus, they ‘‘ignore a vital structural feature of the rachis, the medullary
foam core, which is known to significantly increase mechanical efficiency’’ (L-S
2014, p. 12). The formula used by Nudds and Dyke (2010a, b) was the classical
Brazier buckling formula for thin-walled circular tubes, a reasonable approxima-
tion for the calamus region of the rachis (note also that there is no foam in the
calamus: Purslow and Vincent 1978). This is the region subjected to the highest
bending moment, and thus most likely to be the region to fail.”
L-S’s reply:
“The calamus and the rachis are quite distinct structural components of the pri-
mary feather shaft. Thus, while the concept of the thin-walled, circular engineer-
ing tube may be a reasonable approximation for the calamus because it lacks a
foam center, by default it would not be a reasonable approximation for the rachis,
the structure investigated by Nudds and Dyke (2010a, b), which has a foam center.
For example, Azuma (2006, p. 37) describes the rachis as ‘‘a rectangular center
filled with foam material and can more easily accommodate bending distortion
than the quill [calamus].’’ Furthermore, Palmer refers to the calamus as the region
subjected to the highest bending moment, and thus the most likely region to fail
(a statement he makes without support or citation). Yet, it is irrelevant because of
the quite distinctive structural environment and biomechanics of the calamus com-
pared to the rachis, i.e., quite unlike the rachis it is completely embedded in the
avian skin (Homberger and de Silva 2000).”
Palmer’s comments:
“L-S (2014, p. 12) argues that an alternative formulation should have been used,
one that is applicable to a foam sandwich structure. Had he taken the time to com-
pare the two formulas for a typical rachis geometry, he would have found that,
in fact, the sandwich formula gives a failure bending moment almost an order
of magnitude less than that given by the tube formula. So, had Nudds and Dyke
5.1  Archaeopteryx, the First Bird or Urvogel 177

(2010a, b) used the formula that L-S (2014) argues that they should have used,
they would have predicted even weaker feathers for Archaeopteryx.”
L-S’s reply:
“I did take Corning and Biewener’s (1998) formula on trust, as one invariably does
in respected publications. Nevertheless, the point I had made was based on a sim-
ple question of logic—the rachis possesses a medullary pith, and Corning and
Biewener’s (1998) formula 5 allegedly allowed for a medullary pith (a foam sand-
wich structure; their formula 4 does not). However, Palmer (2014) claims, albeit
without evidence, that formula 5 gives a failure bending moment almost an order of
magnitude less than that given by the bare tube formula. Even if this is accepted, we
have two choices: (1) it invalidates the sandwich principle in typical biological and
engineering systems, or (2) formula 5 is faulty. Furthermore, Corning and Biewener’s
formulae (p. 3059) use a Poisson ratio based on wool, i.e., ‘softer’, more ‘bendy’ (low
modulus) α-keratin. Feathers comprise the stiffer (high modulus) β-keratin—this is
important… That study suffers from additional fundamental weaknesses.”
Palmer’s comments:
“L-S (2014) then goes further in his misuse of Weiss and Kirchner (2010) in
order to criticise Nudds and Dyke (2010a, b) for ‘‘ignoring the foam’’, when he
says that ‘‘during transverse loading of the rachis, the medullary core takes up to
96 % of the load…’’ (p. 12). In fact, the transverse loading referred to by Weiss
and Kirchner (2010) is lateral crushing load (lateral compression), so their result
has absolutely no relevance whatsoever to the dorsoventral bending discussed by
Nudds and Dyke (2010a, b). This point is actually made in the abstract of Weiss
and Kirchner (2010): ‘‘The cortex (longitudinal Young’s modulus 3.3 GPa, trans-
verse modulus 1 GPa) provides 96 % of the longitudinal strength and bending
rigidity of the feather. The medulla (Young’s modulus 10 MPa) provides 96 % of
the transverse compressive rigidity.”
L-S’s reply:
“Palmer attempts to understate the finding by Weiss and Kirchner (2010) with
respect to transverse loading in his subjective dismissal of its relevance solely to
a lateral crushing load. Note, Weiss and Kirchner’s (2010) transverse loading of
the rachis is the closest we have to understanding the contribution to transverse
strength by the medulla. By the same token, Weiss and Kirchner’s findings of lon-
gitudinal stiffness and bending rigidity, which Palmer recommends in support of
Nudds and Dyke (2010a, b), has limited relevance to bending moments involv-
ing buckling, probably the singular most important factor of failure in feathers
(Corning and Biewener 1998)—in Weiss and Kirchner’s work (2010), the rachis
(cortex or medulla or both) was not loaded in pure bending (involving compres-
sive loads), but rather, solely in tension, which gives breaking stress. Corning and
Biewener (1998) demonstrated that the rachis of pigeon flight feathers failed by
buckling during four-point bending tests, and their remarks that ‘‘feather shafts are
most likely to fail through local buckling of their compact keratin cortex’’ is note-
worthy—and underscores the vital role of the medulla in minimizing it (below).”
178 5 Birds

Palmer’s comments:
“These woeful misinterpretations of Weiss and Kirchner (2010) provide the whole
basis of L-S’s (2014) criticism of Nudds and Dyke (2010a, b), yet are totally
incorrect… L-S (2014) uses a demonstrably incorrect interpretation of data and
misuses citations to support a very strong critique of Nudds and Dyke (2010a, b).
His critique has no basis in fact.”
L-S’s reply:
“There is nothing to misinterpret in my citation of Weiss and Kirchner (2010):
‘‘during transverse loading of the rachis, the medullary core takes up 96 % of the
load, leaving just 4 % to the cortex.’’ In contrast, Palmer (2014) and Nudds and
Dyke (2010a, b) completely ignore local buckling loads in feather biomechanics.
Their dismissal of the role of the medulla in feather biomechanics to a minor one
must be seen as a wider, albeit unfounded criticism of the many biomechanical
and engineering applications of foam centers against bending stresses in cylindri-
cal and sandwich structures.”
We will return to the paper by Nudds and Dyke (2010a) briefly in Chap. 7,
which deals with controversies in the field.
Debate on whether or not Archaeopteryx was an active flyer clearly enlists
considerable passion. Bock’s (2013) paper with its useful anatomical discussions
is a necessary contribution to questions with respect to the flying capabilities of
Archaeopteryx. It may be that no single argument proposed may hold the answer,
and that in the midst of the issues raised above there may lie a combination of
strong circumstantial evidence that suggests in Archaeopteryx a bird that may be
beyond a glider but rather on the basal rungs of powered flight. These may be enu-
merated here as: (1) the evolution of a perching foot and Archaeopteryx’s place
either among the trees; (2) the asymmetric feather venation of Archaeopteryx
that has been largely unchanged for over 150 million years of evolution; (3) the
regular spacing of barbs throughout the feather’s length and clear impressions
of barbules; (4) remiges of Archaeopteryx are curved, an expression of aerody-
namic design seen in modern volant birds; (5) presence in flight feathers of a ven-
tral, reinforcing furrow, as in modern flying birds; (6) the classic elliptical wing
as in modern woodland birds; (7) the wing morphology (primaries and coverts)
of Archaeopteryx conforms to that of modern birds, and remiges show robust
rachides (Foth et al. 2014) and; (8) a large brain.

5.2 Feather Evolution

Feathers represent the extreme in integumentary complexity and while there has been
progress in understanding feather biochemistry and molecular structure we have
only recently begun to understand its microstructural and biomechanical complex-
ity (Lingham-Soliar et al. 2010; Lingham-Soliar and Murugan 2013; see end of this
chapter). Hence it is not surprising that the evolution of the feather has attracted as
5.2  Feather Evolution 179

Fig. 5.9  The predicted transition series of feather morphologies from an independent, develop-

mental model of the evolutionary origin of feathers14. The model14 hypothesizes that the first
feather originated with the first follicle—a cylindrical epidermal invagination around a papilla.
Subsequent feather diversity evolved through a series of derived novelties in the developmental
mechanisms within the follicle. The integumental appendages of Sinornithosaurus described here
are congruent with Stages II and IIIa, whereas the integumental appendages of Sinosauropteryx2
(Chen et al. 1998) are congruent in morphology with Stage 1. Stage 1, an unbranched, hollow
filament; Stage 2, a tuft of barbs basally fused to a calamus; Stage 3a, a feather with a rachis and
serially fused barbs; Stage 3a+b, a feather with rachis, barbs and barbules. Stage 4 (not shown),
a bipinnate feather with differentiated distal and proximal barbules and a closed pennaceous
vane; Stage 5a–f (not shown), additional modern feather diversity including asymmetrical flight
feathers. After Xu et al. (2001), courtesy of Macmillan Press Ltd

much attention as it has and also given that it is closely tied to the evolution of birds.
Yet, feather evolution has become highly polarized (Feduccia 1997, 2012; Chiappe
2007). There are essentially two views. One, the classic theory that they evolved
from reptilian scales (Maderson 1972) and the other, as proposed by Richard Prum
and Alan Brush (2002, 2003) that feathers evolved from a novel tubular structure of
the integument (an exaptation of a structure for a new function) that passed through
several stages with the most evolved being the flight feather (Fig. 5.9).
Recent discoveries from the Early Cretaceous of China have highlighted this
aspect of the debate (Xu et al. 2001; Prum and Brush 2002, 2003), with claims
of the discovery of all stages of feather evolution as interpreted from a number
of meat-eating dinosaurs found in Liaoning, China, although the deposits are at
least 25 million years younger than those containing the earliest known bird
Archaeopteryx. The apparent explanations for the time anomaly have been gener-
ally reasonably explained by incompleteness of the fossil record. In this context
the discovery of Anchiornis and Xiaotingia may hold answers to the ‘temporal
paradox’ argument in that they are close in age to Archaeopteryx and may in fact
be slightly older (Sullivan et al. 2014). They possessed advanced feathers simi-
lar to those of Archaeopteryx. On the other hand the earliest of such dinosaurs
believed to have possessed basal feathers, and perhaps the most controversial, is
Sinosauropteryx (of which more will be said in Chaps. 6 and 7) (Fig. 5.10).
The classic view is that the aerodynamic feather evolved first and other feather
types developing later, as suggested in Protopteryx by Zhang and Zhou (2000).
Connected with this view is the belief that while birds and dinosaurs have a
180 5 Birds

Fig. 5.10  A reconstruction
of Sinosauropteryx, a basal
theropod dinosaur sporting
feathers as hypothesized by
some workers

common ancestor, dinosaurs are a separate branch from birds and that birds are
not directly derived from them. Feduccia and colleagues have put forward evi-
dence relating to the most critical character thought to link birds to derived thero-
pods, a tridactyl hand composed of digits 1–2–3. They maintain the evidence
supports interpretation of bird wing digit identity as 2, 3, 4, which appears differ-
ent from that in theropod dinosaurs. They also suggest that a possible solution to
the disparate data is that Aves plus bird-like maniraptoran theropods (e.g., micro-
raptors and others) may be a separate clade, distinctive from the main lineage of
Theropoda, a remnant of the early avian radiation, exhibiting all stages of flight
and flightlessness. This debate was reviewed in Feduccia et al. (2005) and dis-
cussed further in Riddle of the Feathered Dragons (Feduccia 2012). The debate
will not be repeated here except in the context of understanding the integumentary
structures associated with dinosaurs, in particular the idea of protofeathers.
However, a new twist to the story of bird evolution has emerged with respect
to a specimen, Scansoriopteryx (Czerkas and Feduccia 2014) (Fig. 5.11).
Microscopic re-examination of the fossil Scansoriopteryx, a problematic sparrow-
size pre-Archaeopteryx specimen from the mid-Jurassic Daohugou Biotas, has
provided new evidence which challenged the widely held hypothesis that birds
are derived from theropod dinosaurs and flight originated from earth-bound dino-
saurs by a cursorial model. Previously considered a small theropod dinosaur, the
absence of fundamental dinosaurian characteristics the authors argue demonstrates
that this small arboreal archosaur was not derived from a dinosaurian ances-
try and should not be considered as a theropod dinosaur. This specimen they say
provides strong evidence that the basal origins of Aves stemmed from outside the
Dinosauria and further back to basal archosaurs. Impressions of primitive feathers
5.2  Feather Evolution 181

Fig. 5.11  Left mainslab of Scansoriopteryx; and right counterslab, shown slightly smaller than
life size. Scale bars 1 cm. Inset skeletal reconstruction, approximately half life size (reconstruc-
tion, Stephen A. Czerkas). With permission of Czerkas and Feduccia (2014)

on the forelimbs and hind limbs suggest that Scansoriopteryx was a four winged
form and represents a basal form of ‘‘tetrapteryx,” probably at a parachuting or
gliding stage of flight evolution. Scansoriopteryx seems to have fulfilled predic-
tions from the early twentieth century that the ancestors of birds were derived
from earlier arboreal archosaurs which originated flight according to the tradi-
tional trees-down scenario. With future discoveries of additional mid-Jurassic fos-
sils many of the mysteries shrouding the origin of birds may be answered.
Given the recent description of the 11th specimen of Archaeopteryx, we need to
briefly mention the extensive feather preservation, not only on the wings and tail,
but also on the body and legs as described by the authors (Foth et al. 2014). The
authors propose that the wide array of feathers and feather types allow an inter-
pretation with respect to the ongoing debate on how pennaceous feathers evolved.
Their analysis of the phylogenetic distribution of pennaceous feathers on the
tail, hind limb and arms of advanced maniraptorans and basal avialans they say
strongly indicates that these structures evolved in a functional context other than
flight, most probably in relation to display, as suggested by some previous stud-
ies (Zhang and Zhou 2000) and that only later were pennaceous feathers exapted
(taken from an original use to a new and different use) for aerodynamic functions.
Given the contentious nature of the field, there seems little doubt that others views
will emerge over the next few years. We will now move on approximately 150 mil-
lion years to present day birds.
182 5 Birds

5.3 The Unique Flight Apparatus of Birds

The organisms that inhabit our planet are defined by their success in both diversity
and abundance. Diverse groups include many species and abundant groups have
many individuals in some or most species. Flying, extant animals, despite making
use of energetically probably the most expensive mode of locomotion, yet they are
by the above criteria unusually successful. Scientists have named about 22,000 spe-
cies of tetrapods (land vertebrates; see Volume 1 for a description of their incredible
evolution). With over 9,000 species birds make up nearly half of this total and bats
with about 1,000 of the 4,200 known mammal species are the second largest group
among the mammals (only rodents are more diverse) (Alexander 2002).
As we mentioned in Chap. 1, flight in animals involves (1) the shape of the
entire organism, (2) the shape of the limbs e.g., wings, and, uniquely in birds, (3)
the shape and structure of the integumental structures covering the body, namely
feathers. All three conditions are found uniquely in birds.

5.3.1 Wing Structure

The bird wing is shaped by its bony skeleton, muscles, and plumage. The plumage
consists of (1) primary feathers (primaries), (2) secondary feathers (secondaries),
(3) tertiary feathers (tertiaries), (4) humeral and auxiliary feathers such as scapu-
lars, and (5) the alulae or bastard wings.
A birds wing, as a consequence of being formed by numerous, tough individ-
ual feathers, has greater resistance to damage compared to membranous wings,
(see Chaps. 3 and 4), allows packing into a streamline shape and with respect to
the feathers, they are replaced annually and in some birds twice a year. The joint
system within the wings themselves and with the shoulder enable complex move-
ments consisting of “feathering” (pitch change), “flapping” (out-plane) and “lag-
ging” (in-plane) motions. The shoulder is involved in all motions, whereas the
elbow is mostly used to shorten the wing by folding compactly in the lagging
direction or in the shape of the letter Z. In contrast the wrist joint appears to be
responsible for all additional motions of the hand or outer wing, by which the
outer wing attains a widened angle of attack (Azuma 2006, and references therein)
(Figs. 5.12 and 5.13).

5.3.2 Flight Muscles

Flapping flight places strenuous requirements on the physiological p­ erfor­mance 

of an animal. Bird flight muscles, particularly at smaller body sizes, gener-
ally contract at high frequencies and do substantial work in order to produce
5.3  The Unique Flight Apparatus of Birds 183

Fig. 5.12  Bird wing structure showing feather positions. Dorsal view. Modified after Proctor
and Lynch (1993)

Fig. 5.13  Bird wing structure showing feather positions and attachment sites on the hand, fore-
arm and upper arm. Ventral view. Modified after Proctor and Lynch (1993)

the aerodynamic power needed to support the animal’s weight in the air and to
overcome drag (Biewener 2011). Birds power flight primarily by large pectoralis
muscles (approx. 8–11 % body mass), which also pronates the wing, and attaches
to the humerus of the wing at the deltopectoral crest (DPC). Its main portion
(sternobrachialis, SB) originates from an enlarged sternal keel, with more ante-
rior fibers arising from the furcula, or ‘wishbone’ and a much smaller portion
184 5 Birds

(thoracobrachialis, TB) originates dorsally from the ribs. The fibers of the TB and
the posterior region of the SB insert on an internal aponeurosis that merges with
the more anterior SB fibers before attaching to the DPC. The smaller supracora-
coideus, deep to the pectoralis, also originates from the keel of the sternum (but
about one fifth the size of the pectoralis). It is the primary wing elevator particu-
larly at slow to moderate speeds and during hovering, working by means of its
tendon, which inserts and acts dorsally at the shoulder (via the triosseal foramen)
as a pulley and attaching to the dorsal surface of the proximal humerus (Biewener
2011) (Fig. 5.14).
The avian pectoralis muscle is well suited to performing work with large length
excursions. This is a prerequisite for powering flight because the wings must move
through a large excursion during each wing stroke to produce effective aerody-
namic lift. This is enabled by the property of the pectoralis and supracoracoideus
muscles to shorten over a large fraction of their resting fiber length (33–42 %).
Two smaller muscles, the triceps and biceps, operate over a smaller range of

Fig. 5.14  Anatomical organization of avian wing musculature. Modified from Biewener (2011)

5.3  The Unique Flight Apparatus of Birds 185

contractile strains (12–23 %), reflecting their role in controlling wing shape

through elbow flexion and extension (Biewener 2011).

5.3.3 Flight Feathers

The arrangement of wing feathers (remiges) and tail feathers (rectrices) is shown
for a bird of prey (Fig. 5.15). The longest wing feathers are the primaries (P)
which extend from the carpal (‘wrist’) joint towards the wing tip. They are gener-
ally numbered from the carpal joint to the end of the extended wing. This is the
descendant numbering system (Cieslak and Dul 2006 and references therein),
although it should be noted that some books and scientific papers use an ascend-
ant system whereby primary feathers are numbered from the wing tip to the car-
pal joint. The shorter secondary (S) flight feathers grow from the ulna (forewing
bone); these are always numbered from the carpal joint inwards towards the body.
The innermost secondaries are also referred to as tertials or tertiaries, especially
for passerine birds such as the raven (Proctor and Lynch 1993). The primaries
and secondaries together form the lifting surface of the wing. Tail feathers (T)
are numbered from the central pair of feathers outwards. All diurnal raptors, owls
and the raven have 10 functional primaries (P) on each wing and 12 tail feathers.
Raptor vanes may be emarginated on the inner vane or outer or both (Fig. 5.16). A
vestigial eleventh primary (P11) is present in most raptor families except the true

Fig. 5.15  Figure illustrating the location and nomenclature of wing and tail feathers in an
osprey. Modified from “Raptors: a field guide for surveys and monitoring” (Part 3), online (2014)
186 5 Birds

Fig. 5.16  Flight feathers in a juvenile peregrine falcon, Falco peregrinus. From “Raptors: a field
guide for surveys and monitoring” (Part 3), online (2014)

hawks (Accipiters). The number of secondaries is more variable, increasing with

the size of the bird and wing length ranging from 10 to 21 in, e.g., raptors (Gill
1995).
The typical feather consists of a central shaft (rachis), applied to the portion
of the axis of the feather that in life, protrudes from the skin, and the lower part
which penetrates the skin and provides attachment is termed the calamus or quill.
Arising from the rachis are serial paired branches (barbs) extending out from
the shaft at an angle and lying parallel to each other. The barbs possess further
branches—the barbules—and the barbules of adjacent barbs are attached to one
another by hooks. The entire system comprising of the barbs and barbules forms a
vane or web on either side of the rachis, providing the lifting surfaces of the wing
and tail feathers. This construction ensures the elasticity of the feather web as well
as the capacity of the barbs to re-establish linkage if the continuity of the web is
interrupted (Fig. 5.17). We will look at the microstructure of the rachis and barbs
and associated biomechanics in a section at the end of this chapter.
We have seen above a glimpse of the unique adaptations of the integument in
birds that have contributed to their wing and body morphology to produce the
most complex design for flight in the animal kingdom. However, to exploit that
design something special was needed, which we will look at next.
5.4  Flight Control Center 187

Fig. 5.17  Feather-structure in modern bird. a Feather showing rachis and barbules, which make
up the venation. b Diagrammatic cross-section of the rachis. c Inset showing a diagrammatic
view of barbs and barbules. d SEM of venation of approximate section in diagrammatic inner
white circle in c showing how barbules of opposite barbs hook up

5.4 Flight Control Center

A month or so after my arriving in Port Elizabeth, South Africa, Mark Upman, a

local pastor, learning of my interest in bird flight, told me of something strange
he had seen at some high cliffs about 150 km along the coast. He had observed an
eagle dropping something about the size of a football from just above the cliff top
toward the rocks and water over a hundred meters below. However, just seconds
188 5 Birds

Fig. 5.18  Predatory birds need split second timing to catch live prey. This African fish eagle, Hali-
aeetus vocifer, has to adjust to strike at a fish swimming below the water surface by making allow-
ance for the refraction of light altering its apparent position. Photo permission of Clint Ralph

before it could hit the ground the eagle had swooped down and gathered the mys-
terious object in its beak. It repeated this curious behavior several times. However,
on the last occasion he noted that as the object plummeted, to his astonishment
what appeared to be a pair of wings unfolded and he realized at that moment that
the object was the eagle’s young, which it was apparently preparing for flight.
What struck me immediately was the remarkable speed, agility, timing, and gen-
tleness that was needed for this single act. It unlocked a recollection of what John
Maynard Smith had attributed this kind of sophisticated behavior to—the evolu-
tion of the most fine-tuned nervous and sensory system in birds.
Richard Dawkins (2008) in a warm tribute noted not long after the death of
Maynard Smith that his essay ‘The Importance of the Nervous System in the
Evolution of Animal Flight’ (Maynard Smith 1952), fascinatingly brought his two
careers together, an aeronautical engineer during the war that he later traded for
5.4  Flight Control Center 189

biology. Maynard Smith wrote that since birds do not have to learn to fly or at most
need only to perfect by practice an ability already present, it follows that there has
been the evolution of the sensory and nervous system to ensure the correct responses
in flight (Fig. 5.18). He noted, perhaps at first glance seeming paradoxical, that prim-
itive flying animals had a form of built in stability, i.e., forces acting on it tend to
restore it to its course without any modification of that cycle of contractions being
required. Stability requires control in three axes (Fig. 5.19). He added that in practice
the most important type of stability is that for rotation about the pitching axis that is
a horizontal axis normal to the flight path. In both gliding and flapping flight, stabil-
ity in pitch can be ensured by the presence of an adequate horizontal surface behind
the centre of gravity. This stability is referred to as static stability. Maynard Smith
suggested that there is good reason to believe that earliest fliers such as in birds were
stable in the sense defined above—possessed a long tail bordered on either side by a
row of feathers, the whole forming a very effective stabilizing surface.
It appears therefore that primitive flying animals tend to be stable, presumably as
Maynard Smith presciently noted, because in the absence of a highly evolved sensory
and nervous system they would have been unable to fly if they were not, just as a pilot
cannot control an unstable aeroplane. In contrast, in a highly evolved flying animal,
there are great advantages to be gained by instability, perhaps most importantly the
greater maneuverability (at speed) to an animal that catches its prey in the air with split-
second changes of speed and direction. Other advantages are a successful landing in a
large flying animal (in geometrically similar animals, the stalling speed increases as the
square root of the linear dimensions) may be possible only if it can reduce its stalling
speed, and instability is one of the ways in which this may be done. A bird that wishes
to descend rapidly may bank sharply. As the angle of bank (Φ) is increased the radius
of turn becomes smaller but the sinking speed increases (Pennycuick 1972) (Fig. 5.20).
Maynard Smith suggested that the evolutionary changes needed for stable flight
could be made rather quickly while the nervous and sensory adjustments needed
for unstable flight were inevitably slower—requiring a greater adaptability of the
brain. Below, we will briefly look at newer perceptions on bird brains that may
also assist an appreciation of bird flight and navigation in later sections.

5.4.1 Bird Brains

Nathan Emery (2006) has shown that the long-held term bird-brains to imply low
intelligence is incorrect and largely based on the confusing terminology used to
name the different regions of the avian telencephalon (forebrain). Based on this,
birds were thus deemed incapable of producing flexible or intelligent behaviour,
whereas as Emery states it is now known that this nomenclature is based on a fal-
lacy and that large parts of the avian forebrain are derived, not from the striatum,
but from the pallium (Fig. 5.21). Interestingly, the mammalian neocortex is also
derived from the pallium, which places the avian forebrain into a new light where
bird behaviour may now be explained as an adaptation to solving socioecological
problems similar to mammals.
190 5 Birds

Fig. 5.19  Axis of rotation, Mp, Mr and My are the pitch, roll and yaw moments about the trans-
verse, longitudinal (median) and vertical axis respectively, and Cpm, Crm and Cym, their respective
moment coefficients. Modified from Norberg (1990) with photo by permission of Jordan Ralph

Fig. 5.20  A yellow-billed duck Anas undulata, banking (roll around transverse axis) steeply to
lose height quickly. The control of roll can be achieved by differential twisting of the wings so that
the angle of attack can be different in the two wings (here greater in the right wing). The attitude of
the head is retained as though controlled by a gyroscope. Photo by permission of Clint Ralph

Just as in angels, all birds are created equally, only some more equal than oth-
ers. For instance among birds demonstrating the highest cognitive abilities are cor-
vids and parrots, which have forebrains relatively the same size as those of apes,
have demonstrated ape-like intelligence, live in complex social groups and have a
long developmental period before becoming independent (Emery 2006).
5.4  Flight Control Center 191

Fig. 5.21  Bird brain. a Classic view of the avian telencephalon, in which the greatest proportion
of the cerebrum is classified as striatal in origin (dark grey shading), compared to the smaller
extent of the pallium (light grey shading). b Recent view of the avian telencephalon, in which
the majority of the cerebrum has been reclassified as pallial in origin (light grey shading) com-
pared to the smaller striatum (dark grey shading). Adapted from Jarvis and Consortium (2005).
CDL area corticoidea dorsolateralis; E, ectostriatum (classic) or entopallium (revised); HA hyper-
striatum accessorium (classic) or hyperpallium apicale (revised); HP hippocampal complex; IHA
interstitial nucleus of the hyperpallium intercalatum; L2 field L2; LPO parolfactory lobe; OB
olfactory bulb. Figure by permission of Nathan Emery (2006)

E.D. Jarvis (2009) states that the realization of a relatively large and well-
developed avian pallium that processes information in a similar manner to mam-
malian sensory and motor cortices may help explain some of the cognitive abilities
of birds. Jarvis notes some of these abilities as summarized by the Avian Brain
Nomenclature Consortium: pigeons can memorize up to 725 different visual pat-
terns, learn to categorically discriminate objects as ‘human-made’ versus ‘natural,’
discriminate cubistic and impressionistic styles of painting, communicate using
visual symbols, rank patterns using transitive inferential logic, and occasion-
ally ‘lie.’ New Caledonian crows make tools out of leaves or novel human-made
material, use them appropriately to retrieve food, and are believed to pass this
knowledge on to other crows through social learning. Magpies develop an under-
standing of object constancy at an earlier relative age in their life span than any
other organism tested and can use this skill to the same extent as humans. Scrub-
jays show episodic memory, recall for events that take place at a specific time or
place, once thought to be unique to humans. This same species modifies its food-
storing strategy according to the possibility of future stealing by other birds and
therefore displays a behavior that would qualify as theory of mind. Owls have a
highly sophisticated capacity for sound localization, used for nocturnal hunting,
that rivals that of humans and that is developed through learning. Parrots, hum-
mingbirds, and oscine songbirds possess the rare skill of vocal learning. This trait
is a critical substrate in humans for spoken language, and with the exceptions
of cetaceans and possibly bats and elephants, it is not found in any other mam-
mal. Parrots, in addition, can learn human words and use them to communicate
192 5 Birds

reciprocally with humans. African gray parrots in particular can use human words
in numerical and relational concepts–abilities once thought unique to humans.
These vocal behaviors are controlled by vocal learning pathways through both pal-
lial and subpallial regions.
These cognitive functions are carried out by the telencephalon, including the
six-layered cortex in mammals but by nuclear pallial areas in birds. Hence, the
mammalian six-layered cortical architecture is not the only neuroarchitectural
solution for the generation of complex cognitive behaviors (Jarvis 2009). Emery
(2006) notes that such differences suggest that complex cognition has evolved in
species with very different brains through a process of convergent evolution rather
than shared ancestry, although birds and mammals may share common neural
connectivity.
Such new and innovative research may allow us to appreciate better some of
the complex activities of birds. Among which, we may now be a little prepared for
perhaps the greatest wonderment of birds, flight. We will start with a brief look at
some of the earliest recorded observations of bird flight.

5.5 The Phenomenon of Flapping Flight in Birds

Although in this chapter we are concerned with flapping or powered flight, we

include special gliders among birds here because it is connected with their peculiar
behavioral strategies involving the conservation of energy and not a constraint.

5.5.1 Some Early Observations on Bird Flight

The complex flying behavior of birds has both fascinated and inspired human-
kind over the centuries. It is said that much of Leonardo’s success lay in the
fact that he started from basic principles (possibly forced upon him because
apparently he could not read Latin, the language of science at the time).
Significant too, was his implicit belief in Nature as an instructor “That a man
ought not to trust to himself, but ought to consult Nature.” There is no doubt
that birds inspired his flying machines, which can be found in his two Madrid
notebooks that deal extensively with his theory of mechanics. The first was
written in the 1490s and the second between 1,503 and 1,505 but will not be
delved further into here (see Whiting 2005). We move on a few centuries to
other early pioneers of aeronautical engineering such as Sir George Cayley in
the early 1800s, who rejected the notion of using moveable wings on aircraft
and promoted the concept of fixed wings, and the German aeronautical pioneer,
Otto Lilienthal, from whose work the Wright brothers drew heavily. However,
from the perspective of recorded observations of bird flight a little needs to be
said of Étienne-Jules Marey.
5.5  The Phenomenon of Flapping Flight in Birds 193

Fig. 5.22  Drawing from photos showing successive positions of a seagull during one complete
wing revolution. a Front view, b Side view, c Above view. Modified after Marey (1894)

As a result of an innovative camera developed by Marey (1894) he was able

to clarify and analyze the complete cycle of the wing-beating motion of a bird
(Figs.  5.22 and 5.23). Marey was able to develop a “clockwork train” intermit-
tent movement in a photographic “gun” with a sight to “shoot” birds in flight. He
employed strips of sensitized paper in 1887 and paper-backed celluloid in 1889
instead of the fragile, bulky glass. A forerunner of the motion picture camera it made
12 exposures of 1/72th of a second each. In the early 1880s Marey published his
pictures of birds in flight made with his ‘photographic gun’ (Marey 1894). Marey’s
observations concerning the changes in the shape of birds’ wings in relation to air
resistance was a vital precursor to understanding the phenomenon of bird flight.

5.5.2 Understanding Flapping Flight

Studies with a very pragmatic approach to understanding bird flight by pioneers

such as Marey paved the way for investigations in the field in the first half of
the twentieth century. In Chap. 3 we considered gliding or non-powered flight in
194 5 Birds

Fig. 5.23  Sequential photographs of bird flight. a Flight of pelicans. b Flight of seagulls. Modi-

fied after Marey (1894)

which gravity plays a decisive role but here the emphasis is on powered flight as
used by birds working against gravity by beating or flapping the wings (Fig. 5.24).
We have noted that from a mechanical perspective, wing beating consists of
four fundamental motions:
(1) an out-plane motion called flapping. (2) an in-plane motion called lead-
lag or simply lagging. (3) a twisting motion of the wing pitch called feathering,
and (4) an alternately extending and contracting of the wing span called spanning
(Azuma 2006).
Figure  5.25 shows two typical phases of the beating motion of a bird’s wing
in cruising flight. In the upstroke of the wing (or recovery stroke), the downflow
caused by the wingbeat is stronger at the outer wing than at the inner wing, thus
the lifting force, which is normal to the total inflow, is tilted either up- and back-
ward more at the outer wing that at the inner wing for positive angle of attack
(α > 0) or down. In the downstroke or powerstroke, the upflow caused by the wing
beat is again stronger at the outer wing than at the inner wing: thus, the lifting
force is tilted forward more at the outer wing than at the inner wing. The forward
component of the lifting force generates a propulsive force against the drag force
generated by the wings themselves and the body. Overall therefore, the inner part
of the wing produces mostly upward force and no thrust, whereas the outer part of
the wing provides most of the thrust, but may also produce considerable upward
force (Azuma 2006) (Fig. 5.25).
5.5  The Phenomenon of Flapping Flight in Birds 195

Fig. 5.24  Flight strokes
of jackal buzzard, Buteo
rufofuscus. Photo by
permission of Clint Ralph
196 5 Birds

Fig. 5.25  Beating motion and resulting aerodynamic force (see Azuma 2006) of wing sections
(illustrated with photos of a yellow-billed duck, Anas undulata, by permission of Clint Ralph):
a Upstroke. b Downstroke

We saw in Chap. 1 how lift on a wing is achieved namely that it is the vector
sum of the lift (perpendicular to the air flow) and the drag (parallel to the direction
of the air flow), which gives the resultant, i.e., forward thrust. In normal flight such
as in a pigeon for example most of the useful aerodynamic forces are produced
during the downstroke when the wing moves with the downward path ahead of the
upward path relative to the body (Norberg 1990; Pennycuick 2008). To obtain an
optimal angle of attack along the entire wings during the powerstroke, the animal
must be able to twist the wings, which in turn requires adaptations in the skeletal
and muscular systems (Norberg 1990). Thus, the upstroke and downstroke must
be different for the bird to produce thrust. This twisting from wing root to tip is
so that the spanwise station can maintain a reasonable range of angle of attack
(Azuma 2006). As we showed, the basal part of the wing supplies most of the
supporting surface, the wing tip most of the propelling force (cf. bat wing beat
in Chap. 4). The many adjustable features of the bird wing enable the complex
motions of bird flight; it can be shortened or lengthened by flexion; the feathers
of the tip can be spread or closed; the angle of the whole wing or its parts, on
one side or the other or on both sides, can be altered (Figs. 5.12, 5.13 and 5.14).
McNeill Alexander described how these features enable flight in, e.g., the pigeon.
Alexander (1968) showed the wing position of a pigeon flying very slowly with
the body tilted at a large angle to the horizontal (Fig. 5.26a, b). As forward speed
increases, the body is held more horizontally. During the downstroke the wings are
extended and swung downwards and then forwards (Fig. 5.26c, d). They extend
5.5  The Phenomenon of Flapping Flight in Birds 197

Fig. 5.26  Wing tracings
from photographs taken
at intervals of 0.01 s on a
pigeon in slow flight. a–d
Downstroke. e–h Upstroke.
(See text for details).
Modified after Alexander
(1968) and Norberg (1990)

laterally from the body but are nearly parallel to each. Figure 5.26e, f shows the
beginning of the upstroke.
Alexander (1968) pointed out that slow flight in the pigeon seems much more
strenuous than normal flight and can only be maintained for a few seconds. In the
upstroke to reduce wing area and drag the wings are more or less flexed at the
elbow and the wing moves back led by the bent wrist until there is a sudden flick
(Fig.  5.26g) which moves the wing tip very rapidly through the position shown
and extends the wing above the back and the primaries separate as in hovering.
In slow flight the secondary flight feathers at the base of the wing behave very
differently from the wing tip primaries. Frequently, however, the primary feath-
ers in bird flight are treated as one and the same with respect to function, which
is a mistake. In slow flight the secondary feathers near the base of the wing move
slowly because the body is moving slowly, but the primary feathers at the wing tip
move fast. Only the primaries at the wing tip can produce substantial aerodynamic
forces (Alexander 1968). Alexander also notes that although it is suggested the
upstroke is merely a recovery stroke with the feathers “feathered” like oars, that
the distal primaries are bent up and forward (Fig. 5.26g) and that this shows that
an upward and forward force is acting on them.
198 5 Birds

The flight feathers of the wing are so arranged that each feather is overlapped
from the wing tip to the root by the one next to it. Together, they form an adapt-
able lifting surface, capable of keeping together or separating (Azuma 2006;
Fig. 5.27a–d). This is why the primaries keep together during the downstroke, aid-
ing forward thrust, and separate during the upstroke (minimizing loss of forward
momentum (Alexander 1968; Fig. 5.27e). The distal primaries act as individual
aerofoils and produce this force. Observations of an increase in vane asymmetry
toward the wing tip are consistent with this function.
Usually, slow flight is only briefly used, at take-off and landing. Normal,
medium and fast flight are quite different. The whole bird moves quite rapidly
through the air so that the wings do not have to move as fast, relative to the body,
to provide enough lift—as Biewener (2011) notes during fast flight the birds aer-
odynamics play an important part and muscular exertions may be reduced. Both
amplitude and frequency of the wing beats is less in normal flight than at take-off.
Wing beating is modified in birds to perform different functions including the way
in which the wing tip primaries behave. A number of different kinds of birds pro-
duce varying force on the upstroke compared to the downstroke during fast flight

Fig. 5.27  Wing feather
configurations. a Position
on wing. b Tight position.
c Spread position. d Reversed
position. e Feather positions
during flight, upstroke and
downstroke. Modified after
Azuma (2006) and Alexander
(1968)
5.5  The Phenomenon of Flapping Flight in Birds 199

by a reduction of the angle of attack of the wing. Changes are also made in slow
and hovering flight (Alexander 2002). We will see how some of these distinctions
influence the different lifestyles of birds below.

5.5.3 Departures and Arrivals

We saw above the way in which a small bird such as a pigeon may take off—an
upward jump followed by powerful flapping of the wings. However, in many birds
the problems of take-off are compounded by the bird’s weight and wing shape.
Many birds that are beautifully adept and graceful in the air are quite ungainly in
the transition from land to air as seabirds such as the Cape gannet, Morus capen-
sis (Fig. 5.28), because they are encumbered both by weight and need to avoid
smashing the long wings on the ground while vigorously flapping them to gain
lift. Furthermore, dependent on their size, they will need relatively longer runways
to gain enough speed and lift for take-off. In the Cape peninsula in South Africa a
quick and successful take-off may even be a matter of life and death for a gannet,
particularly during the breeding season when jackals see young gannets as easy prey.
The problem of a take-off may be intensified in large water birds with high-aspect
ratio wings and short legs, having to take off and land on water. This is exacerbated
by having to push against a moving substance rather than firm land. Nevertheless, they
appear to do the same thing as they would on land—what they actually do is push down
and back with their wide, webbed feet with a running motion that helps thrust the body
and reduces the drag, which enables lift from the beating wings (Fig. 5.29).
Landing in large birds is perhaps an even greater problem and can be embarrass-
ing or worse if the bird doesn’t get it exactly right. The finest control and timing is
required. Large birds that have to land on firm surfaces on a regular basis cannot
afford to make a serious error even just the once, which can have fatal consequences.
It needs to choose the right place to land and the right speed, especially in the midst
of a crowded flock (Fig. 5.30). It must descend to a chosen landing place and adjust
its speed so that it moves just fast enough to maintain lift while at the same time
slow enough to avoid crashing to the ground. One way would be to increase the
angle of attack of the wings and increase the lift and induced drag. Some birds use
rising air to hover before landing. Other birds landing on water such as a yellow-
billed duck, Anas undulata, may even resort to a ‘ski landing’ (Fig. 5.31).

5.6 The Power of Flight

Research in the late 1960s dramatically revolutionized the way in which some
of the more complex aspects of bird flight would be unraveled. During this time
some of the most inventive and rigorous research resulted in landmark findings
that would address issues such as bird flight energetics and speeds (Tucker 1968;
200 5 Birds

Fig. 5.28  A Juvenile Cape gannet, Morus capensis, taking-off. They need long runways so they
can taxi along for several meters. The long wings may come perilously close to the ground at
times. Photo by permission of Clint Ralph
5.6  The Power of Flight 201

Fig. 5.29  The African darter or snakebird, Anhinga rufa. The bird runs across the water to get
up to flying speed and reduce the flapping effort by the wings to lift it out of the water and into
the air. Photo by permission of Clint Ralph

Pennycuick 1968a, b). We saw in Chap. 1 the phenomenon of turbulence as the

rule and not the exception in animal flight and that while Navier-Stokes equa-
tions (the general differential equations in viscous fluid motion), which describe
the aerodynamic forces that keep fliers aloft, would, in principle, solve the prob-
lem of how birds fly, the complexity of the equations defies scientists to this day.
However, before we continue our discussion on the questions of trailing vortices
202 5 Birds

Fig. 5.30  Cape gannet, Morus capensis, landing. Landing in the midst of a colony requires pre-
cision and timing. The bird may use rising air to slow its descent by hovering before landing.
Photo by permission of Clint Ralph

Fig. 5.31  A yellow-billed duck, Anas undulata, landing on water. The duck reduces speed by a
high angle of attack of the wing and increasing lift by spreading the primary feathers. It touches
down by sliding the tail along the water and using its webbed feet as skis. Photo by permission of
Clint Ralph
5.6  The Power of Flight 203

or wake turbulence and its application to bird flight mechanics we need to first
look at a classic study that revolutionized research on the mechanics of bird flight.

5.6.1 The Power Curve

Colin Pennycuick’s innovative research methods in 1968 using trained pigeons

(Columba livia) in a wind tunnel with strategically placed cine cameras would have
major ramifications on the study of bird flight for years to come (they coincided with
wind tunnel experiments by Vance Tucker (1968) using trained budgerigars). The
application of wind-tunnel research was not new at this time but ranged from routine
testing of airframes to fundamental research on the boundary layer, the slow-moving
layer of air adjacent to any water- wind-exposed body surface. Indeed, at the dawn
of powered aviation the Wright brothers constructed a small wind tunnel with which
to gather their own information on the behavior in an airstream of model wings of
various shapes and sizes, cleverly realizing that the failure of their gliders to match
calculated performance was the result of errors in the experimental data published
by their predecessors. The rest is history. Pennycuick, however, was among the first
workers to apply aspects of aircraft research to the study of bird flight.
Anders Hedenström’s (2009) tribute article to Pennycuick’s paper (1968b) in
the JEB Classics series points to the ingenious results derived from the pigeon
experiments that enabled a quantitatively accurate mechanical model of bird flight.
This data was coupled with that from a companion paper in which Pennycuick
also estimated some basic properties for the bird in steady gliding flight in a tilted
wind tunnel (Pennycuick 1968a), including how the profile drag coefficient var-
ies in relation to the lift coefficient and the magnitude of the parasite drag coeffi-
cient of a bird. Pennycuick used this information about wing lift and drag from the
body and wings to develop his classic ‘momentum jet’ model (as in *helicopters)
of flapping flight mechanics (Hedenström 2009).
*In this model the bird is considered as an ‘actuator’ or circular disc of diam-
eter equal to the wingspan, which generates a downward deflected uniform jet.
However, the fact that the wings are flapping and generating a pulsed wake is
ignored by this model, which will be considered below.
Pennycuick’s wind tunnel experiments allowed him to assign values to the three
power components—induced power due to lift generation (declines with U), parasite
power due to the drag of the body, that increases with U, and profile power due to
drag of the wings (see Chap. 1), which added together yielded the famous U-shaped
power curve of animal flight (Fig. 5.32). The ‘power curve’ which expresses the rela-
tionship between power consumption (energy required) and air speed for a flying
animal, has since come to dominate the study of vertebrate flight and is a convenient
formulation for the performance of a flying animal and valuable as a tool for com-
paring different flight patterns or behavioural strategies.
Essentially the power curve shows that at low speeds more power is required
because the wings must be moved fast enough to support the animals near dead
204 5 Birds

Fig. 5.32  Power curves.
a The induced power (a)
required to fly is a maximum
at zero speed (hovering)
and decreases as speed is
increased, while the parasite
power (b) starts at zero and
increases with the cube of
speed. The sum of these
two components (c) gives
a U-shaped graph with a
definite minimum. b Curve
of power required versus
forward speed, constructed
by adding a constant profile
power Po to the curve of
5.32a. Figure by permission
of Colin Pennycuick (1972)

weight (as we saw above and also in Biewener (2011)), the extreme being when
the animal maintains a stationary position solely by the beating of its wings as
in some kinds of hovering (see below), which requires enormous power input.
Intermediate speeds require the least power. However, as a bird speeds up from
this intermediate speed, it needs increasing power to fly faster because pressure
and viscous drag increase (see Chap. 1), These power requirements at different
speeds are predictable by the U-shaped curve for all animals that use wings to fly.
Pennycuick was also able to develop the law that the mechanical power required to
fly increases as (body mass)7/6, which combined with scaling of power available from
muscles (proportional to mass2/3)—what this means is muscle force is related to the
cross-sectional area of a muscle, which only increases two-thirds as fast as body mass
increases. As an animal gets bigger, muscles move more slowly, there is proportionally
less muscle area, which further reduces available muscle power. Calculations based on
these factors suggest that there is an upper size limit for self-powered vertebrate flight of
about 12 kg (~120 N) (Pennycuick 1972, 2008) (Fig. 5.33).
There was an important practical provision in Pennycuick’s paper (1968b), i.e., it
included tables and diagrams that allowed anyone to calculate potential flight ranges in
migratory birds given only the fuel load (expressed as a fraction of take-off mass) and
a minimum of morphological parameters. This characteristic of Pennycuick’s studies is
maintained to the present day with free distribution of computer programs that allow
workers’ own calculations on bird flight performance such as optimal flight speeds and
5.6  The Power of Flight 205

Fig. 5.33  Body and size

limit in practicable flying
animals. a Power required
to fly. b Power available
from muscles. Figure by
permission of Pennycuick
(1972)

flight range and curves for any species and any atmosphere according to his model.
Pennycuick’s Flight program software is now freely available from: http://www.bio.
bristol.ac.uk/people/pennycuick.htm.
Crucial to such calculations was Pennycuick’s theoretical angle of attack in the calcu-
lations of the flight performance and implicit was the existence of certain optimal flight
speeds, which could be generalized and applied to any bird. Pennycuick’s U-shaped
power curve on bird metabolic measurements and flight speeds (Fig. 5.32) is, however,
not without criticism, principally that some results suggest a flatter power curve (e.g.,
see Rayner and Ward 1999, discussed below). However, generally speaking, the power
required for overcoming viscous, pressure and induced drag at a range of different
speeds conforms very much to his power graphs, which are also more practical to apply.
Today, computer simulations have reduced the amount of wind-tunnel testing neces-
sary and different methods are largely used to study the aerodynamics of bird and bat
flight. Also, while the momentum jet model developed by Pennycuick (1968b) provided
a working model that significantly changed our perceptions on bird flight and in par-
ticular the need for innovative methods of research, there were some simplifications
(Hedenström 2009), specifically in avoiding the highly complex problem of wake vor-
tices produced by a flying bird and consequently insensitive to variability in wingbeat
kinematics and to what certain workers refer to as the true dynamics of vortex flows
in the wake (Rayner 1979a, b). As a result they say the momentum jet model fails to
predict the rise in induced power (the power required to offset gravitational forces) at
high speeds which represents the need for some momentum in the wake to provide an
increasing forward thrust to balance friction drags (see e.g., Von Karman reverse vortex
street in Chap. 1). This will be dealt with in the next section on trailing vortices in birds.

5.6.2 Wake Vortices

We considered so far in this chapter high lift mechanisms involved in beating

or flapping flight in birds. We will now briefly consider the effects of the wake
206 5 Birds

that is created by, and trails off, the beating wing, resulting in a vortex. This is a
theme that will reoccur in our discussions on birds below. As we saw in Chap. 1,
Newton’s Third Law states that for every action there is an equal and opposite
reaction. How the vortex works can be seen in a stationary, hovering helicopter,
it produces an upward force by driving air downward. To fly forward it must drive
air backward as well, to supply the forward thrust. Similarly, an animal that is fly-
ing forward rather than merely hovering must drive air downward, for weight sup-
port, and backward, for thrust.
Birds are known to employ two different gaits in flapping flight, a vortex-ring
gait in slow flight (we will see an exception below) and a continuous-vortex gait
in fast flight (see Chap. 1). In the vortex ring gait, the upstroke is aerodynami-
cally passive (there is no bound circulation during this phase, and hence no trail-
ing vortex), and the wings flex and move close to the body to minimize drag. In
the continuous vortex gait (where each wingtip sheds a separate vortex trail during
both the upstroke and downstroke), the wings are aerodynamically active through-
out (i.e., lift is generated both during the downstroke and the upstroke), while the
wings remain near-planar throughout and deform only by flexure at the wrist.
Hedrick et al. (2002) studied the use of these gaits over a wide range of speeds in
cockatiels and ringed turtle-doves trained to fly in a wind tunnel. Despite differ-
ences in wing shape and wing loading, both species shifted from a vortex-ring to a
continuous-vortex gait at a speed of 7 m/s. They found that the shift from a vortex-
ring to a continuous-vortex gait depended on sufficient forward velocity to provide
airflow over the wing during the upstroke similar to that during the downstroke.
This shift in flight gait appeared to reflect the need to minimize drag and produce
forward thrust in order to fly at high speed.
The ordered large-scale vortex structures in the wakes of flying birds provide
valuable clues to flight performance, to the forces acting on the wings and pectoral
girdle in flight, and to the mechanical energy output (Rayner and Gordon 1997).
By experimental visualization of the wake vortex patterns (e.g., Spedding et al.
1984, 1987) and by ciné-photography of wing beat kinematics it was possible to
visualize wakes by using a cloud of helium bubbles, photographed with multiple
flashes over a brief time period (Spedding et al. 1984; Spedding 1986, 1987, 1992)
(Fig. 5.34). The method was used to show the wakes of the pigeon, Columba livia
and the kestrel, Falco tinnunculus, i.e., the vortex-ring and continuous-vortex gaits
respectively (Fig. 5.34).
Note that, in the vortex ring gait, the intense rotational flows that characterize
the vortices are evident, but these are not seen in the continuous vortex gait. It was
possible to determine that only two locomotor gaits are used by birds in steady
flapping flight (Rayner 1993). The kind of vortex gait determined by the geometry
and strength of the flow fields, which may also be predicted by theoretical mod-
elling, in which the properties of bird wings acting as aerofoils are modelled by
discrete vortex theory (Rayner 1979a) for the vortex-ring gait or by large-ampli-
tude lifting-line theory (Rayner 1993) for the continuous-vortex gait (see Chap. 1,
Fig. 1.26).
5.6  The Power of Flight 207

Fig. 5.34  Flow visualization images by helium-bubble multi-flash photography (top) and sketch

of vortex wake (below) as reconstructed by stereophotogrammetry, for the vortex ring gait in a
slow-flying pigeon Columba livia (~3 m−1) (left from Spedding et al. 1984), and continuous vor-
tex gait in a kestrel, Falco tinnunculus (~7 m−1) in cruising flight (right from Spedding 1987).
Both are seen in lateral view. Figures by permission of Geoff Spedding

These images have hitherto been analysed by manual stereophotogrammetry,

but workers are now able to analyse them automatically with a computer-based
particle tracking system. With this technique it is possible to determine the full
time-varying velocity and vortex fields behind the wings, and from this informa-
tion can more accurately compute the induced drag on the wings and determine
other aerodynamic components of energy consumption and mechanical perfor-
mance in flight.
Some debate surrounds the nature of the U-shaped power curve. Rayner and
colleagues suggest that while direct measurements of total physiological energy
uptake in flight at varying speeds in wind tunnels sometimes show a U-shaped
relationship between power and speed (or components of it), that on other occa-
sions experiments have shown that power is independent of speed (reviews by
Rayner 1993; Rayner and Gordon 1997; Rayner and Ward 1999). As they state the
main distinction between these measurements and the theories mentioned above is
that mechanical energy output is only a component of the total energy balance of
the bird, i.e., considerable energy is released by the muscles in the production of
mechanical work and some energy is consumed by other physiological processes.
Other factors may be that efficiency depends on muscle performance (on contrac-
tion rate and strain), which in turn are determined by wingbeat kinematics. Such
factors may account for flatter power ‘curves’. In the following section on special-
ist forms of bird flight, we will return to some of the above problems.
208 5 Birds

5.7 Behavior and Flight in Birds: Horses for Courses

5.7.1 Wingbeat Kinematics in Slow-Flying

Swallows have adapted to hunting insects on the wing by developing a slender,

streamlined body and long pointed wings, which allow great maneuverability and
endurance, as well as frequent periods of gliding. Their body shape allows for very
efficient flight, which costs 50–75 % less for swallows than equivalent passerines
of the same size.
Commuting or migrating, birds are assumed to fly near the speed yielding mini-
mum energetic costs per unit distance travelled (called maximum range speed,
Umr) on which most bird flight research has focused (Pennycuick 2008). Many
small birds, however, often fly much slower, particularly those that hunt or feed on
the wing or live in cluttered environments. Yet, Muijres and colleagues (2012 and
references therein) state not much is known about their flight speed and distribu-
tions in the wild.
Birds that feed on the wing, such as the bee-eater, Merops apiaster (Fig. 5.35),
and flycatchers, are small. The pied flycatcher weighs about 14 g, an insectivo-
rous passerine hunts insects mainly on the wing. While flying slowly, passerines
generate most of the flight forces during the downstroke, and have a ‘feathered
upstroke’. Pied Flycatchers are adapted to low speed flight, which they habitually
use when catching insects on the wing.

Fig. 5.35  White fronted bee-eater, Merops apiaster, feeding on the wing. The slender, pointed
wings of the bee-eater are the trademark of a bird that feeds on the wing in open airspace and it
saves energy by a form of flight known as bounding flight (discussed in text). Photo by permis-
sion of Clint Ralph
5.7  Behavior and Flight in Birds: Horses for Courses 209

Muijres et al. (2012) estimated the aerodynamic flight performance of three

flycatchers based on stereoscopic flight kinematics measurements in combination
with aerodynamic wake data, measured using stereoscopic time-resolved particle
image velocimetry, PIV, which we saw earlier used in bat flight studies. This tech-
nique enabled them to determine the vortex wake pattern and induced (the power
required to offset gravitational forces) downwash distribution behind the flying
animal, which is used to estimate the temporal flight forces and flight performance
values such as the lift-to-drag ratio (L/D), the span efficiency and the flap effi-
ciency throughout the measured flight speed range.
The authors (Muijres et al. 2012) showed through wake dynamics data that dur-
ing the downstroke, slow-flying flycatchers generate a single-vortex loop wake,
which is much more similar to that generated by birds at cruising flight speeds (see
above in kestrel) than it is to the double loop vortex wake in hovering humming-
birds and pigeons (Fig. 5.34). This is similar to the downstroke wake of blackcaps
Sylvia atricapilla and a common swift measured under similar flight speeds and
test conditions to those of the authors. During the upstroke, slow-flying flycatchers
generated strong tail vortices, while the wings were inactive. This is similar to the
upstroke wakes of blackcaps and swifts at the lowest flight speeds at which they
were measured.
They further found that the wake structure results in a relatively high down-
wash behind the body (see Chap. 1), which can be explained by the relatively
active tail in flycatchers. As a result of this, slow-flying flycatchers have a span
efficiency (rather than flap efficiency as in Pennycuick’s power curves; see above)
which is similar to that of the birds in cruising flight and which can be assumed to
be higher than in hovering hummingbirds (Fig. 5.36).
Unlike in hummingbirds, the pied flycatcher has a ‘feathered upstroke’ dur-
ing which they make their wing inactive by retracting it close to the body and by
spreading the primary wing feathers so that air passes between them. Thus, during
the upstroke, the wings of slowly flying flycatchers generated no significant forces
contrary to Norberg (1990) who suggested that the separated primaries were to
increase lift. On the other hand, significantly, Muijres et al.’s (2012) study dem-
onstrates that the body–tail configuration added 23 % to weight support and that,
during the upstroke, the flycatcher tail generates almost the same percentage of
total lift force as for the wing upstroke in a hovering hummingbird. This suggests
that for slow-flying passerines the tail is very important, and that the upstroke can-
not be called inactive, although the wings certainly are, and the tail is apparently
of importance for flight efficiency and possibly manoeuvrability.

5.7.2 Going Nowhere Fast—Hovering

Hovering is a very expensive form of flying (all of the mass flow is due to the
induced velocity) as we see in the power curves described above (Fig. 5.32a). It is
clear that with little forward speed a bird will have to flap hard to stay in position.
210 5 Birds

Fig. 5.36  Pied flycatchers.
Effective angle-of-attack
(mean ± s.e.) of the quarter
chord point behind the wrist,
a and of the tail, b at flight
speeds of 2 (black), 4 (dark
grey) and 7 m s2 (light grey).
The grey bar at the bottom
of each panel indicates the
upstroke part of the wingbeat.
After Muijres et al. (2012)

Some birds such a hawks that scan the ground for prey hover by facing into the
wind, strictly speaking they are not hovering in the true sense (see below) but glid-
ing slowly into the wind so that their airspeed matches the wind speed and their
ground speed is zero (Fig. 5.37).
The more than 325 described hummingbird species make up one of the larg-
est avian families and encompass a remarkable diversity of flight-related morphol-
ogy, behavior and ecology (Altshuler and Dudley 2002 and references therein).
Hummingbirds are restricted in distribution to the New World, where the great-
est variety and number of species occur in South America. All hummingbirds
are small, and many are minute and miniaturization relative to apodiform ances-
tors has been a predominant morphological theme of hummingbird evolution,
and upregulation of metabolic capacity necessarily occurred in concert with a
reduction in body size. Hummingbirds exhibit brilliant, iridescent colours and
5.7  Behavior and Flight in Birds: Horses for Courses 211

Fig. 5.37  A greater kestrel, Falco rupicoloides, holding station (hanging) by gliding slowly into
a head wind. Photo by permission of Clint Ralph

elaborately specialized feathers (usually of the males only) which led the nine-
teenth-century British naturalist John Gould to give many hummingbirds exotic
common names, many of which are still in use—e.g., coquette, fairy, hill star,
wood star, sapphire, topaz, sun gem, and sylph. Another iconic feature of a num-
ber of hummingbirds, is its bill, which is adapted for securing nectar from cer-
tain types of flowers. It may be rather long and always slender—in the thornbills
(Ramphomicron and Chalcostigma), for instance it is quite short, but in the sword-
billed hummingbird (Ensifera ensifera), it is unusually long, contributing more
than half of the bird’s 21-cm length (Greenwalt 1960).
Hummingbirds have compact, strongly muscled bodies and rather long, blade-
like wings that, unlike the wings of other birds, articulate with the body only
from the shoulder joint, the other joints usually fused, which means that the wing
turns upside down during the upstroke, much like the wings of insects (Azuma
2006). They represent extremes of locomotor and metabolic capacity among the
vertebrates. The ability to hover is the most salient behavioural feature of hum-
mingbirds, but flight in this taxon, more generally, involves remarkable abili-
ties to alter flight speed, trajectory and body orientation–to fly not only forward
but also straight up and down, sideways, and backward and to hover in front of
flowers as they obtain nectar and insects from them. The hovering flight of hum-
mingbirds, which can be of long or short duration, serves a different purpose from
forward flight and is necessary for the precise adjustment of their absolute position
with respect to their surroundings. Small size and high control characteristics are
important for good hovering ability (Azuma 2006) (Fig. 5.38).
212 5 Birds

Fig. 5.38  Wing vortex systems in hummingbird. a Vortex cells generated by both wings in hov-
ering flight. b Vortex cells generated by left wing in cruising flight (the tilt angles of the vortex
wake surface is much shallower than that of the stroke plane because the ridges of the vortex
wake have moved down some distance by the time the valleys are completed). Modified after
Azuma (2006)

A dominant theme in hummingbird evolution is progressive invasion of higher-

elevation habitats. To date, montane regions have provided the best understood
context for ecomorphological interpretations of flight in hummingbirds. Flight
at high elevations presents a double challenge: reduced air density demands
higher lift and power output, whereas reduced oxygen availability can constrain
metabolic power input as hypoxia is known to place limits on the hovering per-
formance of some species, although it is difficult to quantify. Yet the highest
diversity of hummingbirds is found along mid-montane Andean slopes, and some
5.7  Behavior and Flight in Birds: Horses for Courses 213

species range to elevations as high as 5,000 m. The challenge to cold regions is

met behaviorally through compensatory changes in wing beat kinematics, particu-
larly in stroke amplitude. In vertical force production wing motions are bilater-
ally symmetrical and an increase in stroke amplitude is the predominant means
of increasing total aerodynamic force output. Over evolutionary time scales, mon-
tane colonization is associated with increases in body mass and relative wing area
(Altshuler and Dudley 2002 and citations therein).
Hummingbirds exhibit a much stronger negative allometry of wingbeat fre-
quency (the larger the bird the lower the frequency) and a correspondingly greater
positive allometry of wing area relative to body mass (Sapir and Dudley and refer-
ences therein). The smallest hummingbirds have extremely rapid wing-beat rates.
For instance in Calliphlox amethystina, one of the tiniest species, the male has a
wing-beat rate of about 80 per second; the female, which is larger, beats her wings
at a rate of about 60 times per second. In larger species such as the giant hum-
mingbird the wingbeat may be as low as 10 per second. The aerodynamic implica-
tions of these allometries, Altshuler and Dudley (2002) state, are unclear although
they suggest that a reduction in wingbeat frequency may mitigate inertial (resist-
ance) power requirements.
Azuma (2006) notes that the aerodynamically consumed power PA is propor-
tional to the product of the wing area and the cube of the tip speed, which is the
wing span times beating frequency
PA α S(bf )3 .
This is again proportional to five-thirds power of the mass of the flying creature
and to the cube of the beating frequency, or (Fig. 5.39)
PA α m5/3 f 3

Fig. 5.39  Wing beat frequencies in flying animals. After Azuma (2006)

214 5 Birds

The relative wing mass of hummingbirds substantially exceeds that of most

insects, and the overall inertial costs of wing oscillation may therefore be substan-
tial (Fig. 5.39). Elastic energy storage of wing inertial energy may reduce or even
eliminate such costs (see Weis-Fogh 1973). Energy saving by elastic mechanisms
was discussed in marine animals earlier and will be discussed further on in the
section on feather microstructure.
Altshuler and Dudley (2002) note that hovering is extremely rare among vol-
ant vertebrates, yet size limits to hovering performance, be they aerodynamic or
energetic in character, remain poorly understood. For instance, why is sustained
hovering of such restricted taxonomic occurrence, and why did it evolve only in
the New World? How exactly did hummingbirds evolve from a fast-flying, swift-
like ancestor? They predict that these questions should produce exciting develop-
ments in hummingbird research and a better understanding of e.g., comparisons
of hummingbird communities across elevational gradients and the costs of flight
change with body size and wing shape. Since then one such recent investigation
with respect to the biomechanics of backward flight in hummingbirds is particu-
larly interesting and will be considered below.
Flight in hummingbirds generally, involves remarkable abilities to alter speed,
trajectory (backward, forward, up and down) and body orientation. Backward
flight is a frequently used transient flight behavior among members of the hum-
mingbird family (Trochilidae) when retreating from flowers although the biome-
chanics with respect to backward flight is as Sapir and Dudley (2012) indicate
hitherto undescribed for this intriguing locomotor mode. Bats (discussed in
Chap.  4) utilize an upstroke at any speed in which the tip of the wing moves
upwards and backwards relative to the body during the upstroke. But if the speed
of the body is low enough, the tip can sometimes even move backward relative to
the still air during the upstroke (called “tip-reversal upstroke”) (Hubel et al. 2010;
Swartz et al. 2012).
The elevated metabolic demands associated with backward movement likely
derive from the relative terrestrial rarity of this locomotor mode. However, Sapir
and Dudley propose that by contrast, such demands may be negligible for hum-
mingbirds for which this aerial behavior occurs frequently. To test this they meas-
ured oxygen uptake rate (Vo2) and flight kinematics of Anna’s hummingbirds
(Calypte anna) within a wind tunnel using respirometry masks and high-speed
videography, respectively, during backward and forward flight (both at an airspeed
of 3 m s–1), and for still-air hovering (Fig. 5.40). They also repeated this for one
bird throughout a range of backward flight speeds
Oxygen depletion relative to the ambient atmospheric level was integrated over
time to yield the total volume of consumed O2. The instantaneous value of Vo2
was calculated (Sapir and Dudley 2012)
 
FIo2− FEo2
V o 2 = VE
1 − FIo2
where VE is the mass flow of gas exiting the mask, FIo2 represents the frac-
tional concentration of O2 entering the mask and FEo2 represents the fractional
5.7  Behavior and Flight in Birds: Horses for Courses 215

Fig. 5.40  a General setup of the wind tunnel in which Anna’s hummingbirds were studied using
respirometry and high-speed videography during backward, forward and still-air flights. b Pho-
tograph of an Anna’s hummingbird during feeding from the respirometry mask. After Sapir and
Dudley (2012)

concentration of O2 exiting the mask. To further validate respirometry measure-

ments, the authors measured the dilution of airflow under different experimental
conditions using a standardized procedure.
Sapir and Dudley’s (2012) findings show that backward flight in humming-
birds is characterized by distinctive kinematic adjustments, some of which are not
simple extrapolations from trends characterizing hovering and forward flight as
Altshuler and Dudley (2002) had previously suggested. The authors found unex-
pectedly that Vo2 in sustained backward flight is similar to that in forward flight
at equivalent airspeed, and is about 20 % lower than hovering Vo2. For a bird that
was measured throughout a range of backward airspeeds up to a speed of 4.5 m
s–1, the power curve resembled that of forward flight at equivalent airspeeds.
216 5 Birds

Backward flight was facilitated by steep body angles coupled with substantial head
flexion, and was also characterized by a higher wing beat frequency, a flat stroke
plane angle relative to horizontal, a high stroke plane angle relative to the longitu-
dinal body axis, a high ratio of maximum:minimum wing positional angle, and a
high upstroke:downstroke duration ratio.
Warrick et al. (2012) described the musculoskeletal system and muscle activ-
ity in hummingbirds including the enlarged supracoracoideus that provides power
for the upstroke when the wings are inverted to produce useful aerodynamic force
for weight support. They used high-speed X-ray videos of the hummingbird wing
skeleton to reveal that most of the inversion of the wing is produced by supina-
tion of the forearm, which inverts the bones (and feathers) of the handwing. In
pigeons that also display a ‘wingtip reversal’, this inversion of the hand wing
has been shown to produce aerodynamic forces that are used in both weight sup-
port and manoeuvring during slow speed flight. However, this long-axis rotation
of the forearm only inverts the primary flight feathers. For most birds, the hand
wing accounts for ~50 % of total wing area. Hummingbirds, by contrast, have
exceptionally long primary flight feathers, which form 75 % or more of the wing
area. Consequently, by inverting their handwing, hummingbirds achieve a more
completely reversed airfoil during upstroke. Although the neuromuscular control
and musculoskeletal dynamics of the hummingbird’s forearm are not completely
understood, the robust bones hint at their ability to deliver this range of motion
under what must be exceptionally large torsional loads (Fig. 5.41).
The same X-ray video recordings revealed another key to hummingbird hover-
ing flight linked to movements of the humerus. The humerus of hummingbirds is
substantially shortened in comparison with that of other birds (except for their close
relatives, the swifts). It is also held nearly perpendicular to the leading edge of the
wing, and is strongly rotated about its long axis during the middle of the upstroke
and downstroke. In this posture, rather that supinating or pronating the wing, the
torque produced by the pectoralis and supracoracoideus about the humeral long-
axis substantially increases the translational velocity and excursion of the wing.
Hummingbirds generate a leading edge vortex (LEV) on the wing for enhanc-
ing lift production at low flight speeds (Warrick et al. 2009). The trailing vortices
in hummingbirds form a double loop (Fig. 5.42). They are concentrated more at
the wing tip than at the wing root because of the marked spanwise change of the
circulation of the wing, and, similarly, the shed vortices are concentrated near the
switching points of the down- and upstrokes (Azuma 2006; Fig. 5.38). Successive
wing beats should build up a stack of vortex rings, one on top of another. The
wake from a hummingbird was suggested would be little different from the wake
below a hovering helicopter, which produces a continuous stream of air rather than
a series of puffs (Alexander 1992).
The result of these subtle but remarkable musculoskeletal adaptations is a
wing-stroke cycle closely matching in form—although not quite in function—that
of hovering insects. While the two half-cycles of many flying insects may achieve
nearly equal amounts of lift, studies of the vortex wakes and airflow near the
wings of hovering hummingbirds show that they are able to aerobically produce
5.7  Behavior and Flight in Birds: Horses for Courses 217

Fig. 5.41  Flight musculature and muscle activity in hummingbirds. Muscle activity in hum-

mingbirds during hovering; shaded areas represent kinematic downstroke in both, a (Anna’s
hummingbirds) and, b (rufous hummingbirds). a Ventral view of the flight muscles, with regional
(i–iii) variation in muscle activity. b Timing of muscle activity with wing movement. a Modified
from Altshuler et al. (2010); b modified from Tobalske et al. (2010). Photo modified after War-
rick et al. (2012)

25–33 % of their total weight support with the upstroke, enabling backward flight
behavior in retreat from flowers (together with other anatomical, physiological,
morphological and behavioral adaptations) and maintain strictly aerial nectari-
vory (Figs. 5.42 and 5.43). These conditions show a striking degree of convergent
evolution between hummingbird and some hexapod (insect) flight styles, i.e., par-
ticularly in their employment of similar kinematics while engaged in backward
flight, for example during station keeping or load lifting (Sapir and Dudley 2012;
Warrick et al. 2009).
218 5 Birds

Fig. 5.42  Hummingbird
hovering aerodynamics.
Flow field, determined by
particle image velocimetry
(PIV), beneath a hovering
hummingbird at the end of
downstroke, (a) and the end
of upstroke, (b) illustrating
the relative strengths of the
momentum jet (large red
arrows high velocity) at the
end of each half-cycle. The
momentum jet produced by
the downstroke is normally
two or more times that
produced by the upstroke.
Photo, permission of Douglas
Warrick after Warrick et al.
(2012)

5.7.3 Silent Flight

Owls have many extraordinary specializations connected with their highly-evolved

predatory behavior. They have evolved several specialisations for sound locali-
sation: e.g., sound-reflecting feathers on the head, asymmetrically arranged ear
flaps and increased nuclei in the auditory pathway. The hunting strategy of owls
depends upon low speed and silent flight in order to be able to locate the prey
mainly by hearing and to avoid being heard early. For this reason, another spe-
cialization of the owl is the fine structure of its feathers. The owl’s feathers are
equipped with special structures that reduce noises of frequencies more than
2 kHz. Thus, flight noise is reduced within the typical hearing spectrum of the
owl’s prey and also within the owl’s own best hearing range. This contrasts with
pigeons, which are commonly known for a noticeable noise production during
flight, for instance a high frequency sound of rubbing feathers or noises generated
by clap and fling (Bachmann et al. 2007 and references therein) (Fig. 5.44).
5.7  Behavior and Flight in Birds: Horses for Courses 219

Fig. 5.43  Diagram showing wing beat cycles in hovering flight and turning manoeuvres in
Anna’s hummingbird. After Warrick et al. (2012)

While there were comprehensive qualitative investigation of morphological and

functional aspects of bird feathers, Bachmann et al. (2007) provide the first quan-
titative morphometric data on the structures that influence the air flow over the
wing. For the owl, the leading edge comb-like serrations, the trailing edge fringes
on each feather and their velvet-like upper surface are additional parameters rel-
evant for aerodynamics that may present explanations for the underlying mecha-
nisms that lead to a reduction of noise (Fig. 5.45).
Specific structures associated with silent flight are seen only in the barn owl,
Tyto alba. Barn owl feathers are in general larger than pigeon feathers indicating a
lower wing load in this bird that would allow slow flight. The asymmetry of several
parameters between the outer and inner vanes was more pronounced in the barn
owl than the pigeon. This suggested a stiffer leading edge of the feathers due to the
rachides in addition to small outer vanes and a pliant and flexible inner vane. Both
parameters influence the formation of a smooth wing surface during gliding flight
or downstroke in flapping flight and help to minimise the flow resistance through
the wing during the upstroke in flapping flight. Barn owl feathers also have less
radiates, longer pennula, and are more porous than pigeon feathers. This suggested
that air could more easily pass from dorsal to ventral and vice versa in the owl
feathers than in the pigeon feathers. The most conspicuous specialisations in the
barn owl are the serrations at the leading edge of the wing, the fringes at the edges
220 5 Birds

Fig. 5.44  The barn owl, Tyto alba, needs to slow down using outstretched wings and high angle
of attack and tail spread; as it brakes it thrusts its feet forward as part of the precisely coordinated
attack. Photo permission of Jordan Ralph

Fig. 5.45  Silent flight in the barn owl, Tyto alba. The figures a–j show special modifications
of the feathers that enable silent flight during the birds attack on a prey. Figure after Bachmann
et al. (2007)
5.7  Behavior and Flight in Birds: Horses for Courses 221

of each feather, and the velvet-like dorsal surface. Although the specialisations in
the barn owl were previously discussed in the context of silent flight (Norberg 1990
and references therein), Bachmann et al. (2007) present the first convincing quanti-
tative data, which they suggest may serve as a basis for testing the influence of each
specific feature on the owl’s feathers on the air flow field and noise production.

5.8 Offsetting the Costs of Bird Flight

Flying is hard work. Normal powered bird flight is energetically the most expen-
sive means of travel among animals. Birds have developed ways to reduce the
energy costs.

5.8.1 Bounding Flight

Probably the most common style of flight in small birds is a form of intermit-
tent flight that consists of flapping phases interrupted by flexed-wing bounds dur-
ing which the wings are held motionless and flexed against the body. Small birds
with rounded, low aspect ratio wings use intermittent bounds, and small birds with
pointed, high-aspect ratio wings use both intermittent bounds and glides in which the
wings are extended (Rayner et al. 2001; Tobalske et al. 2009 and references therein).
Tobalske et al. (2009) elucidate the contributions of the body and tail to lift
and drag during the flexed-wing bound phase by using particle image velocimetry
to measure properties of the wake of the zebra finch (Taeniopygia guttata) flying
at 6–10 m s−1 in a variable speed wind tunnel as well as flow around taxidermi-
cally prepared specimens. Their measurements showed body lift functions during
bounds to support 20 % of the bird’s body weight. This amount of weight support
was slightly higher than the 16 % estimate obtained from measures of whole body
acceleration in zebra finch. These levels of body lift they propose are sufficient to
make flap-bounding an aerodynamically attractive flight strategy compared with
continuous flapping at flight speeds greater than 6 m s−1 and helps to explain the
widespread use of this behavior during flight in small birds up to the size of large
woodpeckers (Tobalske et al. 2009 and references therein).

5.8.2 Soaring

In large flying animals the Reynolds number and the aspect ratio are so large that
the animal deliberately uses its wings to sustain its weight by lift instead of drag.
A wing of large span or high aspect ratio and a streamlined body are all that are
required for realizing long range flight by maximizing CL/CD. In small birds on
222 5 Birds

the other hand, the Reynolds number and the aspect ratio are small, and the drag
specifically caused by the friction force is too large to obtain the required values
for both CL/CD.

5.8.2.1 Mechanisms of Soaring: Gravitational and Wind/Air Currents

Soaring as the basis of a specialized method of food searching is only possible

in areas and at times, where the occurrence of suitable weather conditions can be
relied upon (Pennycuick 1972). Gravitational gliding is one of the basic mecha-
nisms of soaring, which is restricted to birds, although birds must obtain their
initial elevation by means of flapping flight. The second basic mechanism of soar-
ing involves wind or air currents. Soaring requires that air currents meet one of
two conditions: either the air must have a vertical velocity exceeding the rate of
descent in gravitational gliding, or it must have a horizontal velocity that is non-
uniform in time and space. Whereas static soaring depends upon vertical air cur-
rents, dynamic soaring depends upon horizontal air currents.
Vertical air currents for static soaring are produced when wind strikes an obstruc-
tion such as a hill or cliff face and is deflected upward (Fig. 5.46a). The height of
deflection and the vertical velocity of the air are a function of the angle of deflection
and the velocity of the wind. The easiest method of soaring is slope-soaring in which

Fig. 5.46  Soaring flight. a Slope lift. The best lift is found over a smooth slope (left), while verti-
cal cliffs can produce more complicated flow patterns, but sometimes give useable lift when facing
downward (right). b Dust-devil, triggered by solar heating of the ground and rising as a distinct
bubble. c Vortex-ring, triggered from heated ground and rising as a distinct bubble. d Cross-country
soaring by climbing in a thermal, gliding off, and climbing in a new thermal again. V is forward
speed, Vg is gliding speed, and Vs is vertical sink speed. Modified from Norberg (1990)
5.8  Offsetting the Costs of Bird Flight 223

the bird flies into the zone of rising air (‘slope-lift’). If the vertical velocity of the air
equals the descent speed of the bird, the bird remains stationary in height relative to
the ground. If, however, the vertical velocity is greater, the bird rises, and, if less, the
bird falls at a speed equal to the gravitational descent speed minus the air’s vertical
ascent speed. Among birds of prey (Falconiformes), the use of slope-lift for patrol-
ling a hillside in search of prey is very common (Fig. 5.37).
Air may also be deflected upward by the steep face of waves. Medium-sized and
small petrels, which are entirely pelagic (found in the open sea or regions of deep
water) outside of the breeding season, soar on the slopes of waves at sea. Far out to
sea they are even able to do this in zero wind, by gliding along the forward slope of
a wave which is moving relative to the stationary air (Pennycuick 1972) (Fig. 5.47).
A thermal vortex-ring type is formed by the hot air curving outward, downward, and
then around the vortex (Fig. 5.46b). It is doughnut shaped, with the air rising in the low-
pressure centre and cycling outward and downward. Because the thermal area of lift is
roughly circular (rather than linear as in slope lift), soaring birds spiral downward or
upward in the updraft, making corrective manoeuvres to shift the circle into the strong-
est part of the lift; however, because the air rises faster than birds descend, soaring birds
are carried upward, but at a speed less than that of the vortex. When a bird reaches the
top of the thermal, it begins a straight gravitational glide until it reaches the next thermal
vortex. Thus, static soaring in a thermal vortex can be recognized by its alternating flight
pattern of circling and straight gliding (Fig. 5.46d).

Fig. 5.47  Pair of white-chinned petrels, Procellaria aequinoctialis, slope-soaring over a ‘glassy’

sea. Photo by permission of Lloyd Edwards
224 5 Birds

Fig. 5.48  Shy albatross, Thalassarche caute, dynamic soaring. Photo by permission of Lloyd

Edwards

Unlike static soaring, which is done at relatively high altitudes over land,
dynamic soaring is done at low levels and is usually restricted to oceanic areas
(Fig. 5.48). It is one method that does not depend on vertical air movements but
rather dynamic soaring depends upon a steady horizontal sea wind, which is
laminated into layers of different velocities because of the frictional interaction
between the water and the air; the lower layers have the lowest velocity. This
may include extracting pulses of kinetic energy from discontinuities in the wind
flow (‘gusts’), rather than by exploiting a continuous wind gradient (Pennycuick
2002). The flight path of a bird performing dynamic soaring tends to be a series
of inclined loops that are perpendicular to the direction of the wind. A soaring
albatross, for example, will begin its gravitational glide approximately 15 m
above the sea. Because it glides downwind, its velocity is increased both by
descent and by the wind at its tail. As the bird nears the sea, it makes a turn
into the wind, and the forward flight velocity derived from the downwind glide
and the tail wind combine to lift the albatross slowly back to its initial gliding
height, but with a loss of horizontal velocity. The bird therefore turns downwind
again and begins to repeat the soaring cycle all the while using its wings to gain
or lose height dynamically (Fig. 5.49) (see Pennycuick 1972, 1983).
5.8  Offsetting the Costs of Bird Flight 225

Fig. 5.49  Indian yellow-
nosed albatross, Thalassarche
caute. The bird banks steeply
to lose height quickly (see
caption for Fig. 5.20). Photo
by permission of Lloyd
Edwards
226 5 Birds

5.8.2.2 Wing Shapes and Soaring

We saw above in Pennycuick’s U-shaped power curves the metabolic energy costs
of flights at different speeds. Some birds need to travel great distances in search of
food and consequently need to minimize energy expenditure and the added weight
of storing of large body reserves. Vultures, petrels and albatrosses are among such
birds that exhibit adaptations to limit energy expenditures while in flight, most
important being the wing shape (Pennycuick 2002). Wings as we have seen are
frequently designed to give as much lift and as little drag as possible. For example
in a bird wing well-designed for lift, the lift may be as much as 20 times the drag
(Fig. 5.50).
Warham (1977), in his study of wing shapes of 48 procellariiform species
(albatrosses and petrels), noted that with increase in body mass, the ratio of the
humerus:ulna (manus + primaries) varied significantly. He found that the dis-
tal segment forms a major part in the wing of smaller birds such as in the sooty
black petrel, Hydrobates pelagicus (28 g) and conversely, the proximal segment
in larger birds such as in the snowy albatross, Diomedea exulans chionoptera
(mass  = 8,677 g). He suggested that in the case of the petrel, the large flexible
distal wing section contributes to its great maneuverability whereas in the case of
the albatross, the inner wing segments contribute more to the wing area, forming a
stiffer, thicker, wing suited for soaring (also see Chklovski 2014).
Albatrosses and petrels have high-aspect ratio wings that allow them to soar
(usually as slope-soaring; see above) over vast areas of the ocean looking for fish
or squid. Slope soaring holds the bird aloft by the upward air movements formed
as the slope of the ground or the windy side of waves over the ocean deflects air
upwards. Other birds such as the Rüppell’s griffon vulture, Gyps rüppellii, in con-
trast show the typical wing form seen in thermal soaring over land as described
above. We will see below how these different shaped wings function to achieve
roughly the same end results, i.e., energy saving.

Fig. 5.50  Adjustments of aspect ratio and wing area leading to five different wing shapes. Flight
characteristics of a Magnificent Frigatebird, Brown Pelican, Razorbill and Blue-eyed Shag and
flightless penguin compared to the White-chinned Petrel. Figure by permission of Colin Penny-
cuick (1987)
5.8  Offsetting the Costs of Bird Flight 227

Much of our understanding of the gliding flight of birds we owe to the work of
Colin Pennycuick. His knowledge was acquired through elaborate lab-based wind-
tunnel experiments as well as innovative ‘in the field’ observations in which he
used his skills as a glider pilot to follow vultures in his machine on their daily
journeys in search of food. Petrels and albatrosses (Procellariiformes) include spe-
cies covering a wider range of body mass than any other order. In spite of this, the
Procellariiformes are quite a uniform group in many aspects of their biology. As
regards their flight, all are pelagic, coming ashore only to breed, and all depend
for successful breeding on making frequently long foraging excursions to feeding
areas at sea. For example the fulmar petrel, Fulmarus glacialis, slopes-soars along
waves at sea and cliffs at the breeding grounds. It has pointed wings with aspect
ratio about 12. The related albatrosses are larger and have still higher aspect ratios
(about 20 in the wandering albatross, Diomedea exulans; Figs. 5.51, 5.52 and
5.53). Windward ‘pullups’ are suggestive of the classical ‘dynamic soaring’ tech-
nique Pennycuick (2002) observed in large and medium-sized species. However,
the calculated strength of the wind gradient would have been insufficient to main-
tain airspeed to the heights observed, and he concluded that most of the energy for
the pullups must come from kinetic energy, acquired by gliding along a wave in
slope-lift (Pennycuick 1982).

Fig. 5.51  Nine study species shown with constant wing span, depicting systematic change of
aspect ratio with size. WAN wandering albatross Diomedea exulans, BBA black-browed albatross
Diomedea melanophris, GHA grey-headed albatross Diomedea chrysostoma, STY light-mantled
sooty albatross Phoebetria palpebrata, MAC giant petrel Macronectes sp., WCP white-chinned
petrel Procellaria aequinoctialis, CAP cape pigeon Daption capensis, PRN dove prion Pachyp-
tila desolata, WIL Wilson’s petrel Oceanites oceanicus. Figure by permission of Colin Penny-
cuick (1982)
228 5 Birds

Fig. 5.52  Graph compares lift coefficients of different species calculated while they were flying
over the sea. The Wandering albatross had a mean lift coefficient of 1.0 and the Wilson’s petrel
had a lift coefficient of 0.28. This corroborates the relation between low aspect ratio and high
flying speeds and also demonstrates the relationship between lift coefficients and size. Figure by
permission of Colin Pennycuick (1982)

Pennycuick (1987) compared the flight characteristics of the magnificent frigate bird
(Fregata magnificens), brown pelican (Pelecanus occidentalis), Razorbill (Alca torda)
and blue-eyed shag (Phalacrocorax atriceps) to the white-chinned petrel (Procellaria
aequinoctialis). From Fig. 5.50 it can be seen that five configurations are obtained on
increasing or decreasing aspect ratio and wing area in comparison to the petrel.
The variation in mass among the Procellariiformes is striking as is the aspect
ratio, which together influences the modes of flight. The wandering albatross is
the largest in the group, with an aspect ratio of ~15–20 and a wing span of ~3 m
capable of holding aloft a bird weighing about 9 kg. The wandering albatross is
known to soar between 2 and 12 m above the waves and typically glide in still
air at about 12 m per second but faster when slope soaring. The smallest in the
group is the Wilson’s petrel (Oceanites oceanicus) weighing 0.038 kg with an
aspect ratio of 8. The variation in mass is more clearly seen in Fig. 5.51. Aspect
ratio varied with the 0.12 power of mass. These variations essentially separate
5.8  Offsetting the Costs of Bird Flight 229

Fig. 5.53  The wandering albatross, Diomedia exulans, slope-soaring in rising air. A wave can be
seen in the background. Photo by permission of Lloyd Edwards

the larger species that proceed primarily by gliding from the three smallest spe-
cies that proceed primarily by flap-gliding (intermittent flapping and gliding). For
instance, the lower aspect ratio of the Wilson’s Petrel (AR = 8) forces it to pro-
ceed primarily by flapping or flap-gliding. Figure 5.52 compares lift coefficients
of different species calculated while they were flying over the sea. The wandering
albatross had a mean lift coefficient of 1.0 and the Wilson’s petrel had a lift coef-
ficient of 0.28. This corroborates the relation between low aspect ratio and high
flying speeds and also demonstrates the relationship between lift coefficients and
size (Pennycuick 1982).
In some of these birds the apparent greater commitment to gliding went even
further. Pennycuick (1982) showed that there were anatomical specializations in
the albatross, Diomedea, Phoebetria and the giant petrels (Macronectes) in the
form of a ‘shoulder lock’, consisting of a tendon sheet associated with the pecto-
ralis muscle, which restrained the wing from elevation above the horizontal. This
arrangement was not seen in the smaller species and he interpreted it as an adapta-
tion to reduce the energy cost of gliding flight.
Energy is the great price vertebrate animals, and most invertebrates, must pay
for their travel. Seemingly, the idea of travelling at no cost would be no more than
wishful thinking. Yet, this is not so. Albatrosses seem to fly at almost no cost and
can cover huge distances during their foraging trips without flapping their wings.
These long-living birds spend most of their lives in flight over the sea and return
to small oceanic islands only for breeding. As foraging grounds of all albatross
230 5 Birds

species are pelagic, they have to find productive areas repetitively during the
breeding period. Trips of 15,200 km or flights around the world in 46 days have
been reported for wandering albatrosses (Sachs et al. 2012).
In a recent study on the wandering albatross, Sachs et al. (2012) noted that alba-
trosses are able to: “fly thousands of kilometres at no mechanical cost” by using
dynamic soaring and are capable of mean ground speeds higher than 127 km/h,
which they can maintain for more than 8 h. Assuming a maximum lift-to-drag
ratio of 20 and 8.5 kg weight, an albatross has to develop a power of 81.0 W for
flying at 70 km/h. Thus, substantial energy is needed to keep a bird flying and to
replace substantial weight loss during flight by feeding. Their study distinguishes
between the large-scale movement that appears as a steady-state cruise of long-
distance travel that are well documented and the small-scale movements, i.e., flight
manoeuvres involving dynamic soaring of the order of tens to hundreds of metres,
which have not previously been experimentally investigated. In this context, until
now, the physical mechanisms of the energy gain in terms of the energy transfer
from the wind to the bird were mostly unknown. The authors’ findings showed that
the energy gain is achieved by a dynamic flight manoeuvre consisting of a continu-
ally repeated up-down curve with optimal adjustment to the wind. While this form
of manoeuvering is known, they, however, were able quantify the energy obtained
from the wind by analysing the measured trajectories of free flying birds using a
new GPS-signal tracking method yielding high precision (Figs. 5.54 and 5.55).

5.8.2.3 Wing-Tip Shapes and Soaring: Seabirds Versus Vultures

We looked at the mechanics of wingtip designs in Chap. 1. Here, we will briefly

mention how wing tip shapes affect different types of soaring birds (Fig. 5.56).
The magnificent frigate bird (Fregata magnificens) simply achieves this by having
the longest and narrowest wings that terminate in pointed wing tips. Of the three
birds in the figure it has the largest wing span (2.29 m) and highest aspect ratio.
The black vulture (Coragyps atratus), on the other hand has the smallest wing span
(Pennycuick 1983). However, unlike in the Procellariiform study (Fig. 5.56) the
black vulture lift coefficients do not vary as drastically (Table 5.1). This is in part
due to smaller variations in mass and also due to the presence of emarginated wing
tips on the brown pelican (Pelecanus occidentalis) and black vulture. This emar-
gination compensates for the lower aspect ratio.
Earlier, we referred to the two different soaring strategies as reflected by the
areas of the wings, that of the wandering albatross and the Ruppell’s griffon vul-
ture. Wandering albatrosses averaging 8.7 kg mass had 0.61 m2 wings, giving a
wing loading of 140 N/m2. As a general rule we can say that the higher the aspect
ratio the better the aerodynamic performance of a wing (Figs. 5.51 and 5.52). As
expected, vultures have much higher wing loadings than albatrosses of the same
weight. For example Ruppell’s griffon vultures averaging 7.6 kg mass (74 newtons
weight) had an average wing area of 0.83 m, making the wing loading 90 N/m2
(Alexander 1992). The implications are of different soaring strategies in seabirds
and vultures, which we will look at next.
5.8  Offsetting the Costs of Bird Flight 231

Fig. 5.54  Large- and small-scale movements and dynamic soaring cycle. a Large-scale move-
ment. The 4,850 km path (projected to the sea surface) of a long-distance flight of a wandering
albatross is shown. Logging stopped after the first 6.0 days of this 30-day-long foraging trip.
b Small-scale movements. A 14 min portion of the long-distance flight from Fig. 5.1a shows a
sequence of three connected parts. The flight path consists entirely of winding and curving seg-
ments, not exhibiting any straight horizontal sections. c Dynamic soaring cycle. The small-scale
movements consisted of dynamics soaring cycles featuring distinct motions in the longitudinal,
lateral, and vertical directions. Each dynamic soaring cycle consists of 1 a windward climb, 2 a
curve from wind- to leeward at the upper altitude, 3 a leeward descent and 4 a curve from lee- to
windward at low altitude, close to the sea surface. Figure after Sachs et al. (2012). PloS One
open access. doi:10.1371/journal.pone.0041449.g001
232 5 Birds

Fig. 5.55  Relationship between energy gain, altitude and wind gradient. The left and right dia-
grams show the relationship between the shear wind layer above the sea surface and the altitude
region where the energy gain from the wind is achieved (during the dynamic soaring cycles). On
the left diagram, the energy gain phase is indicated by grey shading. This corresponds with the
phase between the minimum and maximum of the total energy. The right diagram shows the wind
speed (dashed line) and the wind gradient (solid line) as functions of altitude. The wind speed at
10 m altitude was determined to yield VW10 = 11.3 m/s. The shear wind profile, dVW /dh, is based
on a logarithmic wind model. The altitude region where the energy gain is achieved is indicated
by horizontal dashed lines which establish a link between the left and right diagrams. At small
altitudes, large changes in the wind speed occur, resulting in a high wind gradient. As the altitude
increases, the changes in the wind speed continually decrease to become very small in the altitude
region where the energy gain is achieved. As a result, the wind gradient is very weak at this stage.
Sachs et al. (2012 and references therein). Figure after Sachs et al. (2012; see their text for further
details). PloS One open access. doi:10.1371/journal.pone.0041449.g005

5.8.2.4 Do Seabirds Have the Edge on Vultures?

Simple theory suggests that vultures would fly better if they had longer, possi-
bly narrower wings (Alexander 1992). So, why adopt different wing shapes? The
answer put simply is a matter of habitat. The black vulture is most suited to land
soaring and maneuvering through crowded environments. If a relatively large vul-
ture were to be given an albatross-like aspect ratio without reducing its wing area,
the wing span would have to be considerably increased compared to the span of
an albatross of similar mass. The disadvantage to seabirds is if they had to take
off from horizontal surfaces like vultures and pelicans (see below), but because of
their lifestyle of open spaces and cliff-tops (enabling take-offs from high points),
they do not have to make drastic compromises between optimum flight character-
istics and suitable landing and take-off requirements.
Nevertheless, land soaring birds such as eagles, vultures and buzzards have to
save energy too. As mentioned above, because they live in cluttered environments
with trees and other obstacles, vultures and pelicans, e.g., require short, steep take-
offs (Pennycuick 1972, 1983) and therefore low aspect ratio wings. Rather as we
discussed, they have developed a somewhat different trick for saving energy—they
are able to exploit thermals and air currents and thus require large lifting surfaces
with low induced drag. This constraint requires that their wings be shorter than the
5.8  Offsetting the Costs of Bird Flight 233

Fig. 5.56  Aspect ratio and wing tip effects in soaring in Sea birds and Land birds. Silhouettes
from photographs of Fregata magnificens, Pelecanus occidentalis and Coragyps atratus. Figure
by permission of Colin Pennycuick (1983)

Table 5.1  Comparison of flight performance between three soaring species. Table permission of

Colin Pennycuick (1983)
Frigate bird Brown pelican Black
vulture
Wing spam (m) 2.29 2.1 1.38
Aspect ratio 12.8 9.8 5.8
Wing loding (N/m2) 36.5 57.8 54.7
CL 1.33 1.45 1.35
Cirding radius (m) 12 18 17

optimum soaring size seen in sea birds. The compromise evolved is emarginated
wing tips that effectively reduce the induced drag (Tucker 1993), while allowing
shorter, broader wings (see Chap. 1). These highly contrasting wing types having
a common goal of saving energy and underscore an important point—birds are
not pure flying machines. They are living, multiplying creatures that need to fulfill
many other functions, among which is living in varied habitats. As we saw above,
large seabirds, such as albatrosses, perform low cost ‘dynamic soaring flight’
(maintain or gain airspeed) by making use of the energy in vertical wind shears,
i.e., the differences in horizontal wind speed according to the altitude above the
waves (Pennycuick 2002). Because this technique cannot generally be used above
234 5 Birds

land, large terrestrial birds like raptors or storks gain altitude by circling inside
ascending thermal air currents or using orographic uplift (using changes in the
earth’s surface e.g. cliffs and mountains) (Fig. 5.46a, d).
Perhaps one vulture that demonstrates a shift to a higher aspect ratio wing is
the Cape bearded vulture, Gypaetus barbatus, that appears to be a bird in transi-
tion, from old world vultures to new world eagles (Alan Feduccia personal com-
munication, 2014; also Sinclair and Hockey 2005), a distinction that is evident in
Figs. 5.57 and 5.58 (also Frontispiece) when compared with the more typical Cape

Fig. 5.57  Cape vulture, Gyps caprotheres, (top) and Cape bearded vulture, Gypaetus barbatus
(bottom) showing apparent differences in the aspect ratio of the wings. Photo permission of Clint
Ralph
5.8  Offsetting the Costs of Bird Flight 235

Fig. 5.58  Three stages of flapping flight cycle of the Cape bearded vulture, Gypaetus barbatus.
Photo permission of Clint Ralph
236 5 Birds

vulture, Gyps caprotheres. Furthermore, the habitat of the Cape bearded vulture is
also not typical compared to other vultures and more similar to new world eagles.
It prefers nesting and breeding in remote, high mountains, usually above 2,000 m
(like large seabirds) rather than savannah and wooded areas in which shorter
broader wings are more effective. The Cape bearded vulture in South Africa is con-
fined to the Drakensberg and nests on the cliff ledges (Sinclair and Hockey 2005).
Vultures have evolved the most extreme use of soaring-gliding flight. As an
illustration, the record of altitude attained by a bird belongs to a Rüppell’s vul-
ture, Gyps rüppellii, that collided with an airplane at 11,000 m was documented
by Duriez and colleagues (2014). It is thus understandable that this species has
become the focus of studies on soaring-gliding flight. From an ecological perspec-
tive, being obligatory scavengers, vultures evolved an extremely opportunistic life-
style to cope with food resource unpredictable in time and space. Vultures face a
trade-off as they need to travel great distances in search of food while minimizing
energy expenditure and storing large body reserves. This leads to the prediction
that they will exhibit adaptations to limit energy expenditures while in flight.
Duriez et al. (2014) reported the first measurements of heart rate (HR) derived
from electrocardiogram, i.e., offering unparalleled precision in heart rate recording,
together with high-resolution flight behavior (using GPS and accelerometer) in two
species of free flying vultures specialized for prolonged gliding flight: the Eurasian
griffon vulture, Gyps fulvus, and the Himalayan griffon vulture, G. himalayen-
sis—trained for freely-flying. HR increased three-fold at take-off (characterized by
prolonged flapping flight) and landing (>300 beats-per-minute, (bpm)) compared
to baseline levels (80–100 bpm). However, within 10 min after the initial flapping
phase, HR in soaring/gliding flight dropped to values similar to baseline levels in
both species, i.e., slightly lower than theoretically expected. The striking result was
the amplitude and speed of the changes in HR; it took only a few minutes for vulture
HRs to stabilize after flapping ceased. This was unexpected given that HRs of other
soaring birds like the wandering albatrosses, which glides over the sea, the HR of
these birds can take up to two hours to return to baseline levels. Other observations
with respect to heart rate in flight showed that weather conditions influenced flight
performance and HR was noticeably higher during cloudy compared to sunny condi-
tions when prolonged soaring flight is made easier by thermal ascending air currents.
Among the significant findings was the very low HR values, presumably reflecting
the low energy cost of soaring and gliding flight in vultures, comparable to perching
birds. Based on heart rate and metabolic rate Duriez and colleagues calculated that
soaring and gliding vultures may use a similar amount of energy as when perched
and 2–3 times less energy than when flapping or walking comparing with similar
results reported for albatrosses that use dynamic soaring flight (Pennycuick 2002)
but differing in some species that alternate soaring and gliding flights in short bouts,
like Cape gannets, Morus capensis (Figs. 5.28, 5.30), where HR during gliding
phases is only reduced by 20 % compared to that during flapping phases. The energy
gains from soaring in vultures the authors suggest must be off-set by the high costs
of taking-off and landing as well as walking (involving alternation of short walks,
runs, jumps and fights, as well as competing for a carcass given that they feed in
5.8  Offsetting the Costs of Bird Flight 237

groups. Importantly the findings suggest that the increase in energetic costs associ-
ated with flight with distance covered, as commonly assumed for soaring birds like
vultures may be very limited, since they found that vultures expend nearly negligible
greater amounts of energy when flying than when perching (Duriez et al. 2014 and
references therein).

5.8.3 Flying in Formation

5.8.3.1 The V Formation of Bird Flocks

It has been known for some time that birds get some form of energy saving when
flying in V formation (Fig. 5.59). The primary empirical evidence confirming that
this mechanism is used in energy saving is a reduction in heart rate and wing-beat
frequency in pelicans flying in a V formation. In a recent paper, Portugal et al.
(2014) noted that precise aerodynamic interactions showing that birds exploit
upwash capture from the bird in front had not been identified. To investigate the
purported aerodynamic interactions of V formation flight, they studied a free-fly-
ing flock of hand-reared northern bald ibises (Fig. 5.60), a critically endangered
migratory species, using new technology to measure the position, speed and head-
ing of all birds in a V formation.
The team were able to show that a bird flying in the upwash of another bird
needs to generate less lift in order to stay in the air, and, consequently, experiences

Fig. 5.59  Formation flying in the yellow-billed duck, Anas undulata. Even soon after take-off
there is a clear leader. Photo permission of Clint Ralph
238 5 Birds

Fig. 5.60  V formation flight

in migrating ibises. Northern
bald ibises, G. eremita, flying
in V formation during a
human-led migratory flight
(photograph M. Unsöld).
Permission of Portugal et al.
(2014), courtesy Macmillan
Press Ltd

less induced drag. The 14 ibises did manage it for long enough for the scientists to
accurately record both the distance between each bird and the timing of their wing
flaps. Each bird was able to synchronize the flapping of its wings so that it could
exploit the upwash created by the swirling vortex of air from the flapping wingtip
of the bird in front by delaying its wingbeat by just enough to that of the bird in
front to gain from its upwash rather than get caught in the downwash. The findings
show a form of precise coordination between the birds that previously would have
been considered too complex to even anticipate (Portugal et al. 2014 and refer-
ences therein) (see section above on bird brains).

5.8.3.2 Variable Shape of Flocks of Birds

The beautiful coordination in flocks of birds has raised interest for ages in both
laymen and scientists. Amazing in this respect are the aerial displays of huge
flocks of starlings (Sturnus vulgaris) at dawn or dusk. Flocks of birds have great
variation in shape: often different flocks have different shapes and a single flock
changes its shape over time. Extreme changes in shape and density of flocks occur
during the aerial displays of thousands of starlings. For instance, sometimes dur-
ing turning the flock may change in relative proportions, density and volume,
whereas at other times the shape of a flock may remain intact while only changing
its orientation relative to the movement direction. Further, during turning individu-
als may reposition their location within a flock in an amazingly precise way while
travelling at great speed (Hemelrijk and Hildenbrandt 2011).
Hemelrijk and Hildenbrandt show that local variability of behavior in a group
generally leads to more variable flock-shape, but not in cases of local variability
of speed. Instead, high variability of speed results in an oblong shape that is per-
manently oriented in the movement direction. Remarkably, a lower variability of
5.8  Offsetting the Costs of Bird Flight 239

speed, thus, stronger synchronisation in a flock, leads to a variable orientation of

the longest dimension of the shape relative to the movement direction.
The authors show via a model (StarDisplay) that patterns of flocking have been
shown to resemble remarkably those of huge flocks of real starlings when flying
above the roost. They include the following features:
(1) that group size has a great impact on the variability of shape;
(2) A higher number of interaction partners in their model decreases the varia-
bility of flock shape as a consequence of the greater synchronisation of the
flock-members;
(3) Turning has a big impact on the variability of shape;
(4) Change of shape during turning and repositioning of individuals are a conse-
quence of low variability of speed;
(5) This theory implies that the group shape becomes more oblong due to fre-
quent slowing down by its members in order to avoid collisions (as in fish
schools; see Chap. 1).
As an introduction to the next section, I mentioned in Volume 1, it is probably no
exaggeration to say that without β-keratin, birds would never have left the ground and
not be anything like the species we know today. We would have been deprived of one
of the great wonders of nature as glimpsed in the foregoing sections. In the last sec-
tion we will look at how β-keratin became the crucial material in the story of birds.

5.9 How β-Keratin Crucially Influenced Bird Evolution

5.9.1 Feather Structure at Angstrom and Molecular Levels

In the past 30–40 years, there have been many advances in our knowledge of the
microfibrillar, molecular and developmental structure of feather β-keratin (Filshie
and Rogers 1962; Alibardi and Toni 2008; Fraser and Parry 2008, 2011). Filshie
and Rogers (1962) showed after treating feather β-keratin with lead staining that
it was composed of fine microfibrils approximately 30 angstrom (Å) in diameter,
which were apparently embedded in a matrix. At the molecular level, β-keratin is
a natural polymer consisting of long protein fibers surrounded by an amorphous
protein matrix (Fraser and Parry 2008, 2011). The pioneering X-ray studies of
Astbury and coworkers (Astbury and Marwick 1932; Rudall 1947) indicate that
the conformation of the polypeptide chain in the hard keratins of birds and rep-
tiles is based on the β-pleated-sheet (the β-form) rather than the coiled-coil α-helix
(α-form) found in mammalian keratins. Avian feathers have a filament–matrix
texture and X-ray diffraction studies show that the filament has a helical structure
with four repeating units per turn. Each repeating unit consists of a pair of twisted
β-sheets related by a perpendicular diad, and the twist in the sheets is of opposite
hand to that of the helix. Each sheet is believed to comprise a 32-residue segment
of the feather keratin molecule, which contains around 100 residues, the remainder
240 5 Birds

Fig. 5.61  A model for the repeating unit of the framework of the feather keratin filament derived
from the X-ray diffraction pattern (Fraser et al. 1971, reference in Fraser and Parry (2008)). a A
four chain by eight-residue segment of an infinite antiparallel chain pleated β-sheet. The residues
are represented by spheres of electron density centered around the αC atoms. b The repeating
unit is derived from a pair of segments related by a perpendicular diad. c The segments are not
flat as in b but twisted as shown in a right-handed fashion. The repeating units are arranged on
a left-handed helix of pitch length of ~9.5 nm with four pairs of molecules per turn. The various
parameters required to define the model were optimized on the basis of the measured X-ray data
and are listed in the original publication. After Fraser and Parry (2008)

constituting the matrix (Fig. 5.61). Fraser and Parry (2008) collected amino acid
sequences from a range of avian and reptilian keratins from which they identified
a 32-residue segment corresponding to the filament framework, in every case, sup-
porting the notion that there is a common plan for the filament framework in all of
these materials.
In polymers the tensile or bending properties are dominated by the fibers while
the torsional properties are dominated by the compliant matrix (Lakes et al. 1999).
A number of significant mechanical studies by Julian Vincent and colleagues (e.g.,
Purslow and Vincent 1978) and Bonser and colleagues (e.g., Bonser and Purslow
1995) provided valuable data on the tensile properties of the rachis and medulla of
the feather over the years.
The effect of combining soft proteins with stiff minerals in biological materials
to achieve specific combinations of stiffness, strength and toughness was charted by
Wegst and Ashby (2004) in a selection of natural ceramics, biopolymers and their
composites. The mechanical properties of fiber-based composites (artificial and nat-
ural) depend on many variables such as fiber types, orientations, and general archi-
tecture. One such biological material is β-keratin, of which feathers are comprised.
Natural polymers and polymer composites include cellulose, chitin, silk, cuti-
cle, collagen, keratin and tendon, which all have densities of around 1.2 Mg m−3.
Their moduli and tensile strengths are larger than those of engineering polymers:
cellulose fibrils, for instance, have moduli of about 50–130 GPa (the pascal is a
measure of pressure, defined as one newton per square metre) and a strength
of 1 GPa, and silks have moduli of 2–20 GPa and strengths of 0.3–2.0 GPa. Of
5.9 How β-Keratin Crucially Influenced Bird Evolution 241

man-made polymers only Kevlar has a higher stiffness of 200 GPa and strength
up to 4 GPa, which it achieves, as do natural fibers, through its highly oriented
molecular structure (Ashby et al. 1995).
Feathers as we see are composed of a polymer of β-keratin that is well up
with other natural polymers (Wegst and Ashby 2004). Feathers do not have to be
especially strong but they do need to be stiff and at the same time resilient and to
have a high work of fracture (Gordon 1978), which until recent studies (Lingham-
Soliar et al. 2010; Lingham-Soliar and Murugan 2013) were very much a mystery
on how this was achieved at the microstructural level. The latter studies allow an
entirely new biostructural and biomechanical understanding of the feather and for
this reason they are more or less singled out in the following sections, bearing in
mind that they rest on the shoulders of a number of earlier important findings, of
which only a small selection have been mentioned above.

5.9.2 Feather Microstructure—Fibers and Foam

Feathers are the most complex derivatives of the integument to be found in any
vertebrate animal. They are constructed of compact β-keratin, the keratin of rep-
tiles and birds (sauropsids), a light rigid material (Alibardi and Toni 2008). The
demands on the feather connected with flight are extraordinary—its qualities are
almost paradoxical, having to be exceedingly light (or the bird would never leave
the ground) and at the same time exceedingly tough to cope with the stresses of
flight in which accelerations may reach extremely high g-forces (Clark 2009). The
cortex of the feather rachis comprises the bulk of the materials of the rachis and
has been shown to account for most of its tensile strength (Purslow and Vincent
1978; Bonser and Purslow 1995).
Several years ago I hypothesized that the mechanical structural organization of
the rachis was hierarchical and predicted that higher levels of fiber organization
were obscured by the tight polymer matrix surrounding the β-keratin fibers. Hence
it was necessary to circumvent the limits of conventional structure-determination
methods by ‘inventing’ a novel system employing a microbial fauna (fungi, natu-
ral to feathers) to selectively biodegrade the matrix and thus delineate the hypoth-
esized thicker bundles of keratin filaments. The investigations and findings were
recorded in Proceedings of the Royal Society (Lingham-Soliar et al. 2010; also see
details on methods etc. in the “Supplementary Information”).
Following the SEM examinations, the fungi were identified by rRNA sequence
analysis as Alternaria arborescens, A. citri, A. alternata and A. tenuissima
(Lingham-Soliar et al. 2010). The significant result was the delineation of a major
new structural fiber hierarchy of the feather rachis, a magnitude greater than any
other keratin fiber-type previously known (in α-keratin they are 0.5 µm thick
(McKinnon 2006) and in β-keratin till then several magnitudes smaller). The newly
revealed fibers were cylindrical and enormous at 6–8 µm in diameter (cf. 30 Å, as
revealed by Filshie and Rogers (1962)), elongated proximo-distally and interrupted
242 5 Birds

Fig. 5.62  SEM of fibers (syncytial barbules) in the cortex of feather rachis of Gallus gallus
exposed after fungal biodegradation (delineation) of matrix (resin embedded and etched). All fib-
ers show regularly spaced syncitial nodes that extend in the proximo-distal direction of the rachis
(vertical arrow on the right). The syncitial nodes show variations in morphology, terminating in
hooks (arrow) or a ring (arrowhead), while others are intermediate between the two. Fibers are
densely packed through the cortex (curved arrow) and indicate that the nodes are staggered in
arrangement in two- and three-dimensional planes. Circled higher magnification. After Lingham-
Soliar et al. (2010) by courtesy of the Royal Society, London

by regularly-spaced nodes along the filament—characters strikingly identifiable

point-by-point with syncytial barbules, previously only known in the free bar-
bules of downy and embryonic feathers (Chandler 1916; Lucas and Stettenheim
1972; Stettenheim 2000) (Figs. 5.62 and 5.63). Thus, these fibers of the rachis are
referred to as syncitial barbule cells or fibers.
Figure 5.64, particularly because it represents a section only partially degraded
by fungi, helps demonstrate visually the cement-like bond between the polymer
matrix and fibers, and the enormity of the problem of delineation accounting
for why conventional histological methods were unsuccessful in distinguishing
anything but the finest fibrils (comprising the syncitial barbule cells). The find-
ings (Lingham-Soliar et al. 2010) refute a previous contradictory claim that the
β-keratogenic tissue of the rachis and barbs was fully characterized ultrastructur-
ally by histodifferentiation, i.e., that the bulk of the rachis, calamus, and barb rami
were comprised of typical, tile-like, stratified squamous epithelial tissues (Alibardi
and Toni 2008; Maderson et al. 2009).
Syncytial barbules cells (hierarchically the largest structural bundling of fibers
in the rachis), comprise the entire cortex in two distinctive zonal layers, a deep
inner layer oriented longitudinally with the rachis, comprising ~80–85 % and
above which is a zone of circumferentially oriented syncytial barbules ~15 % of
the cortical depth (Lingham-Soliar et al. 2010) (Fig. 5.64). The biomechanical
5.9 How β-Keratin Crucially Influenced Bird Evolution 243

Fig. 5.63  Syncytial barbules in the bound state (within rachis cortex) and the free state (e.g., at
the base of plumulaceous feathers). a Native (non-fungal-biodegraded) syncytial barbules in the
feather rachis of Falco tinnunculus. b Free syncytial barbules (similar to rachidial cortex fibers
in a) from the downy part of a pennaceous feather of Falco peregrinus. Arrows show both ringed
and hooked terminations of the syncitial nodes. Inset shows the megafibrils of the syncytial bar-
bules. After Lingham-Soliar et al. (2010), courtesy of the Royal Society, London

Fig. 5.64  SEM. Feather rachis of Gallus gallus (fungal matrix delineated; resin embedded and
etched). Circumferential fibers (syncytial barbules), identical to the longitudinal fibers (below
in figure), wound round the outer circumference of the rachidial cortex. The matrix is partially
degraded and shows the honeycomb-like structure in which the fibers are embedded in life (top
centre). The fibers are analogous to steel rebars in concrete (see text). Long arrow long axis of
rachis. Scale bar  = 10 µm. After Lingham-Soliar et al. (2010), courtesy of the Royal Society,
London
244 5 Birds

significance will be discussed later. The microbial biodegradation methods used

above to delineate the fiber structure of the rachis paved the way for another study
on feather microstructure which will be described next.
Birds groom and repair their feathers regularly because it is vital to maintain-
ing efficient aerodynamic surfaces. The process of nibbling or ‘‘zipping’’ the barbs
together by means of minute hook-like barbules at their ends involves considerable
lateral flexibility (proximo-distal movement of the barb in relation to the rachis’
long axis). The thin cross-sectional structure of the lateral walls of the barbs and
rachides, to which the barbules and barbs are attached respectively, compared to
the much thicker dorsal and ventral walls of both barbs and rachides, occurred to
me to be significant for allowing lateral flexibility and maintaining vertical sta-
bility. It was this attachment of the barbs to the lateral walls of the rachis, given
they were much thinner, that prompted my hypothesis that the lateral walls of the
barbs and rachides may have been comprised of a more ductile surface comprising
crossed fibers as a response to shear and torsional stresses. Our knowledge at the
time was that the lateral walls of the rachis and barbs were constructed in exactly
the same way as the dorsal and ventral walls, i.e., comprising of longitudinal fib-
ers, and that these walls differed only in being much thinner.
The lateral walls of the rachis and barbs of numerous feathers in a number of
bird species were investigated using the fungal delineation process (adapted with
respect to the infection process; Lingham-Soliar and Murugan (2013), also SI data).
The findings proved to be significant. Again, given that fungal selective delineation
is a relatively new method of investigation, all findings here, as in the previous study
(Lingham-Soliar et al. 2010), were supported by conventional histological meth-
ods. I had mentioned earlier the problems with respect to conventional dissections
of ‘fresh’ feathers. However, despite these difficulties, now we had the hindsight
knowledge of knowing what to look for and to persevere until they were found.
Importantly, the cortex of the feather barb, despite being considerably thin-
ner than that of the rachis, was also found to be comprised of syncytial barbules
(Lingham-Soliar and Murugan 2013), here again contradicting the thesis that the
cortex of the rachis and barbs was comprised of tile-like, stratified squamous epi-
thelial tissues (Alibardi and Toni 2008; Maderson et al. 2009). In the barbs, how-
ever, the syncitial barbule cells are oriented solely along the long axis. Undoubtedly
though, the most significant part of the results of this study was the discovery of
an entirely new structural organization of β-keratin fibers as revealed by the fun-
gal matrix degradation—the lateral walls of the rachis and barbs comprised alter-
nate layers of oppositely oriented fibers approximately 45° to the long axis of the
barbs and rachides (Figs. 5.65, 5.66 and 5.67). While this crossed-helical array
of β-keratin fibers dominates the structure of the lateral walls of the barbs, a few
superficial layers of fibers, near the boundary with the cortex, extend parallel to the
rachidial long axis and overlie the crossed-fiber layers (Fig. 5.67a, top).
This new structural architecture of cross fibers occupies the entire area of the
lateral walls of the rachis and barbs. A complete cross-sectional dissection of the
lateral rachidial wall of a native flight feather of Falco peregrinus includes the
superficial cuticle and shows the entire cross-fiber architecture of approximately
5.9 How β-Keratin Crucially Influenced Bird Evolution 245

Fig. 5.65  SEM of feathers (fungal matrix delineated). Rachis epicortex. Gallus gallus. a

Dorso-lateral view of the boundary between cortex and epicortex of the rachis showing cross-
fiber structure. Arrows show the boundary where the cortex overlaps the epicortex, with a
degraded area between arrows showing underlying epicortex with cross-fibers. Fungi can be
seen at bottom of image. b Cross-fiber system in epicortex further down the section. c Shows
a tangential surface of the epicortex just above the medullary pith cells, which are impressed
upon the layer. Modified from Lingham-Soliar and Murugan (2013) PloS One; doi:10.1371/
journal.pone.0065849.g001

16 two-ply layers (Fig. 5.66b; see Lingham-Soliar and Murugan (2013) for high
resolution photos). Given this novel structure of the lateral walls of the rachides
and barbs, i.e., a geodesic organization of alternating oppositely oriented fibers
in multiple layers compared to the predominantly longitudinal fibers of dorsal
and ventral walls (cortex), the lateral walls were named the epicortex (meaning,
around or near the cortex).
In addition to the longitudinal sections described so far (Figs. 5.62 and 5.63a),
cross-sections of fungal delineated cortices of the rachis (Fig. 5.68) were also made
(also see Lingham-Soliar 2014a, SI figures). Two partial cross-sections were shown
for the first time (Lingham-Soliar 2014a) (Fig. 5.68) at two different points along the
rachis, one at an undamaged section and the other at precisely where it is seriously
buckled. In the buckled cross-section (Fig. 5.68b), some of the syncitial barbule fib-
ers seen in transverse view are compressed, whereas they are more or less undis-
torted in the undamaged section (Fig. 5.68a; see biomechanical section below).
Also found in the rachidial cortex was a superficial layer of syncytial barbules a
few cells deep and longitudinally oriented that adds to the data reported in the previous
study (Lingham-Soliar et al. 2010). They overlie the circumferential fibers described
above, probably for aerodynamic streamlining, i.e., to present a relatively smooth sur-
face as opposed to transversally oriented fibers at the surface. The significance of the
feather microstructural fiber architectures of the two studies (Lingham-Soliar et al.
2010; Lingham-Soliar and Murugan 2013) enabled a new model, which will be dis-
cussed from a functional perspective below (Lingham-Soliar 2014a) (Fig. 5.69).
246 5 Birds

Fig. 5.66  SEM of feathers of Gallus gallus and Falco peregrinus. a Gallus gallus. Fungal
degraded. Rachis epicortex between successive barbs. Patches of cuticular microvilli (middle,
right) indicates section is at the surface. Successive layers of cross-fibers form a meshwork. The
rippling effect represents fiber loss of tension (possibly from wear) nearest surface (see text;
left to right = long axis of rachis). Lower inset rectangle shows two geodesic cross-fiber layers
from a section in which fibers are under tension (straight). b Falco peregrinus. Native (nonbio-
degraded). Rachis epicortex adjacent to barb. Transverse section of entire depth of epicortex, cut
at acute angle, shows numerous fiber layers as they naturally occur with matrix intact. Section
shows approximately 16 layers, each comprised of a two-ply of oppositely oriented fibers (see
rectangle). Top left shows epicortex surface with villus cuticle intact while bottom right tapers
sharply to near tangential plane to union with barb. After Lingham-Soliar and Murugan (2013),
PloS One open access. doi:10.1371/journal.pone.0065849.g002
5.9 How β-Keratin Crucially Influenced Bird Evolution 247

Fig. 5.67  SEMs of cross-fiber architecture of epicortex of barbs and rachis (a–c, e are fungal
delineated), d is native (non-biodegraded). a, b Gallus gallus. Several alternating layers of oppo-
sitely oriented fibers of the barbs just below barbules. Arrow show long axis of barb. c Gallus
gallus, two geodesic cross-fiber layers from a section of the rachis in which fibers are under ten-
sion (straight). d Bubo africanus, native barb epicortex tangentially dissected to show 3 fiber lay-
ers. e Gallus gallus, alternating cross-fiber structure of epicortex in section of barb just above a
barbule and below the cortex. Fungus in bottom right corner shows papulose apical tip of hypha.
After Lingham-Soliar (2014a), courtesy of Journal of Ornithology, Springer

5.9.3 Feather Biomechanics at the Microstructural Level

The biomechanics of the β-keratin fiber structure of feathers with particular refer-
ence to the syncitial barbule and crossed-fiber structure of the rachis and barbs are
discussed with particular reference to: (1) Crack-stopping, (2) stiffness, ductility
and buckling, (3) torsion and (4) ductile tearing (for related physics and mechanics
see Chap. 1).
248 5 Birds

Fig.  5.68  Cross-sections of rachis showing syncitial barbule cells (fungal delineated). a

Unstressed rachis. The diameters of the syncitial barbule cells vary depending on whether they
are transected closer to the nodes or further away and because of staggering of the syncitial bar-
bule cells, as defined by the nodes (arrows), along the long axis of the rachis. Diameters, cut
closest to the centre of the nodes, are largest and hexagonal shaped (lower arrow). b Buckled
rachis. Some of the syncitial barbule cells are considerably flattened (squashed) transversely
(black arrows). Two syncitial barbule cell nodes (white arrows) are identifiable despite being
transected nearer the node base rather than close to its centre. Lingham-Soliar (2014a), courtesy
of Journal of Ornithology, Springer

5.9.3.1 Crack-Stopping

In the feather, the position of the rachis at the quarter-chord position is designed
to minimize the forces associated with coupled bending and torsion. Such forces
mean that the composition of the rachis must be able to resist fracture, specifi-
cally the propagation of a crack (see Chap. 1). From a physicochemical perspec-
tive, β-keratin is among natural materials that have a good ability to resist fracture
(Ashby et al. 1995). Here, we look at how the mechanical properties of β-keratin,
principally involving the syncitial barbule cortical cells of the rachis and barbs,
might work to significantly increase the ‘work of fracture’.
5.9 How β-Keratin Crucially Influenced Bird Evolution 249

Fig. 5.69  A new microstructural fiber model of feather rachis and barbs (see Chap. 1, Figs. 1.7
and 1.11 for classic engineering analogues). An exploded view of three fiber divisions of the
rachidial cortex and one of the barb cortex (both in dorsal and ventral walls). The cortex is iden-
tified by the thick syncytial barbules cells (6–8 µm in diameter). The lateral walls of the rachis
and barbs, the epicortex, are characterized by a crossed-fiber structure and absence of syncytial
barbules cells. One barb shows cortex removed to expose the medullary pith cells. Modified after
Lingham-Soliar (2014a), courtesy of Journal of Ornithology, Springer

The node-to-node regions of the syncitial barbule cell (~60–70 µm long) effec-
tively create a repeated dogbone shape along the fiber length. The nodes of one
fiber are invariably staggered with those of adjacent fibers in both 2- and 3-dimen-
sional planes (Figs. 5.62 and 5.70).
Rather than the traditional brick and mortar arrangement (Lingham-Soliar et al.
2010), the periodic nodes suggest an architecture perhaps even more comparable
with the ‘‘brick-bridge mortar’’ structure proposed for nacre (Song and Bai 2001;
Katti and Katti 2006) (Fig. 5.70b, c). The syncitial barbule nodes provide con-
nectivity for the entire fiber system by bridging the space occupied by the matrix.
As in nacre (Katti and Katti 2006), such bridges are considered here to influence
the strength and toughness at the interfaces and resistance to axial fracture by the
pattern of crack extension. In compressive loading, feather keratin also shows a
number of novel characteristics that aid in the type of horizontal crack-stopping
discussed by Ashby et al. (1995). The nodes of one fiber frequently align with the
250 5 Birds

Fig. 5.70  Mechanical structure of syncitial barbule cells (fibers). a Syncitial barbule cells in the
cortex of the feather rachis showing nodes (inset below shows detail of the syncitial barbule cells,
comprised of fibrils). b Diagrammatic representation of fiber bundling (syncytial barbules) in
three-dimensions. c Diagrammatic brick-bridge mortar structure between syncytial barbules and
polymer matrix demonstrating crack-stopping mechanisms (see text). Scale bar  = 5 µm. Ling-
ham-Soliar (2014a), courtesy of Journal of Ornithology, Springer

midpoint of adjacent fibers (Fig. 5.70b, c), hence a microcrack emanating from

transverse stresses will spread across a longitudinally oriented fiber but has a high
probability of stopping at the node of an adjacent fiber (Fig. 5.70c, arrow 1). On
the other hand if the path of a crack at right-angle to a fiber is not in line with
a node in the adjacent fiber the crack will enter the interfibrous matrix and the
chances are it will be deflected axially (length of ~45 µm) before it is trapped
between nodes (Fig. 5.70c, arrow 2). This Cook-Gordon crack blunting mecha-
nism coincides with short microcracks of similar length and near-periodic domains
observed in mechanical tests on the feather rachis (Bodde et al. 2011).
As in wood and young bones in which the bulk of fibers are also arranged lon-
gitudinally, fracture in the feather rachis is prone to occur longitudinally because
of failure by the Cook-Gordon mechanism (Gordon 1978; Ennos and van Casteren
2010). This danger is considered to be minimized in the rachidial cortex by a band
of several layers of circumferential fibers overlying the bulk of longitudinal fibers
(Figs. 5.64) (Lingham-Soliar et al. 2010; Lingham-Soliar and Murugan 2013).
5.9 How β-Keratin Crucially Influenced Bird Evolution 251

5.9.3.2 Stiffness, Ductility, and Buckling

The thickest fiber bundles of the feather rachis and barbs, the syncitial barbule
cells (Lingham-Soliar et al. 2010), which are bound by a polymer interface,
need to be put in an engineering context to fully understand the functional rami-
fications. In engineering systems, there are a number of major problems asso-
ciated with materials involving polymer fibers, e.g., axial fiber fracture, fiber
pull-out and, delamination of fibers as a consequence of debonding of the matrix
(Goodfellow 2004). Goodfellow (2004) found through fracture mechanics that
interfacial fracture might be reduced by increasing the fiber diameter or by coat-
ing the exposed fiber with silicone or a similar material. Recently, Naraghi et al.
(2010) working with carbon nanotubules, which are known to have among the
highest individual toughness in synthetic materials, found that when they were
bundled together they lose strength because of lateral slippage. They discovered
that, by adding a polymer matrix between the nanotubules, it resulted in very high
ductility and a very high toughness (reported to be higher than Kevlar), with the
ability to absorb and dissipate large amounts of energy before failure (see Munch
et al. 2008; Erb et al. 2012 for polymer toughness improvement in other materi-
als). Yet, this was achieved in a natural material, β-keratin in the feather of birds,
specifically in the structure of the rachis—in both conditions, i.e., increased fiber
bundle thickness and an interfacial polymer matrix or ‘‘glue’’—remarkably some
150 million years earlier.
In the feather rachidial and barb cortex one further key function of the dogbone
shape of the syncytial barbules deserves mention namely, to prevent or minimise
‘pull out’ of the fibers from the surrounding matrix and improve the transmis-
sion of forces (Fig. 5.70a, b). In engineering, this is analogous in structure and
function to steel rebars used as concrete reinforcement in composite materials in
high-rise building construction (Santos et al. 2007; Lingham-Soliar et al. 2010).
Furthermore, the cross-sections of the rachidial cortex (Fig. 5.68) may give a vis-
ual impression of how the syncitial barbule cells might respond during buckling
of the rachis. In the non-buckled section, syncitial barbule cells between nodes,
in transverse section, are more or less circular (Fig. 5.68a). This contrasts with
state in the buckled section, where some of the syncitial barbule cells are severely
distorted (compressed) (Fig. 5.68b, black arrows). The exceptions are where the
syncitial barbule cells are cut across or close to the nodes (Fig. 5.68a, b, white
arrows), which are more or less hexagonal in shape (seen best nearer the mid-
point of the node, Fig. 5.68a, lower arrow) and show little distortion in the buck-
led section. Given that nodes are staggered along the length of the rachis, these
unusual visual images indicate the stabilizing role they might play in delaying or
preventing buckling of the rachis during transverse stresses, i.e., the cracks may be
stopped along the radius at the nodes (Fig. 5.70b, c). Given also that the polymer
matrix was delineated by fungi, in the normal condition it is clear that it would
also help to strengthen the cortex (see Goodfellow 2004; Naraghi et al. 2010) and
prevent/delay fiber bundle (syncitial barbule) collapse during buckling.
252 5 Birds

5.9.3.3 Torsion and Flexion

The feather rachis may be regarded as a weakly pressurized system given the
gas-filled cells in the medulla. This pressure is confirmed by impressions on the
epicortical walls of the rachis and barbs (Lingham-Soliar and Murugan 2013)
(Fig.  5.65c), which the cross-fibers are suited to deal with. Without them even a
small longitudinal crack could spread dramatically. I use the thin-walled cylindri-
cal structure to simply demonstrate at the extreme end how a structure may fail by
splitting along the long axis (the hoop stress is twice as much as the longitudinal
stress) as a consequence of increased internal pressure (Gordon 1978) according to
the equation

s2 = rp t
where s is stress, t thickness, p pressure, r radius (Chap. 1, Fig. 1.11).
We have known for some time that the fibrous structure of the rachis cortex
is anisotropic—microfibers predominantly longitudinally oriented and a thin layer
or two circumferentially oriented. The related functions were discussed above. We
now know, with the discovery of a cross-fiber system in the epicortex of the barbs
and rachis, that the feather microfiber structure is far more complex than previ-
ously thought and highly anisotropic. The importance of the epicortical cross-fiber
architecture is emphasized by the fact that it occupies a surface area at least equal
to that of the cortex (Lingham-Soliar and Murugan 2013). The mechanical conse-
quences, which can only be considered briefly here, are significant. The cross-fiber
system involves a specialist bioengineering design principle (Wainwright et al.
1976, 1978; Lingham-Soliar 2005a, b) that enables rigidity in torsion in cylindri-
cal structures (high contraction or Poisson ratio, discussed in Chap. 1). The system
is widely found in nature and may be comprised of a variety of structural fibers in
different organisms, including collagen, chitin, (Wainwright et al. 1976) cellulose
(Gibson 2012) and β-keratin (Lingham-Soliar and Murugan 2013). Wainwright
et al. (1978) describe in shark skin the mechanical principles involved: ‘‘Since
twisted cylinders of homogeneous material fail by splitting at 45° to their long
axis [6], the best design for torsional stiffness in the shark’s caudal peduncle
would be collagen fibers in the skin wrapped at 45° to the body’s long axis’’ (note,
6, in parenthesis, refers to Wainwright et al. (1976). In the feather, the cross-fiber
architecture may provide a key mechanism for preventing damage to the rachis
and barbs. However, a rigid system risks being loaded with dangerously high
forces during flight. In this context, it is noteworthy that the longitudinal fiber
system of the cortex not only provides stiffness but, in contrast to the cross-fiber
system of the epicortex, importantly, allows torsion, which would help to lower
the critical bending moment needed to cause local buckling failure (Corning and
Biewener 1998). At the core of this understanding is the presence of two distinc-
tive fiber systems, that of the epicortex and of the cortex, which in given circum-
stances will inevitably function in synergy to promote ideal feather aerodynamics.
The potential for future biomechanical studies are clear.
5.9 How β-Keratin Crucially Influenced Bird Evolution 253

A highly important feature of the feather rachis and barbs is that, rather than
being hollow cylinders, they are comprised of a gas-filled core or foam (medullary
pith), which is tightly integrated with the rachidial and barb cortex (Purslow and
Vincent 1978; Bonser 2001) and epicortex (Fig. 5.71). Note the rachis and barbs
are not pressurized in the true sense of the word but Wainwright et al. (1978) dem-
onstrated that the crossed-fiber architecture could almost as effectively work in a
non-pressurized system. The medullary foam was shown to have a much lower
modulus than compact keratin (around 15 MPa) and stress–strain behavior typical
of that seen in closed-cell gas-filled foams (Bonser 2001). It has been suggested
(Lingham-Soliar et al. 2010) that the foam-filled centre of the rachis delays the
onset of buckling under compressive loading by transference of tensile stresses
from the cortical layer and absorption of the energy by the foam. Experimental
evidence has shown that a foam core significantly increases the elastic buckling
resistance of a cylindrical shell over that of a hollow cylinder of the same weight
in a number of biological structures, including plant stems, animal quills and the
feather rachis (Vincent and Owers 1986; Karam and Gibson 1995; Gibson and
Ashby 1999; Dawson and Gibson 2006; Fratzl and Weinkamer 2007).

Fig. 5.71  Native (non-biodegraded) medullary pith of Otus leucotus (resin embedded. a Part

of a 3-D, part longitudinal section (top) and transverse section (bottom) of rachis showing the
medulloid pith. Relief impressions of the medulloid pith cells can be seen on the overlying epi-
cortical layer indicating its ductility. Dissected cells (arrows) show thin polymer capsule lining
of the closed cells (see text). b Transverse section of barb adjacent to rachis showing medullary
pith cells. Inset, trabecula-like support of the cell walls shows a second level of porosity (see
text). Lingham-Soliar (2014a), courtesy of Journal of Ornithology, Springer
254 5 Birds

The actual extent of the mechanical role played by the medullary foam dur-
ing horizontal loading was calculated from tensile tests performed by Weiss and
Kirchner (2010). They found that resistance was dominated by the medullary pith
and that, as both cortex and medulla undergo the same displacement, the total elas-
tic energy is shared in the same proportion, i.e., 96 % of the total elastic energy
is stored in the medullary foam and 4 % in the cortex shell (this was discussed
in the context of Archaeopteryx’s flight capabilities, above). They concluded that
the medullary foam acts as an energy absorber. This potential for storing large
amounts of elastic energy in the medullary foam and in the cross-fiber architecture
of the epicortex of the rachis and barbs may indicate that the feather, as in a num-
ber of other structures in nature (Pabst 1996), has the capability of behaving as a
‘spring’ and that such capability might play an important role in restoring barbs and
rachises to their normal position following torsion or flexion (Lingham-Soliar and
Murugan 2013) (cf. caudal fin of Carcharodon carcharias; Lingham-Soliar 2005b).

5.9.3.4 Ductile Tearing

Mechanical characterization of the cortex of retrices (tail feathers) of the Toco

Toucan (Ramphastos toco) (Bodde et al. 2011) showed that the dorsal and ventral
surfaces are significantly stiffer (prone to brittle fracture) than those of the lateral
cortex (here, epicortex). Ductile tearing coincided with tangentially oriented fibers
rather than longitudinal, which is consistent with the latest findings on the struc-
ture of the epicortex (Lingham-Soliar and Murugan 2013).
Unlike in brittle fracture (low energy required), in soft materials, e.g., in
β-keratin of the epicortex, a much higher work of fracture is required because the
material is ductile, i.e., it has the capacity to deform permanently in response to
stress. In a ductile material, tension and compression failure occur by shear stress
at ~45° to the long axis—in the feather epicortex, the fibers are ideally aligned in
the direction of the greatest stress. Furthermore, the extensibility of a cross-fiber
architecture allows the epicortex to deform elastically (i.e., recoverably) rather than
crack and perhaps fracture (cf. the stiffer cortex and brittle fracture above; note that
in a ‘soft’ ductile metal like steel, the same sliding occurs except involving the mol-
ecules). This latest understanding of the feather epicortex also shows that it is no
coincidence that the barbs and barbules are attached to a ductile surface, given that
it would enable greater resistance to stress compared to a brittle surface (in which
they would snap off) and only confirms the ‘clever’ ways (Gordon 1978) in which
nature ‘solves’ complex problems by multifunctional designs.

5.9.3.5 Feather Microstructure and Evolution

The evolution of birds and of feathers ranks among the most contentious top-
ics in evolutionary biology today (see Feduccia 2012; see above). The capacity
to form diverse structural elements (Lingham-Soliar et al. 2010; Lingham-Soliar
5.9 How β-Keratin Crucially Influenced Bird Evolution 255

and Murugan 2013) is particularly notable, given that β-keratin is considered con-
strained in an evolutionary sense by a highly conserved molecular structure, con-
sidered a plesiomorphic feature of the archosaurian ancestor of crocodilians and
birds (Sawyer and Knapp 2003). Although current knowledge suggests that these
newly revealed micro-structures of the feather cortex and epicortex may be solely
associated with avian β-keratin and not part of the ancestral condition of keratin,
this is yet to be confirmed by further work on other types of β-keratin (see below).
Recently, Greenwold and Sawyer (2011) helped to refine families of β-keratins
that evolved since the protein first appeared almost 300 million years ago. They
found that in a central portion of the protein, one amino acid sequence (31 resi-
dues long) is highly conserved throughout all the species that express β-keratin.
They reported a preponderance of feather β-keratin sequences in modern birds–a
wide range of similar but not identical sequences that began to multiply in their
view, albeit tentative, at that important junction 125 million years ago when the
modern feather β-keratin began to proliferate throughout the avian genome. They
propose that the appearance of the subfamily of feather β-keratins in modern
birds altered the biophysical nature of the feather establishing its role in powered
flight and hypothesize that Archaeopteryx did not possess this ‘modern’ type of
β-keratin, which precluded it from flapping or powered flight, citing support from
the now soundly refuted study by Nudds and Dyke (2010a, b), as shown above.
While the development of a new subfamily of feather β-keratins may indeed
be an important refinement that began/spread about 125 MYR at the time of a
major radiation of birds, the conclusion that it may have been a defining moment
for powered flight, does not take account of the fact that animals are not simply
defined by their chemistry or molecular structure (convergent evolution empha-
sizes how vastly different chemistries may enable highly similar functional roles
through complex mechano-structural designs. A lack of data on the structural
attributes of the feather beyond the molecular and angstrom/nanostructural levels
led to a failure to understand its high work of fracture compared to that of many
other materials and structures in nature. Furthermore, the advanced morphological
characteristics of feather structure in Archaeopteryx (discussed above) compared
with modern birds indicates the high probability that the advanced feather micro-
structure described above, and concomitant biomechanical ramifications, was pre-
sent in Archaeopteryx. Given the massive evolutionary developments in bird flight
since the Cretaceous, the new refinements in β-keratin would almost certainly have
evolved in line with advanced birds but requires caution when using them as a
defining moment in the early stages of flapping flight in birds.
If the view above with respect to the microstructure of Archaeopteryx is correct,
where do the findings of a hierarchical micro-structure, culminating in the syncitial
barbule, fit in with respect to the evolution of the feather. When I sent a copy of the
paper (Lingham-Soliar et al. 2010) first describing syncytial barbules in the feather
rachis to the notable expert on feather structure, Peter Stettenheim, he replied with a
kind email (Peter Stettenheim personal communication, 2010) that included the fol-
lowing comments,“[i]t is a fascinating and very original piece of work, both for its
findings and its method of feather preparation… Your finding not only furnishes a
256 5 Birds

good indication of how the rachis originated, but also seems to support the old notion
that the earliest feathers were downy, not pennaceous…” Ironically, I had diverged
from paleontological research on the origin of the feather because I was sick and
tired of some of the hostile, biased and ill-conceived criticisms (see above, Padian
and Norell) that my findings were receiving and the determined efforts by many
influential workers to suppress them by the most reprehensible methods as referees
and editors. It was taking 5–10 times the normal effort to get a decent paper pub-
lished in this climate (see Chap. 7). Occasionally, in contrast there was a pleasant
reminder of the integrity of some scientists such as seen through the words of one
reviewer of the self-same paper, “[t]he SEM pictures (Figs. 1–4) are the heart of this
[study], but their interpretative diagram (Fig. 5) is the one that will end up in the text-
books. Others will dispute the details of their interpretation, but that is as it should
be. I would not propose changing anything. This study is going to be much cited.”
What showed the calibre of this anonymous referee were the words “but that is as
it should be.” Ironically, I had no idea that in trying to get away from the paleonto-
logical cauldron of Birds are Dinosaurs, my neontological research would take the
twist that would drive it back into the heart of the controversy of feather evolution,
as Peter Stettenheim (quite removed from the controversy) so presciently noted when
he received a copy of the paper. His remarks struck a chord because it is difficult to
reconcile the advanced structural and biomechanical features of the syncytial barbules
within rachides and barbs, described above, with being acquired in a single evolu-
tionary step, i.e., in a flight feather. It seems too predetermined (for the flight stresses
to come) whereas I am more inclined towards Dobzhansky’s (1962; see Volume 1)
idea of inheriting advantageous characters being more a matter of chance, “the dice
of destiny.” Consistent with Peter Stettenheim’s views, the nodes and hooks and claws
of the syncytial barbules would seem to have evolved for an entirely different func-
tion, i.e., in a downy protofeather stage to keep the filaments apart so as to trap air
for effective insulation (Stettenheim 2000). These syncytial barbules complete with
nodes, hooks and claws, would presumably then have been exapted without prede-
termination or plan into the internal structure of early barbs and rachides, with their
new biomechanical ramifications being a fortuitous throw of the dice. In contrast, if
syncytial barbules were a structural design feature occurring in a fully evolved flight
feather, then it would seem that they would be an inherent design feature of β-keratin
per se, and not of avian β-keratin specifically. If the latter case, then the acid test
would be that syncytial barbules should be found in other occurrences of β-keratin,
outside of feathers, involved in load-bearing (investigation in the pipeline).
Where does this leave the contentious question of protofeathers in dinosaurs.
I have always believed that the idea of protofeathers was a good one but rather
that thus far the execution of converting a good hypothesis into reality is dismally
poor and contrived and that most, if not all, reported cases of protofeathers, are
in fact collagen (some perhaps even keratin) structural fibers. A genuine ‘downy’
protofeather in this context would in my view almost certainly possess thickened
nodes, given their greater robustness, and possibly hooks. Gail Robertson showed
a perfectly preserved duck down feather barbule with complete nodes and hooks
and internal fibrils (~0.5 µm thick) dated 1,000–3,500 BP, without apparent miner-
alization (Robertson 2002; see Frontispiece, far right). This is consistent with my
5.9 How β-Keratin Crucially Influenced Bird Evolution 257

earlier comments (in Feduccia et al. 2005), “[c]ould any of the integumental struc-
tures preserved in theropod dinosaurs be feathers? On the basis of current evidence
this seems unlikely. Nevertheless, we underwrite this comment with the view that it
would be foolhardy and dogmatic for either side of the debate on the origin of birds
(dinosaurian or non-dinosaurian) to proclaim that the subject is closed”
If protofeathers were to be genuinely found in an archosaur/non-avian dinosaur
ancestral to birds does this signify support for a ground up hypothesis for bird flight?
On this quite emphatically my answer would be no. There is no reason to think that a
creature with protofeathers (for whatever reason they originated), as with present day
mammals with hair, would not have found trees as a safe refuge from predators and
that over the course of evolution might not have become effective gliders on the road
to active flight, with the incipient feathers developing into more effective flight sur-
faces. Indeed, Alan Feduccia’s reasonable idea that an insulative coat of protofeathers
would be ineffective when wet (without the shelter of a parent as in ostriches) may
be another reason that drove bird ancestors up into the shelter of trees.
The field of biomimetics, in which inspiration in engineering is gained from
nature, is becoming increasingly important (Meyers et al. 2006, 2013). Historically,
the feather microstructure has been understudied, largely because it has been hin-
dered by the complexity of its polymeric structure, and consequently underesti-
mated. As a result, one of the most remarkable structures in nature has contributed
very little to the field of biomechanics and biomimetics. The present study briefly
reviews the ubiquitous present of syncitial barbule cells as a vital component of
feather structure as well as the equally important crossed-fibre architecture. I have
shown how important our new understanding of the microstructure of the feather is
to the problem of crack-stopping and the stresses involved in bird flight. As well as
adding to our understanding of questions related to bird flight, our increasing knowl-
edge of self-assembling avian β-keratin fibres may provide inspiration for new gen-
erations of nanofibers in the field of biomimetics. I predict exciting times ahead.

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Chapter 6
Integumental Taphonomy

The taphonomy of the integument in the present chapter is focused predominantly

on the high-profile studies involving the popular idea of Birds are Dinosaurs and
its impact on questions relating to the origin and evolution of birds. The studies,
particularly with respect to the alleged discoveries of early feathers or protofeath-
ers will be the main focus below, more or less chronologically based on studies
in which I have been personally involved in the debate. However, to get an appre-
ciation of the problems involved in interpreting fossilized soft tissue we start with
studies involving ichthyosaur soft tissue. As we saw in Volume 1, ichthyosaurs
were marine reptiles.

6.1 Ichthyosaur Soft Tissue

An understanding of the functional importance of the ichthyosaur dermis started

with a re-description and reinterpretation of the integumental fibers in the 200 mil-
lion-year-old Lower Lias ichthyosaur, specimen, Ichthyosaurus GLAHM V1180a
(Lingham-Soliar 1999), which showed for the first time that ichthyosaurs had a
crossed-fiber architecture of the dermis, the first such observation in any fossil spe-
cies. It was highly significant in reinforcing the hypothesis that Jurassic ichthyosaurs
were fast, thunniform swimmers (Volume 1 and Chap. 2 in this volume). It led to
further studies on preserved soft tissue in ichthyosaurs in other specimens that would
have an impact not just for ichthyosaur biology and biomechanics but would serve
as a road map to understanding and interpreting fossilized integumental structures in
other vertebrate animals. A crucial part of that paper (Lingham-Soliar 1999) was in
demonstrating why Delair’s (1966) original description, published in Nature, had got
it so wrong. What he had described were not integumental fibers at all, but slender
parallel patches of tissue (a consequence of wrinkling) and if anything, it served to
demonstrate that the investigation and interpretation of preserved soft tissue in fossil

© Springer-Verlag Berlin Heidelberg 2015 263

T. Lingham-Soliar, The Vertebrate Integument Volume 2,
DOI 10.1007/978-3-662-46005-4_6
264 6  Integumental Taphonomy

animals was far more complex than apparent (with due respect to Delair he did draw
attention to the soft tissue). It was the lesson learned from that study that would lead
to increasingly more incisive questions being asked about the ichthyosaur integu-
ment which culminated in answers at nano-structural levels (Lingham-Soliar and
Wesley-Smith 2008) (Chap. 2).
The above study raised questions relating to structures interpreted as early
stages in feather evolution in dinosaurs, commonly referred to as protofeathers.
The explanations were based on simplistic arguments, despite the enormous rami-
fications, and on flawed investigations. Among such flaws was a total dependence
on the visual image and an absence of comparative and experimental studies. This
exists to the present day, with one exception which will be dealt with later.
Studies on ichthyosaur fibers (Lingham-Soliar 1999, 2001) opened up an
understanding of fossilized collagen fibers in the context of decay and taphonomic
processes. It was shown that collagen fibers could take various shapes following
the death of the animal as a consequence of decay. They also showed that the idi-
osyncrasies of preservation may account for fibers diverging or forming a myriad
of patterns (Fig. 6.1). Underscoring the preservation of soft tissue in vertebrate
fossils is the fact that collagen may comprise up to 40 % of the animal’s structural
proteins and may frequently occur in multiple layers of the integument and mani-
fest different dimensions and orientations. Furthermore, collagen structural fibers
may form structural support for numerous external structures such as frills, crests,
flaps, etc., or may simply during decay preserve along the edges/periphery of the
animal on the substrate, as for example noted in the ichthyosaur Stenopterygius
SMF R 457 (Lingham-Soliar 2001, 2003a) (Fig. 6.1).
A study by Currie and Chen’s (2001, p. 1719) was the catalyst for showing how
poorly understood the preservation of soft tissue was with respect to the Chinese
dinosaurs. For instance, the authors stated that the fossilized integumentary struc-
tures of the theropod dinosaur, Sinosauropteryx, were “soft and pliable.” This is
highly speculative, given that all the organic material of most fossils is diageneti-
cally transformed into inorganic molecules. We do not know their biological com-
position, hence impossible to say what they might have been like in real life based
on a sinuous appearance without detailed histological studies, let alone that they
were ‘soft and pliable’. For instance, collagen fibers are affected by various con-
ditions, e.g., with loss of muscle tension with death and subsequent decay they
contract and become sinuous or wavy. Another speculation of Currie and Chen’s
was that under a microscope the margins of the larger structures are darker along
the edges but light medially. They therefore suggested that it was an indication that
the fibers may have been hollow, but produced no evidence to support what they
allegedly saw i.e., a photo. Regardless, the wholly unsupported speculation has
grown into fact over the years. On the other hand a more parsimonious explanation
was shown in the ichthyosaur SMF 457, in which fibers show different stages of
mineralization, darker toward the edges and lighter in the middle (Lingham-Soliar
2003a), which included photographic evidence (Fig. 6.1f, arrows).
Allegations such as those by Currie and Chen (2001) cloud one of the impor-
tant questions in evolutionary biology, the evolution of the avian feather. The sub-
ject necessitates that the suggested presence of protofeathers in dinosaurs must
6.1  Ichthyosaur Soft Tissue 265

Fig. 6.1  Integumentary fibers in three ichthyosaurs (a–g) and a shark. a SMF 457, disorganized
fibers on the posterodorsal surface; the result of, for example, fiber breaks and false joins. b, c
PMU R435, tufts of fibers apparently branching from a narrow basal point. d SMF 457, integ-
umentary fibers on the matrix near the anterodorsal surface showing rachis-like filaments and
stubs (arrows). e SMF 457, posterolateral surface showing fine fibers preserved over thick fib-
ers, resembling rachis and barbs (arrows). f SMF 457, matrix above posterodorsal surface show-
ing fibers resembling rachis and barbs; arrows show? mineralization of long fiber. g GLAHM
V1180a shows two integumentary fiber layers, the patchy top one impresses on those below.
Note, “bending” of fibers (in life). Shark integument. h Fibers in the white shark, Carcharodon
carcharias, just anterior to dorsal fin (Lingham-Soliar, unpublished data) showing instances of
herringbone patterns and an example of fibers curving around openings in tissue (arrow). i Cross-
section of the shark’s skin and fibers showing thin collagenous fibers in the superficial dermis
(arrow) and thick fiber bundles in the deeper dermis (arrow/circled). Note that the large fiber
bundles are divided like muscle fasciculi into smaller fiber bundles and ultimately fibrils (the
latter seen under SEM). SMF Senckenberg Museum Frankfurt, PMU Paleontological Museum
Uppsala, GLAHM Glasgow Hunterian Museum
266 6  Integumental Taphonomy

be proven or rejected based on incontrovertible evidence, especially given the

p­resence of similar filamentous structures in other groups of fossilized archo-
saurian and non-archosaurian reptiles (Lingham-Soliar 2003a). The latter study
showed marked similarities in branching patterns of collagen fibers in Jurassic
ichthyosaurs point-by-point with filaments preserved in the non-avian theropod
dinosaur Sinosauropteryx, structures previously considered to be protofeathers.
The same study also showed that the that structures shown to be fibers supporting
the wings of a pterosaur (Unwin and Bakhurina 1994, reference in Chap. 4), i.e.,
straight, closely packed fibers on the outer half of the wing and shorter, loosely
packed fibers close to the body may have been wrongly interpreted as two different
kinds of structural fibers. One, was construed to provide increased elasticity close
to the body and the other, greater rigidity further away. I pointed out (Lingham-
Soliar 2003a) that the fibers showed all the characteristics of collagen fibers and
that the fibers closest to the body were more decayed and hence lost their tension
and became bent, compared to those further away from the body. The study served
to show that the thesis of dinosaur protofeathers required more substantial support
than provided but emphasized that simply because the studies were poorly con-
strained, “[i]t is impossible to say that the famous Chinese dromaeosaurs did not
possess feathers” but rather that each occurrence of preserved soft tissue “needs to
be scrutinized on its own merits with scientific rigor” (Lingham-Soliar 2003a).

6.2 Death of a Dolphin

Rather than the verificationist approach adopted by, e.g., Currie and Chen (2001),
it was important to test the visual image and to investigate whether or not colla-
gen fibers/fiber bundles (Fig. 6.2) during decay and degradation could mimic the
alleged protofeathers. To attempt to achieve this, a dolphin carcass was buried for

Fig. 6.2  Schematic
illustration of type I collagen
fibers. The typical banding
of type I collagen fibrils
is readily detectable in
longitudinal view. The five
fibers depicted comprise
a bundle and many such
bundles may form larger fiber
bundles
6.2  Death of a Dolphin 267

a year so as to obtain data on the important stages of decomposition that precede

potential fossilization following the death of an animal (Lingham-Soliar 2003b).
At the end of a year dermal tissue samples of the dolphin were removed for exami-
nation. The fibers in the dermis showed a wavy structure, almost downy in appear-
ance. Within the hypodermis, toward the central thicker parts of the section, the
collagen fibers had compacted and the three dimensional latticework, observable in
fresh dolphin blubber, had more or less collapsed (Fig. 6.3a, b). Chromatographic
analysis of this layer revealed pronounced oxidation of the unsaturated lipids, which
probably accounted for the collapse of the latticework (only saturated fatty acids with
14, 16, and 18 carbon atoms remained) (Lingham-Soliar 2003b). Nearer the edges of
the blubber (hypodermis) sections (Fig. 6.3c–e) there was wholesale breakdown and
disruption of fiber bundles of various size classes (Fig. 6.3f, g). The process of “peel-
ing” apart of the collagen bundles was evident in many places.
The experiments showed clearly that the degrading dermis and in particular the
collagen fibers that reinforced it could visually mimic feathers and protofeathers.
Another feature widely observed in decomposing dolphin tissue was a bead-like
structure of the collagen fibers (Lingham-Soliar 2003b), normal in fresh tissue.
A similar condition was noted in fossilized integumental fibers in ichthyosaurs.
However, under polarized light at different azimuths, tangential sections of dolphin
blubber and shark skin (Lingham-Soliar 2003b, and here Fig. 6.3b) showed peaks
and troughs of the fibers, a consequence of regular, short waves (at about 50 μm
intervals), which coincided with the observed bead-like structure and confirmed
that they were not breaks in the fibers. In this feature it was an artifact of prepara-
tion, i.e., dehydration. All sections were air-dried to increase transparency and bire-
fringence during light microscopy, which resulted in slight contraction of the fibers
(Lingham-Soliar 2003b). In fossils, rippling of the skin would probably occur with
dehydration and the peaks of the “waves” in collagen fibers would fossilize as beads.
Significantly, collagen in the integument of many living animals does not
appear as simple parallel strands dispersed in a matrix, but rather collagen may
form highly organized complex architectural systems, frequently providing s­ pecific
forms of reinforcement (Wainwright et al. 1976; Lingham-Soliar 2005a, b). To test
the different types of fiber organization the dermis of a number of ­modern-day ani-
mals including reptiles was investigated (Feduccia et al. 2005). The reptiles studied
provided no exception to the complexities of collagen architectural systems found
in animals. These findings on morphologically complex organic material it was
hoped would provide a better understanding of how soft tissue might fossilize and
how they could be affected by the idiosyncrasies associated with the processes of
decomposition.
Investigations into the dermis of the white shark, Carcharodon carcharias
(Lingham-Soliar 2005a, b) proved very useful in understanding the integument of
fossil animals. The collagen fiber bundles in the dermis of these sharks showed
both a crossed-fiber architecture as well as fibers uni-directionally arranged. These
complex architectures also present in dolphins, are capable of breaking down to
show irregular branching patterns because of the very nature of their fiber organi-
zation and bundle structure, which we saw in the dolphin experiment and in pre-
served soft tissue in ichthyosaurs.
268 6  Integumental Taphonomy

Fig. 6.3  Fine fibers from the SDS (subdermal connective tissue sheath) of the decomposing dol-
phin observed by polarized light microscopy. a Layers of fine collagen fibers undergoing degra-
dation but still retaining tension. b Fine collagen fibers losing their tension and taking on a wavy
appearance. Collagen fibers in decomposing dolphin blubber observed under polarized light. c
Peripheral collagen fiber bundles extending about 10–15 mm from the edge of the small sample
(they may be traced a similar distance into the material). d Detail of single fibers in c showing
component fibers during degradation, including filamentous branching patterns. e Plume-like pat-
terns of some of the fibers. f Two thick fiber bundles. g Fiber bundles in f showing disorganiza-
tion of the finer fibers and bundles to produce overlapping feather-like patterns (note that f and g
 6.3  The Dermis in Extant Reptiles 269

 Fig. 6.3 (continued)
indicate how different levels of magnification and preservation capture featherlike patterns of
d­ifferent size classes; arrows show small fiber bundles). h Peeling of fibers and coalescing with
­others, indicating a glue-like substance binding fibers together

6.3 The Dermis in Extant Reptiles

In the dermis of reptiles and birds examined in Feduccia et al. (2005), the col-
lagen fiber bundles of the dermis showed a variety of architectures. Thick colla-
gen bundles occur in the dermis in the tail of Agama utricolis and slightly thinner
bundles in the skin on the reptile’s ventral surface (belly region) (Fig. 6.4a, b).
Fiber bundles in several sections (Fig. 6.4a) showed orientation in the same direc-
tion (left-handed). A crossed-helical pattern of the fiber bundles is present in
neck of the turtle Caretta caretta and body of the Burmese python molurus biv-
ittatus (Fig. 6.4d, g). The smaller black snake, Macrelaps microlepidotus, how-
ever, showed fiber bundles in layers oriented in a single direction, left-handed
(Fig. 6.4e). The crest in Basiliscus plumifrons extends from the longitudinal mid-
point of the skull to the tail, varying in height. The crest is covered by translu-
cent scales, is almost entirely cartilaginous, and is strengthened along its length by
ossified structures (Fig. 6.4c). The comb of the domestic chicken, Gallus domes-
ticus which was found to be very different in structure from the crest of a lizard
such as B. plumifrons or the skin generally; stiffness is achieved by dense adipose
tissue reinforced by a matrix of collagen fibers (Fig. 6.4i), very similar to stiffen-
ing of the caudal peduncle in dolphins and lamnid sharks (Lingham-Soliar 2005b).
From the tests, Feduccia et al. (2005) were able to report that the two major
types of architectures of collagen fibers, namely, crossed-fiber (left- and right-
handed orientations) and non-crossed fiber (fibers oriented in a single direction),
were found variously in the reptiles studied. Furthermore, a novel adaptation of
the crossed-helical fiber architecture was observed in the dermis of the Burmese
python (Fig. 6.4g), wherein the fibers of one layer cross-weave with the next in
left- and right-handed orientations. The functional interpretation of this unusual
architecture may be that it probably provides greater stiffness to the skin. This may
be useful in protection of the body and may also provide more support in regions
that are likely to experience considerable stress, e.g., during the ingestion of large
prey (cross-weaving of fibers was noted in some dermal layers of certain sharks
[Motta 1977]). The study underscored the difficulties of making generalizations
with respect to the architecture of the integument of living animals, let alone fossil
forms, with all the vagaries associated with the taphonomic processes.
It is axiomatic that collagen fibers/fiber bundles disrupted either during decay
and/or degradation (erosion or mechanical abrasion) (Fig. 6.3) are capable of
forming aberrant patterns. Almost invariably, fibers open up such that the most
compact are where they are attached to the tissue mass (“glued,” see above),
unraveling and spreading out further away, and finally becoming frayed and
270 6  Integumental Taphonomy

Fig. 6.4  Collagen in vertebrate (mainly reptile) integument. a The agamid lizard, Agama utri-
collis. Thick bundles of collagen fibers in the dermis overlying the anterodorsal part of the tail
near its union with the body; above some of the component fibers (arrows) comprising a thicker
bundle are seen; below some fiber bundles have separated as a consequence of mechanical abra-
sion (microtomy) to form an aberrant branched structure (arrow). b Agama utricollis. Collagen
fiber bundles (arrows) in the dermis in the ventral surface of the animal, approximately mid-point
between the anterior and posterior legs (arrows show some collagen bundles). c Part of the semi-
transparent head crest of the Jesus lizard, Basiliscus plumifrons, showing translucent scales and
thick fibers (arrows), probably collagenous, within a dense matrix of connective tissue (tangen-
tial section of crest, 0.25 mm thick, includes the scaly surface). d The loggerhead turtle, Caretta
caretta. Collagen. Fiber bundles in the dermis in the neck show alternating layers of fibers in
left- and right-handed orientations (arrows); on the left can be seen traces of the overlying layer
of left-handed fiber bundles (left arrow). e The Natal black snake, Macrelaps microlepidotus.
Dermis on the lateral surface of the body (mid-length) showing slightly wavy bundles of collagen
fibers (arrows); waviness is probably a consequence of loss of muscle tone or dehydration of the
tissue (Lingham-Soliar 2003b); all sections showed the same orientations. f Detail of some fiber
 6.3  The Dermis in Extant Reptiles 271

 Fig. 6.4 (continued)
bundles in g shows fine fiber components breaking off from the thick bundles. g Burmese python,
Python, molurus bivittatus (3 m long). Unusual cross-weaving of layers of oppositely oriented
helical fibers in skin at body mid-length (lateral surface); this architecture probably achieves
increased strength with possibly a slight reduction in skin flexibility (see Lingham-Soliar 2005b,
for further discussion on different functional types of collagenous architectures of the dermis).
h Crocodilus niloticus, newborn juvenile (body 15.4 cm long). Collagen fibers in the skin in the
lateral surface of the neck. On the right can be seen the edge of a scute. i Domestic chicken, Gal-
lus domesticus. A matrix of collagen fiber bundles reinforces the dense adipose tissue making up
the comb. From Feduccia et al. (2005), courtesy of John Wiley and Sons, Ltd

narrow at the tips of the structure (comparable to the shape of a flame) (Fig. 6.3e).
These characteristics of collagen are considered in the context of certain fossilized
integumental structures that have been interpreted by some workers as protofeath-
ers, albeit without any experimental or histological evidence.

6.4 Sinosauropteryx, A Basal Theropod

The idea of protofeathers has strengthened the resolve of many paleontologists

that birds are direct descendents of theropod dinosaurs (e.g., Chen et al. 1998;
Currie and Chen 2001; Prum and Brush 2002). The spectacular Early Cretaceous
Jehol biota in Liaoning Province, China has thus added a potentially power-
ful new dimension to the hypothesis of the dinosaurian origin of birds with per-
haps the ‘prima donna’ of the discoveries being the basal theropod dinosaur
Sinosauropteryx, proclaimed to be the first ‘feathered’ theropod dinosaur (Chen
et al. 1998; Currie and Chen 2001).
Given the importance of Sinosauropteryx as a basal dinosaur with alleged
protofeathers, a new specimen of Sinosauropteryx was investigated (Lingham-
Soliar et al. 2007) in addition to existing material, including the holotype. The
hypothesis required that if these structures were to be accepted as feather pro-
genitors the investigation should fulfill (i) sound analytical methods and minimal
speculation, (ii) support for findings from extant and extinct vertebrates, (iii) an
appreciation of decompositional and taphonomic processes, and (iv) open presen-
tation of data and photos in support of any proposals (Lingham-Soliar et al. 2007).
All the investigations in IVPP V12415 showed that the integumental structures
proposed as protofeathers are the remains of structural fibers that provide tough-
ness. The preservation in the proximal tail area revealed an architecture of closely
associated bands of fibers parallel to the tail’s long axis, which appeared to be der-
mal in origin. In adjacent more exposed areas, the fibers were short, fragmented
and disorganized. Fibers preserved dorsal to the neck and back and in the distal
part of the tail are the remains of a stiffening system of a crest, peripheral to the
body and extending from the head to the tip of the tail. Among the more instruc-
tive of the findings were that the fibers identified within the body area were similar
272 6  Integumental Taphonomy

Fig. 6.5  Sinosauropteryx IVPP V12415. Integumental structures. a Overview of the area with

significant soft-tissue preservation within the body rather than coronal. Integumental structures
occur in the tail recess and overlying the vertebrae; the chevrons have been displaced. b Detail
in (a). Red arrows show some isolated integumental structures; white arrows show integumental
structures closely associated to give the impression of branching; white circle shows two closely
associated integumental structures; large black arrows shows the vertical part of the excavation in
which the best preservations occur. c Integumental structures at the juncture between the neck and
body, detail in circle shows the angles of the beaded fibers. d Integumental structures in the distal
part of the tail showing gaps between preserved tissues (cf. holotype, Fig. 1b). e Detail, showing
beaded integumental structures. f Schematic of (d). g Isolated integumental structures from vari-
 6.4  Sinosauropteryx, A Basal Theropod 273

 Fig. 6.5 (continued)
ous parts of the preservation, reoriented for ease of viewing; b1–6, 8, from the integument within
body outline; b5 circled in (Fig. 2b), b7 represents integumental structure overlying well-preserved
vertebrae. h Integumental structures in the last but three terminal caudal vertebrae preserved.
i Detail of h showing integumental structures as part of a matrix of connective tissue at their lower
half, while in the distal half, the individual structures are more evident (circled), becoming pro-
gressively more degraded toward the tips; circle shows mid-stage of a sheath of regular, tight, par-
allel fiber associations. Scale bars, a, d 2 cm, b, c 1 cm, g, h 1 mm, i 1 cm and j 2 mm

in structure to those that were in peripheral regions of the neck, shoulder, back and
tail, i.e., belonging to the crest (see Frontispiece), confirming that they were struc-
tural fibers, probably collagen (Fig. 6.5). Yet the most striking evidence of this
came from Sinosauropteryx NIGP 127587 from the figures in the original study by
Chen et al. (1998). It showed geometrically precise bands of parallel fibers previ-
ously undescribed (Fig. 6.6). At the edges of these bands, degradation is evident
as a consequence of which the fibers start to become disorganized and sinuous
(Lingham-Soliar et al. 2007, Fig. 4). The geometric pattern noted is maintained
so long as there is tension in the tissue regardless of whether this is in the skin,
muscle or frill. Once tension is lost, the fibers may take on a sinuous appearance
(Gordon 1978; Lingham-Soliar 2003a, b). In both the nature of the fibrous struc-
tures and the structural architectures (geometrically parallel) in Sinosauropteryx,
they compare with collagenous fiber reinforcements of the dermis in living ani-
mals (Feduccia et al. 2005 and references therein; Lingham-Soliar 2005a, b).
Among the important findings on Sinosauropteryx (Lingham-Soliar et al. 2007)
were those relating to its taphonomy. Preservational bias of fibers, e.g., occurrence
in one well preserved specimen and not in another is one of the enigmas of fos-
silization frequently noted in different specimens. For example, in the ichthyosaur
Stenopterygius dermal fibers were preserved over vertebrae and external substrate
(Fig.  6.1d, f) in one soft-tissue specimen but solely within the body in another

Fig. 6.6  Integumentary structures in Sinosauropteryx NIGP 127587. Structural fibers along the

ventral border of the tail. Detail of the dermal tissue shows the fine horizontal geometric fibers
that were not in a state of decomposition as evident from their tension. Scale bar 0.5 cm
274 6  Integumental Taphonomy

(Lingham-Soliar 2001) and similar differences are noted in soft-tissue preserva-

tion in the two Psittacosaurus specimens mentioned above (Mayr et al. 2002;
Feduccia et al. 2005; Lingham-Soliar and Plodowski 2010; Lingham-Soliar 2008).
Preservation of a hypothesized crest occurs in our specimen over the neck and tail
(with scanty remains over the animal’s back). In the holotype (Chen et al. 1998),
it is virtually complete from the neck to the tip of the tail. Differences of preserva-
tion may depend, e.g., on how much of the animal was imbedded in the sediment
(mud) immediately after death. For instance, among the many complexities of
preservation (Lingham-Soliar 2003a, b, 2012, 2013; Lingham-Soliar et al. 2007),
if the crest at the highest part of an animal lying on its side, i.e., the body and
thicker part of the tail, was not rapidly and completely imbedded in the sediment
(a possible fate in our specimen) then rapid degradation and destruction of the frill
may occur by, e.g., mechanical agents (albeit not exclusively) such as wind, water
and by scavengers. Initially, the matrix of the crest would permit the fibers a good
degree of tension, but with decomposition, this tension will inevitably be lost.

6.5 Pushing Feathered Dinosaurs into the Mid-Triassic

6.5.1 Beipiaosaurus

Xu et al. (2009, p. 832) reported the discovery of novel “feathers” in a theropod

dinosaur Beipiaosaurus. These “elongated broad filamentous feathers (EBFFs)”
they stated can be distinguished from all other feathers previously reported in
non-avian dinosaurs, i.e., “short, slender filamentous feathers.” Given their nov-
elty, reference to them as feathers from the very first paragraph onwards, rather
than, e.g., integumental structures, is perverse given that normal scientific pro-
cedure for establishing things as “novel” requires an investigation before assum-
ing the answer (we will see in Chap. 7 more on the total breakdown of scientific
procedure by these workers and various colleagues in a series of highly flawed
papers). On the basis of their findings, Xu et al. (2009, p. 832) state that “all major
predicted morphotypes have now been documented in the fossil record”, i.e., a
complete transitional series in the evolution of the feather—a unique structure in
evolutionary biology. This transitional series of feather morphologies they say was
shown to coincide with a developmental model (see Chap. 7).
Their analysis was as follows. Compared to other descriptions of protofeath-
ers in non-avian theropods, the EBFFs (Xu et al. 2009, p. 832; see critiques,
(Lingham-Soliar 2010a, b) which includes some of the comments below) “differ
significantly in morphology,” i.e., they are mono-filamentous, broad, much longer
than normal filamentous feathers, and flattened in appearance. Xu et al. (2009)
attempt to associate their EBFFs with feathers by two features: (1) a somewhat
flattened tubular (elliptical) cross-sectional profile in accordance with the some-
what flattened feather rami in modern birds and, the more critically important fea-
ture, (2) hollowness. These two conditions are considered below largely through
their own words.
6.5  Pushing Feathered Dinosaurs into the Mid-Triassic 275

(1) Rather than a sub-circular cross-section, Xu et al. (2009) state: “Because the
EBFFs are preserved as dark carbonized impressions, their relatively great
width makes them appear planar” and that it is “more probable that the fila-
ments developed as stiff large tubes with an elliptical cross-section.” For this
cross-section, with no known modern-day analogue they (Xu et al. 2009,
p. 833), cite as support Lucas and Stettenheim (1972), bearing in mind the fila-
ments are no more than a carbonized smear on the rock, stating that in mod-
ern feathers the “individual rami and barbules are also somewhat flattened.”
Lucas and Stettenheim’s (1972, p. 239) actual comment regarding modern
feather cross-sections is “the rachis is generally four-sided [not elliptical] and
slightly wider than thick,” a shape that would be indistinguishable from cir-
cular or elliptical cross-sections when flattened as carbonized impressions.
Next, they add (Xu et al. 2009, p. 833), “The cross-section of the epidermal
collar was PROBABLY [my emphasis] elliptical, rather than subcircular, a
condition that would explain the planar appearance of the preserved EBFFs
of Beipiaosaurus.” However, other than speculation for an epidermal col-
lar (Xu et al. 2009, p. 833), i.e., “each EBFF on the body of Beipiaosaurus
PRESUMABLY [my emphasis] grew from an epidermal collar,” there is neither
a description of one nor graphic illustration that even remotely suggests such
a structure (Fig. 6.7a, b). Thus, since the epidermal collar is hypothetical, its
elliptical cross-section must also be hypothetical—yet the authors conclude that
it provides an explanation for the elliptical cross-section of the EBFFs (above).
The circularity of this ‘argument’ is clear, with one unfounded character provid-
ing support for another unfounded character (circulus in probando), i.e., prem-
ise (p)1 [presence of hypothesized epidermal collar (EC)] is used to prove p2
(EC, is elliptical); p2 is used to prove p3 (EBFF therefore elliptical); p3 would
presumably prove p1, completing the circle (Lingham-Soliar 2010a, b).

Fig. 6.7  EBFFs in Beipiaosaurus. a EBFFs in Beipiaosaurus sp. STM31-1. b Tail of the B.

inexpectus holotype (Xu et al. 2009, Fig. 1B, C). Unfortunately, the fibers are poorly preserved
and no detail is evident. Scale bars a 15 mm, b 10.5 mm. After Lingham-Soliar (2010a, b) from
an original figure by Xu et al. (2009), courtesy of MacMillan Press Ltd
276 6  Integumental Taphonomy

(2) Xu et al. (2009) recognize how important the character of hollowness is in

order to establish affinity of the EBFFs with feathers (as we saw above in
attempts by other authors). Yet, we have another argument that has no scientific
credibility. Xu et al. (2009, p. 833) state, “[b]ecause feathers are essentially
tubular structures, the EBFFs are probably hollow.” This again is textbook
circular reasoning (petitio principii), since the proposition that it is a feather
is being used as proof of its own conclusion (Lingham-Soliar 2010a, b).
But of course there was no proposition or hypothesis from their paragraph 1,
so why prolong the charade?
It is also obvious that taphonomy and histology are of no consequence in their
statements on fossil material over 130 million years old, and that intensive and
contrary investigations as demonstrated above are simply ignored as though they
do not exist, do not matter, let alone deserve mention (see Feduccia (2012) on
censure by omission). The Beipiaosaurus story of yet another “feathered” dino-
saur clearly belonged to a new form of consensus science that required no test-
able evidence at all as evident from the first descriptive sentence on the structures,
“In STM31-1, feathers [my italicization] are preserved along the skull and neck,
and trunk, around the forelimbs.” It might mean having to explain why the EBFFs
cannot be the degraded remains of support structures for a crest, frill or lappet,
given their peripheral condition, known for example in the frills of modern reptiles
(Feduccia et al. 2005; Lingham-Soliar 2010a, b), despite the fact that they pale in
comparison to their “glorious” ancestors.
Xu et al. (2009) state their EBFFs are feathers (from the first paragraph) by
textbook circular arguments—feathers are hollow, therefore EBFFs must be hol-
low, feathers are somewhat flattened, therefore EBFFs must be flattened, feathers
have elliptical epidermal collars therefore based on an imaginary elliptical epider-
mal collar, the EBFFs must be elliptical. Thus if the EBFFs are flattened and hol-
low, and elliptical, they must be feathers.
With this done, Xu et al. (2009, p. 834) go on to unveil their new hypothesis—
the EBFFs are the first filamentous display feathers (Xu et al. 2009, p. 834) and
first unbranched filaments “All reported feathers in nonavian theropods are com-
posite structures formed by multiple slender filaments (1, 5–7), which are mor-
phologically congruent with relatively ADVANCED STAGES [my emphasis] in
feather evolution predicted by recently proposed developmental models of the evo-
lutionary origin of feathers (14, 15).” We will deal with this further in Chap. 7.
On all of three of the most fundamental rules of scientific methodology, i.e.,
transparency of evidence (to make phenomena perceivable by objective means,
e.g., the epidermal collar), logical argumentation, and an attempt to discover
observed exceptions to the postulated rule, i.e., contradictory evidence (the law of
falsifiability) (Popper 1959), Xu et al. (2009) fail to validate their major conclu-
sion concerning the EBFFs, i.e., that they have any affinity with feathers at all.
Notwithstanding, Xu et al. (2009) proceed as though from strength to strength,
“The EBFFs of Beipiaosaurus provide the first evidence supporting the occurrence
of integumentary display using filamentous feathers among nonavian theropods.
Because pennaceous feathers have not been reported in therizinosaurs and more
6.5  Pushing Feathered Dinosaurs into the Mid-Triassic 277

basal coelurosaurian groups, EBFFs are thus inferred to have appeared phyloge-
netically at a more basal point than did feathers of modern aspect. This indicates
that integumentary display using feathers evolved at an earlier stage than flight,
which is associated with pennaceous feather types.” They add, the EBFFs “share
some striking similarities with the filamentous integumentary structures seen in
the ornithischian dinosaur, Psittacosaurus (20) [Mayr et al. (2002), who actually
were at pains to show the filaments “were originally cylindrical],” which charac-
terizes a clade more inclusive than the Coelurosauria, and might “push the origin
of monofilamentous integumentary structures into the Middle Triassic at least.”
Sadly, these highly speculative notions on evolution were published on the 150th
anniversary of Charles Darwin’s Origin of Species.

6.5.2 Psittacosaurus

Given the links Xu et al. (2009) made with Psittacosaurus, it seemed appropriate
to consider some of the points made by Mayr et al. (2002) on the animal espe-
cially with respect to alleged hollowness of the filamentous structures along its
tail. Mayr et al. (2002) proposed that “a dark stripe of varying width along at least
a part of their midline possibly indicated the presence of a hollow lumen inside
these structures.” However, I (Lingham-Soliar 2010a) showed that this hypothe-
sis for a hollow lumen was without substance. A degraded bristle in one area of
their figure seriously undermined the entire notion (Fig. 6.8, single-headed white
arrow within a circle). Here, there is part of a black stripe with no surrounding
material, which in life would have been the material that made up the outer tube
itself. Given the black stripe represents nothingness [Oxford English Dictionary
(OED): an opening, passage, or canal] and can only exist in conjunction with the
solid outer tube, then, with the outer tube degraded, it ceases to exist as a visual
phenomena. Yet it does exist, as we see in Fig. 6.8a (white arrow in circle). “The
“black stripe” clearly represents substance and not an empty space, i.e., nothing-
ness as proposed. The most reasonable explanation for the “black stripe” is some
form of diagenesis, i.e., chemical change to the “bristle” (depending on the chemi-
cals involved and diagenetic pathway, some could proceed from dark to light and
others from light to dark). This also makes a lot more sense with respect to the
varying breadth of the black substance including its granular condition (arrow-
heads) in some of the bristles” (Lingham-Soliar 2010a).
In his response, Mayr (2010) loses focus of the argument on semantics saying
“Lingham-Soliar (2009) [published date print version, 2010a] depicted in the out-
of-focus inset of his Fig. 3 [here Fig. 6.8], the outer tube is not “degraded”, but was
destroyed during preparation.” I answered in my response (Lingham-Soliar 2010b),
“Whatever the agent for the degradation of the bristles, it does not affect the argu-
ment. The end result is that the “outer tube” was degraded or “destroyed” (during
preparation) leaving the inner “black stripe.” The tangibility of the stripe remains
the same regardless of the agent of degradation. To the point that a bristle in the cor-
ner of Fig. 6.8a was entirely black (Lingham-Soliar 2010a), Mayr (2010) attributed
278 6  Integumental Taphonomy

Fig. 6.8  Psittacosaurus SMF 4970, detail of “bristles.” a Dark stripes proposed by Mayr et al.
(2002) to represent hollowness (their large black arrows). In one place, the black stripe lacks the
solid, light-colored surrounding material of the bristle (white arrow in circle). The Adobe Pho-
toshop Eyedropper tool was used to obtain the tonal quality of the dark stripes and surrounding
material of the bristles (tonal boxes on right): (1) darkest part of stripes of Mayr et al. (2002);
(2) darkest part of my “stripe’ at the point of white arrow; (3) surrounding material of bristle,
excluding dark stripe; and (4) matrix. b The long bristle is significantly darker than those on
either side and shows even darker, broad blotches (within circle, off-center) and perhaps several
thin stripes (white arrow). Scale bar 5 mm. (Figure [original] from Mayr et al. (2002) by permis-
sion of Prof. Gerhard Plodowski, Senckenberg Museum, Germany)

this to” a photographic artifact of vignetting, i.e., reduced brightness in the image
periphery. In response (Lingham-Soliar 2010b) another photo was figured showing
an entirely black filament that was not in the corner (here Fig. 6.8b). Mayr’s lumen
notion clearly could not stand up to investigation, even reading between the lines in
Mayr’s (2010) response, “I will not discuss whether a lumen represents a “nothing-
ness” (Lingham-Soliar 2009) or may eventually be filled with organic matter.” This
6.5  Pushing Feathered Dinosaurs into the Mid-Triassic 279

was clearly a half-hearted implication of a different argument and acceptance of

my criticism, i.e., it is not hollow in the present state but was so at an earlier state,
which would now require and even more implausible notion of some sort of subse-
quent injection of each of the hollow bristles with foreign matter. Hardly the most
parsimonious of explanations compared with, e.g., chemical digenesis.
There are many other flaws in Mayr et al.’s (2002) study and response (2010)
which were discussed at length (Lingham-Soliar 2010a, b). One other will be
briefly mentioned here. Mayr et al. (2002) alleged with respect to the chemical
identity of bristles in the ornithischian dinosaur Psittacosaurus, “under ultraviolet
light they show the same fluorescence as the epidermal scales, which indicates that
they might have been keratinized” (without any details of the equipment used or
the wavelengths as excitation sources). They also said that the bristles “exhibit a
completely different texture than the ossified tendons [collagen].” Quite remark-
able in a thin film of preserved carbonaceous material of a 130 MYR fossil that
keratin may be distinguished from collagen by texture! However, in response, I
(Lingham-Soliar 2010a, b,) pointed out that investigations in medical research by
Wu et al. (2004, p. 3221, 2005) using the most sophisticated solid state lasers as
excitation sources showed “that fluorescence from the keratinizing tissue layer
presents the spectral lineshape similar to collagen and elastin” and that “the only
way to distinguish collagen from keratin is histologically.” There was no response
from Mayr (2010) to this point.

6.6 Return to Sinosauropteryx

6.6.1 Rufous-Colored Dinosaur

Earlier we mentioned that there was one exception in papers on Birds are
Dinosaurs, in which modern methods of investigation were used in an attempt to
establish that the integumental structures were protofeathers. This involved a study
by Zhang et al. (2010) who investigated the presence of melanosomes in the integ-
umental structures of certain non-avian dinosaurs and fossil birds (Vinther and
Briggs 2008). However, what was remarkable, was Zhang et al.’s (2010, Fig. 3c)
claim that melanosomes were found embedded inside the integumental structures
of the dinosaur Sinosauropteryx. What made this so potentially pivotal was as
mentioned above Sinosauropteryx’s basal theropod status, i.e., it is considerably
removed phylogenetically from the advanced dromaeosaurs or the troodontids
(James and Pourtless 2009). Melanosomes (a pigment of feathers) if found embed-
ded inside the integumental structures of Sinosauropteryx would be sound evi-
dence that its integumental structures, which are not obviously feathers, are in fact
the elusive primordial feathers. Sinosauropteryx was clearly the singular factor of
the study that made it Nature worthy, a fact emphasized by it alone being singled
out in the paper’s abstract (Zhang et al. 2010), Nature’s editorial (Gee 2010, com-
ments and reference in Chap. 7), and by the extensive media coverage devoted
280 6  Integumental Taphonomy

to color in Sinosauropteryx (e.g., BBC’s Science in Action and The New York
Times). Widespread claims that the integumental structures of Sinosauropteryx are
feather homologues are not new and had provoked a study that was highly critical
of earlier alleged evidence (Lingham-Soliar et al. 2007 and references therein).
Zhang et al. (2010) proposed that in order for the structures to be identified as
melanosomes, they have to be conclusively distinguished from bacteria (a straw man
because this is only one alternative). Nevertheless, before we go to the heart of the
study let us look at the reasoning why the structures found in the rachis cannot be
bacteria. Zhang et al. (2010) refer to the absence of the calamus and proximal part of
some filaments in certain Jehol dinosaurs as evidence that they lacked melanosomes
and that they were not a consequence of bacterial decay, i.e., “[t]here is no reason to
suppose that a film of keratinophilic bacteria would have developed elsewhere over
the surface of the feather, but not on these parts, nor could their absence imply that
these portions were buried in the skin and so escaped bacterial replacement.” This is
terribly flawed reasoning as pointed out (Lingham-Soliar et al. 2011)—the authors
surely cannot question that the calamus possesses structure just because it lacked
melanosomes? In fact it is comprised of one of the toughest biological materials,
β-keratin (see Chap. 5), Hence, if it is accepted that the calamus has structure and it
is missing in certain Jehol dinosaurs, what do Zhang et al. (2010) suggest is respon-
sible for its absence, if not bacteria or other microorganisms? The parsimonious
explanation of why the calamus is missing is that it is closest to the decomposing
body (Lingham-Soliar 2011). Before we consider a viable alternative explanation in
fossil birds and non-avian dinosaurs for this entire question of melanosomes versus
bacteria let us not forget that bacteria are themselves, as all other organic matter,
albeit occasionally preserved, subject to the effects of degradation and consequently
invariably leave little or no trace of their activities, otherwise the consequences
would be disastrous—the earth would be engulfed by bacterial remains. Put simply,
a bacterial film may give evidence of bacterial activity but bacterial activity may not
give evidence of a bacterial film (Lingham-Soliar 2011).
It is worth noting that the burden of proof that the fossilized particles in the
integumental structures of Sinosauropteryx are phaeomelanosomes ultimately
rests with Zhang et al. (2010) and not whether or not counterarguments can prove
the particles represent something else—i.e., proof by default. Yet, that they repre-
sented something else is exactly what was demonstrated (Lingham-Soliar 2011).
A number of similarly faulty arguments was proposed by Zhang et al. (2010)
in favor of melanosomes in Sinosauropteryx (Lingham-Soliar 2011) but the cen-
tral thrust will be briefly mentioned here. This involves the actual identification
and descriptions of phaeomelanosomes and the claim (Zhang et al. 2010) that they
are based on empirical evidence. First, the authors have shown a single image of
alleged melanosomes in an area we are obliged to infer is from what they refer to
as the “dark-colored stripes” in the tail filaments of “chestnut to rufous (reddish-
brown)” hue. The authors’ “Methods summary” on Sinosauropteryx (five lines),
e.g., shows no information on how the conclusion of red and white stripes was
arrived at (space constraints are no problem in this day and age with ample oppor-
tunity to include exhaustive data online as supplementary information). Judging
from their figure (Zhang et al. 2010, Fig. 3b (inset)), the filaments they depict
6.6  Return to Sinosauropteryx 281

are approximately 2 mm in length allowing potentially about 150–200 sectors of

comparable dimensions to their Fig. 3c for investigation. Yet, besides the section
represented in their Fig. 3c (Zhang et al. 2010; here Fig. 6.9a, b); also see Lingham-
Soliar (2011), there is no evidence of even one other section being examined,
e.g., with even greater constraints with respect to limited material in an ichthyo-
saur, data on 329 D-bands in 38 individual fibrils were collected (Lingham-Soliar
and Wesley-Smith 2008; see Chap. 2)—essential in any attempt to verify a criti-
cal morphological structure. An isolated observation based upon which there are
profound evolutionary ramifications raises serious questions that will be dealt with
in the course of this study. Second, because size and shape are the only physical
properties that Zhang et al. (2010, p. 1077) use to define the structures as melano-
somes, supporting data are imperative. Despite this, the authors merely allude to the

Fig. 6.9  SEM. Reproduced from Zhang et al. (2010) Fig. 3c. a (Lingham-Soliar 2011, reprinted
with permission from Zhang et al. (2010). Copyright Macmillan Publishers, Ltd.). b SEM.
Reproduced from Zhang et al. (2010) Fig. 3c at about 2× the size printed in their article (see
Fig. 13a). In the bottom right, biodegradation of the structures has advanced even further with the
particle size 70–100 nm in diameter. In inset i (arrow shows location), small bead-like structures
in parallel rows are reminiscent of 67 nm D-banding of collagen, e.g., in an ichthyosaur, inset ii
and rat, inset iii. Scale bar 2 µm; insets i 1 µm, ii and iii 0.5 µm
282 6  Integumental Taphonomy

size of the melanosomes as, “most are between 500 and 700 nm long (occasion-
ally up to 900 nm) and 300 and 600 nm wide.” There are no vital, basic statisti-
cal data of measurements, e.g., numbers measured (n) their mean (x) and standard
deviation (SD) or how the ranges were obtained. Hence, it is clearly speculation.
Certainly, there is no record of melanosomes conforming to the highly irregular and
random shapes of the alleged phaeomelanosomes in Sinosauropteryx. Zhang et al.’s
(2010) implication of some form of uniformity of particle shape and size is incor-
rect, which, however, would have made the particles more easily measureable than
they actually are. Nevertheless, despite the obvious difficulties, detailed measure-
ments were made by Lingham-Soliar (2011) that show a mean length of 302.06 nm
(n = 55, SD = 88.18, min = 166.82, max = 571.87) and mean width of 222.6 nm
(n = 55, SD = 74.96, min = 98.9, max = 492.55). These are very different from
Zhang et al.’s (2010) speculations. Third, Zhang et al. (2010) claim to have iden-
tified dark stripes in the integumental structures of Sinosauropteryx but data are
strikingly absent. There are no SEM results for the lighter bands nor even any
indication that they were even tested nor the precise area in the depicted filaments
from which the SEM image came (by either high power optical microscopy or low
power SEM such as), e.g., the use of high- and low power SEMs to contextualise
fibril structure within a collagen fiber (Lingham-Soliar and Wesley-Smith 2008; see
Chap. 2, Fig. 2.27). Their optical microscopic image of the filaments (Zhang et al.
2010, Fig. 3a, b, plus inset) shows minimal information and, in particular, no detail
whatsoever of their external structure nor the alleged color banding. Apparently the
authors imply that because the white filaments lack melanosomes they are not able
to leave trace evidence of their existence in the fossil record. Zhang et al. (2010,
p. 1076) state it “has been shown (Vinther and Briggs 2008, Fig. 1a) that eumela-
nosomes occur only in dark bands of banded FEATHERS [my emphasis], and not
in light bands” (the white bands show no structure). However, that specimen refers
to black and white areas of a single fossil feather found in an entirely different for-
mation in Brazil with no evidence whatsoever to equate it with the integumental
structures in Sinosauropteryx. This is a house of cards. Nevertheless, it is a circular
argument, i.e., the proposition that the filaments in Sinosauropteryx are feathers is
being used as proof of its own conclusion, i.e., it would first have to be shown that
there are striped patterns in Sinosauropteryx before the comparison is made with
feathers from a bird or even a dromaeosaurid or troodontid dinosaur. Furthermore,
it would seem curious that only melanosomes would be preserved in this Jehol ver-
tebrate and not the robust structural protein of feathers, i.e., β-keratin, given that
we know that dermal collagen (identified by its unmistakable multi-layered, geo-
metrically precise architecture in typical alternating right- and left-handed weft), a
less robust protein than keratin, was preserved in, e.g., Psittacosaurus (Lingham-
Soliar 2008, Fig. 2b, c; also see Volume 1), Sinosauropteryx (Lingham-Soliar et al.
2007, Fig. 4) and Xianglong zhaoi, a gliding lizard (as filaments; Li et al. 2007),
all from the same Early Cretaceous Jehol Group of China. Either, crucial evidence
for Zhang et al.’s (2010) proposals for stripes in Sinosauropteryx is not produced or
their stated evidence is that β-keratin per se does not preserve in the Jehol biota ver-
tebrates unless reinforced by melanosomes. This is speculation and not the empiri-
cal evidence Zhang et al. (2010) promised so emphatically.
6.6  Return to Sinosauropteryx 283

On these technical arguments aside, and a number of others that will not be
discussed here (see Lingham-Soliar 2011), the study by Zhang et al. (2010) is far
from convincing on any level of investigation, let alone empirical. However, Zhang
et al.’s (2010, p. 277) arguments do not bear scrutiny at a much more basic level—
the visual observations and conclusions of “ovoid to sub-spherical” structures of
specific shape and size are based on an optical illusion. The image as presented
in their Fig. 3c (here, Fig. 6.9a, b) certainly gives the impression the authors sug-
gest—but only at low image size. However, by no more than doubling the size of
the image as here in Fig. 6.9b (also see Lingham-Soliar 2011), it becomes very
clear that there is a mishmash of indefinable shapes and sizes with only a small
number that could be interpreted as spherical to oblate and conforming to the sizes
mentioned by the authors. In the study (Lingham-Soliar 2011) substantial empiri-
cal evidence was referred to including from ichthyosaur soft tissue studied over
the years and in particular SEM investigations (Lingham-Soliar and Wesley-Smith
2008) and of SEMs of soft-tissue in a number of groups of modern-day verte-
brates. All of these demonstrated that decay of collagen fibers results in globular
structures (Lingham-Soliar 2011; here Fig. 6.10) far more convincing than the
predominantly irregular structures in Zhang et al. (2010, here Fig. 6.9b), despite
different diagenetic processes, i.e., the ‘softer’ phosphatic preservations in the ich-
thyosaur compared to the ‘harder’ carbonaceous images of the Sinosauropteryx.
The strong probability that both materials are collagenous is the identification of

Fig. 6.10  SEM section showing advanced stage in the decomposition of collagen fibers in Ich-
thyosaurus (longitudinal or tangential view of degraded fiber; phosphatic preservation hence
‘softer’ than carbonaceous). Many globular structures show traces of the beaded D-bands of the
basic fibrils (arrows) (see Lingham-Soliar and Wesley-Smith 2008). Lingham-Soliar (2011),
courtesy of Springer, Germany
284 6  Integumental Taphonomy

apparently the collagen D-band structure (a ‘fingerprint’ of collagen) in a corner

of the of the Zhang et al. (2010) image (here Fig. 6.9b, inset a). However, more
investigation is needed (cf. Lingham-Soliar and Wesley-Smith 2008).
As stressed in the paper (Lingham-Soliar 2011) and earlier (Lingham-Soliar
et al. 2007, p. 1823), “It must be emphasized, however, that the present study’s
criticism of phaeomelanosomes in Sinosauropteryx may in no way be construed
as a comment one way or the other of such structures in other non-avian dino-
saurs and fossil birds nor of the hypothesis of the dinosaurian origin of birds.”
What underscores the studies (Lingham-Soliar and colleagues) in the context of
Birds are Dinosaurs rather is the exposure of exceedingly poor scientific procedure
and the derailing of scientific protocol that challenges the very ethos of science
(see Chap. 7). Part of that methodology included the erection of false dichotomies
such as, if the structures are not bacteria they must be melanosomes. That was
compounded by their neglect of one of the most important factors concerning the
material namely the taphonomy of ancient fossilized filaments about 130 million
years old. That the alleged ovoid structures might reasonably represent the decay
products of original organic matter was not given any consideration whatsoever.
Instead readers were blindsided by the false dichotomy—either the structures were
bacteria or they were melanosomes. Further, as demonstrated, they eliminated bac-
teria on the weakest of possible arguments including a disregard for statistical data
(measurements).

6.6.2 Death by Volcano

In a study of a number of Sinosauropteryx specimens (Lingham-Soliar 2012)

I concluded that the death of at least one animal, specimen NIGP 127587 (here
Fig.  6.11), may have occurred as a consequence of volcanic activity associated
with the Jehol Group (Zhou et al. 2003). It was also noted in the study that there
was a noticeably high degree of carbonization associated with the fossil. We will
see in a later study (below) that death as a consequence of volcanic activity is
probably the most viable explanation for the vertebrates of the Jehol biota.
The most significant findings concerns the dermal tissue/structures preserved
over the dorsal surface of Sinosauroptery NIGP 127587. It comprises the greater
part of the external tissue, extending as a continuous band from the head to the tail
(Fig. 6.11). This is quite unmistakable. It shows that the filamentous structures were
internal support fibers that together with the overlying dermal tissue comprised a
composite structure such as an external crest. Furthermore, a large part of this struc-
ture has arched away presumably as a consequence of the large compressive and
tensile forces (Fig. 6.11, white arrows) that occurred during opisthotonus of the tail
and neck, i.e., strong upward and forward curvature of the tail and backward curva-
ture of the neck, and the structure tearing away at its base (Lingham-Soliar 2012).
This is a clearly unified structure consistent with a crest and the above observations
argue against individual feathers or protofeathers. The study also shows preserved in
one specimen of Sinosauropteryx a large spatula-shaped terminal expansion of the
6.6  Return to Sinosauropteryx 285

Fig. 6.11  Sinosauropteryx NIGM 127587. Specimen shows a large amount of externally pre-

served soft tissue (dark gray). The dorsal crest is forced upward by the compression between the
anterior and dorsal spine during opisthotonus, showing that it is a unified structure. Lingham-
Soliar (2012), courtesy of Springer, Germany

Fig. 6.12  Sinosauropteryx sp. GMV 2124. The dorsal edge of the spatula-shaped termination of
the tail shows a remarkably smooth outline. Filaments are preserved within the structure. Inset,
whole fossil. Tail overlaps head and ends at bottom right. Lingham-Soliar (2012)

crest (here Fig. 6.12), which explicitly shows the smooth edge of the membrane. All
the indications are, given the very watery environment (lakes), that Sinosauropteryx
was probably a well-adapted swimmer aided by a powerful tail and a crest that iim-
proved hydrodynamics as in, many modern reptiles (Lingham-Soliar 2012)).
286 6  Integumental Taphonomy

In a subsequent study (Lingham-Soliar 2013) the presence of scales in

Sinosauropteryx IVPP V12415 was demonstrated, some crucially overlying fibers.
The latter as we know had been interpreted by other authors in other similar preserva-
tions as protofeathers. This was described in Volume 1 and will not be repeated here.

6.6.2.1 Ordeal by Fire

A recent study of Sinosauropteryx IVPP V12415 provides the most graphic evi-
dence from the Cretaceous (~130 MYA) of a violent end to an animal during a
volcanic eruption (Lingham-Soliar 2014a), believed to have generally resulted
in the widespread destruction of the Jehol biota (Jiang et al. 2014). It compares
with relatively recent human and animal victims of a similar fate, i.e., from a vol-
canic catastrophe in the ancient Roman cities of Pompeii and Herculaneum. The
information on Sinosauropteryx was obtained from a specimen of the dinosaur
that shows the opisthotonic process (sharp upward recurvatures of neck and tail)
immediately following the animal’s death. The animal is hypothesized to have
been incinerated at temperatures of about 300 °C [cf. Mastrolorenzo et al. (2010)]
resulting in rapid and complete destruction of restraining muscles. The surviving

Fig. 6.13  Sinosauropteryx
IVPP V12415. All confusing
matrix deleted and dinosaur
highlighted by Adobe graphic
pen to show the three stages
of opisthotonus. Lingham-
Soliar (2014a), courtesy of
Springer, Germany
6.6  Return to Sinosauropteryx 287

ligaments in the badly burnt tail (close to the bone) resulted in its contraction and
leaving behind a unique, trail of burnt remains including traces of bone, which
showed the severity of the heat, until it came to rest (Fig. 6.13). This had to have
occurred in minutes because of the intense incineration and not in the usual time
for normal occurrences of opisthotonus. In their detailed investigation of vic-
tims of volcanic pyroclastic surges at Pompeii, Mastrolorenzo et al. (2010) also
reported that most of the groups of the victims display a variety of death postures
from convulsion (contraction of the ligaments).
Of further interest in Mastrolorenzo et al.’s (2010) study, some skeletons at
Herculaneum such as the famous “ringed lady” (on account of a number of gold
rings found with the skeleton) showed a reddish hue of the bones. To discover the
cause, Mastrolorenzo et al. subjected human and equine bones to temperatures up
to 800 °C and found color variations ranging from natural bone color to pale yel-
low to reddish brown. The reddish brown color of the bones of the “ringed lady”
and other specimens occurred at about 300 °C in their tests and are strikingly
similar to expanses of reddish brown color in Sinosauropteryx IVPP V12415. This
adds strong circumstantial evidence against the notion, which earlier had been
soundly refuted on technical grounds (Lingham-Soliar 2011; described briefly
above), that the reddish hue in Sinosauropteryx was a consequence of melanosome
pigmentation in the dinosaur’s alleged feathers (Zhang et al. 2010).

6.7 One Day in the Life of Kulindadromeus Zabaikalicus

Godefroit et al. (2014a p. 451) reported scales and feathers, including “basal
plates,” in an ornithischian dinosaur, Kulindadromeus zabaikalicus from Siberia.
They dismissed the alternative of collagen fibers by straw man arguments. I
refuted (Lingham-Soliar 2014b) the study virtually in its entirety because of a fun-
damental misinterpretation of structural collagen which included a gross underes-
timation of fiber sizes. Such mischaracterizations demonstrated the unfamiliarity
of the authors with tissue histology, particularly with respect to structural fibers,
making their understanding of preserved filaments in a 150 MYR fossil, an unen-
viable task. Two fundamental mischaracterizations were:
(1) “First, integumentary collagen fibers typically occur in layered arrays of
parallel, densely packed fibers where fibers in successive layers are oblique to one
another” (supplementary materials) and, (2) “[I]ntegumentary collagen fibers are
typically on the order of several microns in diameter; the structures we describe
are at least two orders of magnitude larger” (Godefroit et al. 2014a, SM).
Central weaknesses of the study are discussed from my paper (Lingham-Soliar
2014b) and others briefly in response to their Technical Response, which will be
pursued elsewhere in detail (Godefroit et al. 2014b). I was obliged to point out
to the authors that oppositely oriented fibers in layers, “are not typical but form a
highly specialized design architecture associated with special biomechanical func-
tions—for example, enabling stiffness and mobility either of the whole body (2–6)
288 6  Integumental Taphonomy

or of organ systems such as arteries (7), rectal sheaths, and linea alba (8).” The
references in the quote included the specialist design of the cross-fibered archi-
tecture in marine fast swimming vertebrates. They contradict their own argument
in their response (Godefroit et al. 2014b), “Lingham-Soliar compares the size of
the filaments in Kulindadromeus with that of bundles of collagen fibers in marine
tetrapods. The validity of a direct comparison between integumentary collagen in
marine tetrapods and a terrestrial dinosaur is uncertain given the marked differ-
ences in mechanical stresses acting upon the skin in these different animals. Indeed,
Lingham-Soliar and his colleagues showed that the organization of collagen fibers
into thick bundles is linked to high tensile stiffness and efficiency of the locomo-
tory organs in high-speed marine tetrapods (4, 7).” Godefroit et al. (2014b) have
forgotten the fact that it was they who had said that the cross-fiber architecture of
collagen is a TYPICAL pattern (demonstrating a fundamental lack of understand-
ing of structural fibers) and now to add insult to injury they instruct me, despite
the fact that I had to inform them that it is a specialist design, NOT TYPICAL as
they declared, hence my references that included SPECIALIST marine vertebrates
(Lingham-Soliar 2014b). They incorrectly say that I use, “varied filament angles” in
the Kulindadromeus fibers as evidence that they are collagen fiber bundles. While
they agree with this variation, this was not my argument that collagen fibers have to
be oblique but theirs’, which I show is evident in their fossil, whether genuine or an
artifact of preservation, thereby contradicting their argument, not mine (Godefroit
et al. 2014a, b, SM). My argument, which they seem to forget, was that collagen
fibers were not confined to the cross-fiber architecture, which they claimed, but
often occurred in discrete “non-opposing orientations” (Lingham-Soliar 2014b).
They say in their uncompromising, yet ill-informed reply, “there is no taphonomic
or biological mechanism that could explain different modes of preservation of
integumentary features in the tail and in the distal parts of the limbs, versus those in
proximal regions.” This is incorrect because they are not different modes of preser-
vation necessarily but rather different degrees or absence or presence of preserved
tissue that emanate from a multitude of taphonomic factors that are commonly
referred to as the ‘vagaries’ or ‘biases’ of preservation, a complex subject which
cannot be gone into here. However, in this case it is less vague, for one reasonable
explanation among many, which can be found in any standard textbook on taphon-
omy, is that the femur, proximal tibia and fibula and humerus, where the small
scales are more degraded, are closer to the body and gut [see Godefroit et al. 2014a,
Fig. 1 (animal reconstruction)] where degradation is usually severest.
Consistent with their demonstrated mischaracterization of structural fiber
organization and filament sizes in vertebrates, living and extinct (Godefroit et al.
2014a), they also mischaracterize the filamentous structures of Sinosauropteryx,
given they are making comparisons with it, i.e., when they state, “their filaments,
more closely resemble the monofilaments in the basal coelurosaur Sinosauropteryx
(20 [Currie and Chen 2001]).” What Currie and Chen (2001) actually said with
respect to Sinosauropteryx is that the integumentary structures comprise “central
shafts and plumulaceous barbs” and have a “simple branching structure.” So, not
monofilaments then (also see Chap. 7).
6.7  One Day in the Life of Kulindadromeus Zabaikalicus 289

With respect to thickness they are again clearly wrong, ‘several microns’ thick
or as they also put it “at least two orders of magnitude” smaller than their fila-
ments, which they continue to get wrong. Now, having apparently accepted my
correction of their initial error in which they stated the cross-fiber architecture of
collagen is typical (Godefroit et al. 2014a) they now state that the size class of
1 mm thick is found in marine animals and cannot be compared with sizes in their
dinosaur because it is terrestrial. While they fail to understand the principles of the
crossed-fiber system which are the same from worms to whales (see Chap. 1), nev-
ertheless to be generous I shall remove the marine vertebrates from the equation.
They allege that around the humerus filaments are 0.2 to 0.4 mm wide. However,
a paper they attest familiarity with (Feduccia et al. 2005) shows a small agamid
lizard (minute compared to their dinosaur), Agama utricollis, with collagen fib-
ers just under 0.2 mm thick (a great difference from their original understanding
of collagen fibers being just several microns thick and two orders of magnitude
smaller [Godefroit et al. 2014a]), so nothing special in a much larger animal show-
ing some filaments about 0.2–0.4 mm wide. They also seem unaware that around
the ribs for example in many vertebrates including ostriches and horses thick col-
lagen fibers may form braces between ribs, i.e., a kind of Fink truss (Gordon 1978;
see Chap. 1). Varying angled, thick structural fibers are also seen between the ribs
of the Nanjing specimen of Psittacosaurus (Feduccia et al. 2005, Figs. 12 and 13)
(Fig. 6.14).
They describe collagen fibers as very densely packed, abutting fibers and that
in contrast, the simple monofilament structures in Kulindadromeus (at least in one
area) are, “widely spaced, filling only a 30 to 40 % fraction of visible area (2)
[Godefroit et al. (2014a)], e.g., Figure 2I.” This is poor analysis of their own mate-
rial including lack of regard for serious decay and degradation. If they look at the
bottom right of the same figure they will see three filaments without an iota of
space between them, indicating that the alleged spaces are clearly artifacts of pres-
ervation (decay, erosion, etc.).
The authors state (2014b), “[i]t is highly unlikely that Kulindadromeus pos-
sessed similar particularly large muscles [as e.g., in linea alba] in the region of

Fig. 6.14  The ornithischian
dinosaur Psittacosaurus
(Nanjing specimen).
Bands of well-preserved
integumental structures are
seen oriented in two opposing
directions between the ribs
(approximate area 4 × 3 cm),
and between several other
ribs in the specimen.
Modified from Feduccia et al.
(2005)
290 6  Integumental Taphonomy

Fig. 6.15  The tibia of a
1.5 kg chicken, Gallus gallus.
Just a small percentage of
the ribbon-like collagen
fibers are exposed. Note,
each broad ribbon-like strand
is bilaterally divided with
a dark line indicating the
halves. The entire structure
is comprised of thinner
collagen fibers, not seen at
this magnification. Author’s
unpublished data

the tibia, and thus it is unlikely that the ribbon-like structures represent structural
collagen.” While, I do not necessarily state that the fibers are from the tibia (they
could be anything including plant—the authors reference to a personal communi-
cation rejecting this has no scientific data, hence of little scientific value), the read-
ers attentions is drawn to my Fig. 6.15, which shows many ribbon-like fibers in
the tibia of a domestic chicken, Gallus gallus, demonstrating the critical errors the
authors make stemming from poor knowledge of the biology and anatomy of liv-
ing animals (we saw the critical errors in histology and structure). Given such pau-
city of biological knowledge, it is clearly difficult to understand how the authors
can interpret fossilized biological soft tissue, a far more complex task requiring at
the very least a background of basic comparative anatomy.
I will also add just a brief word on the taphonomy, here. I am at a complete
loss as to what the scanning electron microscope picture of the skin in a tiny zebra
finch, Poephila guttata, is meant to represent in the authors argument since it
appears to be a degraded mass which one would expect after 6 months in water.
Rather, most experts propose that exceptional preservation requires obrution (rapid
burial), stagnation, and cyanobacterial coverings (Seilacher et al. 1985), or early
diagenetic mineralization as the principal factor among the complex processes
leading to soft-part preservation (Allison 1988), or even that dehydration may play
a significant role in delaying the decay processes (Lingham-Soliar and Glab 2010).
Hence the significance of Godefroit et al.’s (2014b) rather perplexing, apparently
unpublished bird decomposing ‘experiment’ eludes me. Of course over time (like
6 months under water) no one disputes that feathers (β-keratin) might survive bet-
ter. Also, at least one member of this group of workers (Godefroit et al. 2014a, b)
6.7  One Day in the Life of Kulindadromeus Zabaikalicus 291

proposed in an earlier study on Sinosauropteryx (Zhang et al. 2010) that keratin

did not preserve on its own merits in some of the best known preserved soft tissues
in dinosaurs—when the then objective was trying to establish melanosome pres-
ervation, “[n]otably, those parts of a feather that lack melanosomes, the calamus
and proximal part of the rachis [both comprising β-keratin], are repeatedly absent
in Jehol materials.” Thus we have it that β-keratin per se does not preserve unless
containing melanosomes. Of course, they have ignored any alternative, perhaps
more viable, argument that the calamus and proximal rachis are most vulnerable
to decay because of their proximity to the decomposing body (Lingham-Soliar
2011), yet again demonstrating a poor understanding of taphonomic processes. An
underlying factor of Godefroit et al.’s studies (2014a, b) is that it is based solely
on confirmatory evidence (MacCoun 1998) rather than falsifications that science
demands (Popper 1959).
Next, smaller scales (β-keratin) experience a greater problem in preserva-
tion because they are frequently thin and connected by the much lower modulus,
α-keratin. Being outermost, they are most vulnerable to degradation and attack
by organisms but help protect the underlying collagen in the meantime, which
therefore has the potential to survive longer. But these are complex questions of
taphonomy which cannot be confronted in the rather simplistic way the authors
do, i.e.,—feathers survive better underwater over 6 months than collagen, there-
fore filaments preserved in the fossil record are feathers (as we saw above, if mela-
nosomes are the prevailing notion, then β-keratin does not preserve). Creating a
universal philosophy from a narrow observation is Panglossian (Voltaire 1759)—
we have two legs so that we can wear trousers. By the same argument since ich-
thyosaurs were preserved underwater it would mean the integumental structures
preserved must be feathers (or feathers with melanosomes).
One of the severest criticisms of the study is that the most critical evolution-
ary questions are based on some of the worst preservations and on single-minded
interpretations (including even the astonishing proposal of a new feather mor-
photype) (Godefroit et al. 2014a, b). The preservations are unquestionably bad,
emphasized by the need for highly subjective interpretive drawings on all the crit-
ical issues. I would pre-empt any argument that observations may be more con-
vincing in the actual material—because the objective of science is to communicate
evidence in publications, which you either can do or you cannot. Couple these
shortcomings with a poor demonstrated understanding of the biology of living and
extinct animals as seen in the authors’ discussions whether on the size and struc-
tural architecture of collagen fibers (Godefroit et al. 2014a) or on gross anatomy
of vertebrates and equally poor understanding of taphonomic processes (Godefroit
et al. 2014b) and we have a technically flawed paper that is exacerbated rather
than helped by the authors’ response to my critique (Lingham-Soliar 2014b). Such
flaws prevail in ‘protofeather’ studies and each poor study in ‘primetime’ journals
fuels the next and vice versa (see Chap. 7) perpetuating the myth that the quantity
of such observations versus quality should determine the validity of the hypothesis.
292 6  Integumental Taphonomy

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Chapter 7
The Last Best Hope

7.1 Freedom of Expression

On April 12, 1633, a frail and old man was brought to trial before the Inquisition
in Rome. The man was Galileo Galilei and he was charged with heliocentricity—
of propagating the Copernican idea that the earth moves around the sun, which
was at odds with mainstream thinking. To avoid torture, imprisonment, and even
death he recanted. It is rumored that as he left the court he muttered, “Eppur si
muove”—and yet it does move—unable to betray the truth.
Galileo’s parting line does not correspond to reality—there is no record in the
transcripts (Hofstadter 2009). Rather, he defaulted, as Berthold Brecht portrays
him in his play Galileo—at the moment when what the world needed was one man
to be true to himself, even against the wrath of the world, which was the Catholic
Church at the time. So the myth was created, but why? The reason is fairly sim-
ple, we need to believe Galileo said those words because we would like to believe
it reflects a part of us, and in time (very quickly) we convince ourselves it does,
without any need to uphold those values—honor by default. We will see time and
again below that the reality is considerably different.
In a bold commentary entitled “Science, Truth and Other Values,” Benno
Muller-Hill (1993) pulled no punches in exposing the dishonesty prevalent in
science, especially in some of the highest institutions. He also did not shy away
from the racist ideology of Germany from well before the Second World War and
because of its importance I have cited the whole Passage: “During the Third Reich,
Jews were excluded from science. German scientists were encouraged not to help
them and not even to cite them. Most scientists yielded to that pressure. For exam-
ple, almost all German scientists eagerly accepted offers to become the successors
of their Jewish colleagues who had been fired. The simple acceptance of such offers
in the name of science made them loyal to the regime. Until recently I thought that
there was not a single person who resisted that temptation. I was wrong. Boris

© Springer-Verlag Berlin Heidelberg 2015 295

T. Lingham-Soliar, The Vertebrate Integument Volume 2,
DOI 10.1007/978-3-662-46005-4_7
296 7  The Last Best Hope

Magasanik told me the story of Otto Krayer. Krayer was the associate professor of
physiology in Gottingen. When he got the offer to become the successor to Philipp
Ellinger, a fired Jewish full professor in Düsseldorf, he wrote to the Ministry of
Science on 15 June 1933: “…the primary reason for my reluctance is that I feel
the exclusion of Jewish scientists to be an injustice, the necessity of which I cannot
understand, since it has been justified by reasons that lie outside the domain of sci-
ence…. I therefore prefer to forego this appointment, though it is suited to my incli-
nations and capabilities, rather than having to betray my convictions…” (Goldstein
1987, pp. 153–154). This letter led to Krayer’s firing, and he had to leave Germany.
He died in 1982 as a retired full professor at Harvard Medical School. I have to
repeat, Otto Krayer was the lonely exception. All other German scientists accepted
those jobs vacated by expelled Jews.”
It is a reminder that position or status is not morality by proxy. We will return
to this or something similar, possibly even worse in my own country, toward the
end of the chapter.

7.2 Peer Review

The propagation of ideas in democratic societies as defined by the Universal

Declaration of Human Rights in 1948 is meant to be unfettered, with only very
few exceptions. There is one strong restriction to the freedom of speech (spoken
or written), the “harm principle” (Mill 1859), i.e., protection by law against any
such speech, spoken or in print that causes harm to others. Nevertheless, there is
one other form of restriction to freedom of expression that not only occurs regu-
larly but has a widespread and profound effect on our daily lives and on society.
It concerns the propagation of novel ideas in the arts and sciences, specifically in
the printed medium. Such novel ideas in, e.g., a scientific journal are strictly con-
trolled by the peer review system, i.e., a process by which one’s peers are allowed
to decide whether or not one’s views may be published.
A number of reasons have been suggested as justification for peer censorship in
the sciences. As Elizabeth Wager (2006) noted “[P]eer review provides an impor-
tant veneer of respectability. Findings published in a famous journal take on the
aura of the journal’s reputation.” A generally accepted value of peer review is that
the accuracy, clarity, and correctness of scientific papers tend to improve with care-
ful review by colleagues or editors, although formal evidence on this is rather weak
(Devries et al. 2009). However, an acknowledged downside of the peer review
system concerns conflict of interests between authors, funding bodies, reviewers,
editors and publishing houses, indeed anyone connected with the outcome of a par-
ticular study (Godlee and Dickerson 2003). There are many other negative effects,
e.g., very poor direct knowledge of a specialist field (Resnik et al. 2008), lack of
integrity and honesty and scientific envy (Mahoney 1997; MacCoun 1998; Abate
2008) that should be dealt with within the peer review system and will be discussed
later. Criticism of the peer review system is frequently met with a conformist
7.2  Peer Review 297

approach namely that the peer review system is the best we have. In theory, the
idea that we need a peer review system is not in question here. It is the modus oper-
andi that is of concern. The peer review system is outdated in its rules and in the
power vested in the institutions and people that govern it given the high stakes in
the present day society (Jansen 2011; Feduccia 2012). Above all, it should not be
used as a form of perverse censorship for legitimate ideas that simply do not con-
form to those of a particular group of people (Mahoney 1997). The Deputy Editor
of the British Medical Journal (BMJ), Trish Groves (2006), acknowledges this
in a short but seminal article. Among a number of recommendations to make the
whole peer review and publication process as transparent at the BMJ as possible
she states, “Most important, we use an entirely open peer-review system in which
authors and reviewers know each others’ names and addresses, and reviewers can-
not make separate comments to the editor or easily succumb to bias—for instance
against unknown authors from non-prestigious institutions and/or against women.”
Fiona Godlee (2009), the current Editor of the BMJ, proposes three impor-
tant reasons that may explain why there has been little real change in the struc-
ture of the peer review system in the past 40 years, (1) Conservatism within the
academic community, (2) the deeply entrenched system of credit in science, and
(3) publishers commercial self-interest. In a hard-hitting article Dvoskin (2008)
expressed concern at the “unscientific line of reasoning, the editors at the most
renowned and prestigious of science journals [Nature] have rationalized away the
need to fix an ailing peer-review system.” With respect to the single-blind review
system, Dvoskin refers to the growing amount of evidence “against this lop-
sided method” namely that “knowledge of authors’ identity gender, nationality,
research institution, level of experience in the field can (and does) bias reviewers’
opinions on the merit of the research.” Dvoskin identified one argument in par-
ticular that Nature produced from its own trial of open peer review, which they
concluded a failure, namely, “Non-anonymous reviewers, faced with the prospect
of being held accountable, are less likely to criticize; and submitting authors are
more likely to hold a grudge against a reviewer who rejects their paper, welcom-
ing a later opportunity to retaliate when the tables are turned.” If anything this is
the purest indictment of the subjectivity, lack of professionalism and ethics in the
peer review system that is precisely why serious changes are needed. Anonymity
is by Nature’s self-confession a license for even the wildest criticisms by a ref-
eree without having to be held accountable. Yet, accountability is what defines sci-
ence (more on that below). Who but the author is in a position to do this? Rather
than a “grudge” the first thing an author wants to know is a referee’s suitability
with respect to the subject under study. The naming of referees will discour-
age outlandish, poorly supported, and false statements as well as reviews from
incompetent referees. In an anonymous survey at a British government research
institute 61.8 % claimed to have experienced incompetence by a referee at some
point during peer review and 50.5 % demonstrated that bias was the next most
common problem (Resnik et al. 2008). They recommended that other investiga-
tors follow up on their exploratory research with additional studies on the ethics
of peer review. Harboring a “grudge” or resentment occurs precisely when there
298 7  The Last Best Hope

is a lop-sided view to scientific debate. More specifically, the argument is hope-

lessly out of touch with the twenty-first century. Researchers regularly post on the
World Wide Web, Facebook and at conferences their highly politicized views as
well as hostile statements against their opponents (see below)—not to mention in
their publications. So, clearly personal identification, rather than being avoided,
is flaunted and the whole argument of grudge retaliations as an argument for ano-
nymity in the twenty-first century is rather facile. Furthermore, better to identify
the right person in a “grudge” then guess and “retaliate” at one or more wrong
persons. The entire argument by Nature is Victorian in outlook and holds very lit-
tle logic or substance.
However, many editors (and referees happy to conform) will not welcome
naming their referees for a number of reasons. Foremost, it will expose the high
probability of a small database of regularly used referees who are chosen more
for who they are and frequently ignoring a politicized knowledge of the subject,
rather than for the specialist knowledge needed for a fair and scholarly appraisal
of a new study. Prejudice by referees is potentially disastrous in this hand-in-glove
system of the peer review system with a generally closer (appreciative) relation-
ship between editor and referee than that between the editor and author. This is
exacerbated in journals with little or no protection or redress for an author/s who
wish to challenge a referee’s decision in Science and Nature. For instance, with
respect to an author questioning a rejected ms by Science, they advise: “This is
probably not a good idea” and most requests are not successful. One further objec-
tion to removing referee anonymity might be that most referees provide their time
and expertise gratis and in a sense may have journals “over a barrel.” While this
is true it is not as altruistic as it sounds—it is rather a case of scratching each oth-
er’s back, i.e., science would not function for any of us otherwise—we provide
reviews gratis and receive reviews in return gratis. If we are not prepared to pro-
vide reviews when required to (other than for ethical reasons, etc.), then it is base
to expect others to review our studies. Joan Sieber (2006) reflected a similar atti-
tude, “Reviewing is a lot of pro bono work for a busy professional if done prop-
erly, but it is also a responsibility to the community, a learning experience to keep
up with the field and perhaps a status symbol.” There should be no cost, least of
all in fairness and honesty. Furthermore, the word peer in peer review, should be
taken literally, i.e., to mean equal not better, regardless of geography [a possible
euphemism for race], gender, institution, etc., (Opthof et al. 2002; Goldsmith et al.
2006). There is no doubt that disingenuous referees will withhold their “services”
in attempts to derail the changes proposed, particularly as a reaction against being
named. The publishing world would be well rid of such referees and those editors
who protect them, regardless of their or their institutions’ status. Kirby Lee and
Lisa Bero (2006) proposed an Ombudsman in an Ethics Review Board for appeals
by authors who allege unfair treatment and it is worth noting that prestigious jour-
nals, e.g., the Lancet and BMJ have such a system in place. At stake is the “free
communication of ideas” as laid down by Article 19 of the Universal Declaration
of Human Rights (see Appendix), which is being flouted in scientific publications
with obtuse and obsolete arguments.
7.2  Peer Review 299

The response by editors at the BMJ should be treated as a wake-up call that
all is not well. While the seriousness and immediacy of the problem are clear in
medical research and big corporations such as the pharmaceutical industry, in a
free society vested interests should be outlawed at all levels of publishing. Three
crucial areas of conflict of interest: (1) financial gain, (2) work commitments, and
(3) intellectual and personal matters, in which special steps are needed to assure
that conflicts do not interfere with the responsible practice of research. The need
for disclosure of financial interests has received considerable attention in the medi-
cal and pharmaceutical journals but the latter two proposals far less so. In addition,
it is the authors and not the reviewers that usually are asked to declare their inter-
est as Cooper et al. (2006) found “many more journals have a conflict of interest
policy for authors than they do for peer reviewers and editors.”
Despite commendable recommendations by the Council of Science Editors
(CSE) White Paper (2011). On Promoting Integrity in Scientific Journal Publications
and by the International Council for Science (ICSU) and Committee on Freedom
and Responsibility in the conduct of Science (CFRS) (September 2011), and the
COPE Codes of Conduct for Editors and Publishers, it seems that they have simply
been ignored by most editors and referees. Some of these recommendations are:
(1) Treating all authors with fairness, courtesy, objectivity, and honesty
(2) Establishing and defining policies on conflicts of interest for all involved in
the publication process, including editors, staff (e.g., editorial and sales),
authors, and reviewers
(3) Protecting the confidentiality of every author’s work
(4) Establishing a system for effective and rapid peer review
(5) Making editorial decisions with reasonable speed and communicating them in
a clear and constructive manner
(6) In instances when there are conflicts of interest between reviewers and
authors, editors request that reviewers decline to comment on the manuscript.
(7) Journals should set a low threshold for publishing corrections and protocols
for handling author appeals. Conflicts of interest and bias are not avoid-
able in themselves and need not be avoided provided it is done with integ-
rity (Abate 2008; Goldsmith et al. 2006). Nevertheless, as touched on above
conflict of interest in the medical and pharmaceutical fields can have serious
implications, not least because of connections with billion-dollar industries.
Admittedly, the pharmaceutical and medical industries are connected with
ethical implications that may have a profound impact on society and literally
include matters of life and death. Nevertheless, less obvious ramifications of a
faulty peer review system are much more widespread. Henry Kissinger’s quip
that low stakes were the reason that academic politics are so low is no longer
the case. Today, academic jobs at research universities are highly prized, with
great prestige, high salaries, and more freedom than in almost any other pro-
fession (Feduccia 2012), besides which there is frequently a blurring of the
lines between academic and industrial research. Publications or their lack in
such prestigious journals as Nature, Science, and PNAS can make or break
careers with certain prestigious universities and corporate industries.
300 7  The Last Best Hope

Some of the most intense instances of rivalry and bias in science involves the
social sciences. MacCoun (1998) stated, “[t]he latter half of this century has seen an
erosion in the perceived legitimacy of science as an impartial means of finding truth.
Many research topics are the subject of highly politicized dispute; indeed, the objec-
tivity of the entire discipline of psychology has been called into question.” MacCoun
and Paletz (2009) showed that bias and lack of impartiality was deeply rooted in
society. Citizens, especially those holding conservative beliefs, tended to attribute
studies with liberal findings to the liberalism of the researcher, but citizens were less
likely to attribute conservative findings to the conservatism of the researcher. These
findings tend to reflect the situation in the Birds are Dinosaurs debate both in sci-
entific views and in those of the public as well as those of cross-disciplinary scien-
tists not directly connected with the debate. They also paint a wider picture of how
lack of impartiality in the peer review system is a far greater problem than many are
prepared to accept and may be less sanguine than imagined. Any feeling that bias
might be in the eye of the beholder may be taken with a pinch of salt. Anonymity
has become the scourge of our profession. The purpose here therefore is to dem-
onstrate the urgency for changes to the peer review system as recommended by an
ever-growing number of interested parties. Here, I add to that growing number with
experiences in a field that I am connected with, paleontological research (at least
some areas of the field). The bias and hostility prevalent in the peer review system
came to my notice when I legitimately questioned certain aspects of the “feathered”
dinosaur hypothesis on bird origins, which I felt was my duty as a scientist and
where my expertise on the vertebrate integument and taphonomy led me rather than
being aligned to either side of the argument.

7.3 The Birds are Dinosaurs Debate

One of the most controversial and much sensationalized and politicized subjects
in biology today concerns the evolution of birds. For those readers unfamiliar with
the debate some background is presented (see Feduccia’s Riddle of the Feathered
Dinosaurs (2012) for a detailed discussion on specific issues).
Although there is general agreement that birds are related to theropod dinosaurs
at some level, debate centers on whether birds are derived directly from highly
derived theropod dinosaurs—the popular view—or from an earlier common archo-
saurian ancestor shared by birds and dinosaurs. Recent discoveries from the Early
Cretaceous of China have highlighted the debate, with claims of the discovery of
all stages of feather evolution and ancestral birds (theropod dinosaurs), although
the deposits are at least 25 million years younger (more recent) than those contain-
ing the earliest known bird Archaeopteryx (Feduccia et al. 2005; Feduccia 2012).
However, Anchiornis and Xiaotingia significantly may hold answers to the ‘tem-
poral paradox’ argument in that they are close in age to Archaeopteryx and may in
fact be slightly older (about 161–160 Ma for the fossiliferous Linglongta strata)
(Sullivan et al. 2014).
7.3  The Birds are Dinosaurs Debate 301

The idea that birds originated directly from dinosaurs, indeed that birds are
dinosaurs (BAD, the generally accepted acronym by both sides), is a beguiling and
evocative hypothesis that has received mass support from paleontologists as well
as lay people with a fervor rarely seen in the natural sciences. Thus when a photo-
graph of a Chinese dinosaur fossil unveiled at the annual meeting of the Society of
Vertebrate Paleontology in New York in 1996—showed it sporting a mane of thick
filaments running from neck to tail tip—it could not have been more timely. This
was the small turkey-sized theropod dinosaur, Sinosauropteryx (“Chinese dragon
feather”), which was considered by many of the paleontologists present as the
ultimate support for the theory that birds descended from dinosaurs. Soon after,
without any scientific investigation, a pen-and-ink sketch of the sensational speci-
men appeared on the front page of The New York Times, as support for the theory.
In 1998, a description of Sinosauropteryx appeared in the journal Nature (Chen
et al. 1998). With respect to the dorsal filaments, besides mention of locations,
lengths and photos, there was still no technical analysis of the filaments. It was
the writing on the wall for a new disturbing phase that dinosaur study was mov-
ing into—consensus science. Despite admitting an inability to examine individual
filaments because they are “piled so thick” the authors concluded that the integu-
mentary structures of Sinosauropteryx “suggest that feathers evolved from sim-
pler, branched structures that evolved in non-avian theropod dinosaurs, possibly
for insulation.” On the basis of this visual image of the filament mass it has been
generally accepted by supporters of the theropod origin of birds that the integu-
mental structures in Sinosauropteryx are protofeathers. Although there have been
many so-called feathered dinosaurs since, it is Sinosauropteryx’s basal theropod
status as well as the apparently primitive nature of the alleged feathers that has
made this dinosaur so critical with respect to both bird and feather evolution (see
Chap. 6). As Feduccia (2012) noted, “Birds as ‘living dinosaurs’ is now a corner-
stone of modern paleontological thought. But a consensus is always in danger of
turning into dogma.”
Perhaps the preeminent reasons here for discussing some of the problems of
bird and feather origins, at times in detail, are that it may help expose many of the
general problems in scientific publishing discussed above through the perspective
of this highly polarized subject as featured in influential popular magazines such
as National Geographic and in high-profile scientific journals in the world such as
Science, Nature, and PNAS.

7.3.1 How Did We Sink so Low?

Alan Feduccia (2012) documented some of the outbursts from advocates of the
theropod origin of birds—Mark Norell and Luis Chiappe of the AMNH wrote a
review in Nature (1996) aimed at critics of Birds are Dinosaurs entitled “Flight from
Reason” that was so polemical that paleontologist Peter Dodson of The University
of Pennsylvania, commented “Such a sulfurous heading poisons the well of an
302 7  The Last Best Hope

otherwise respected and responsible journal” (2000); 2 years later again in Nature,
one of its editors, Henry Gee, triumphantly announced “Birds are dinosaurs: the
debate is over” (1998), following a cover article describing two 125-million-year-
old putative dinosaurs, Protarchaeopteryx and Caudipteryx, with true avian feathers
(more will be said below). The mantra was added to by Richard Prum (2002) (now
at Yale University) who wrote, “it is time to abandon debate on the theropod origin
of birds” (we will see some of his dubious tactics in achieving this goal later) and;
paleontologist Christopher Brochu proclaimed in 2001 that the origin of birds from
theropod dinosaurs is “no longer the subject of scholarly dispute” to which Prum in
agreement stated, “current critics of the theropod origin of birds are not doing sci-
ence” (for the references in this paragraph see Feduccia 2012). We will see a more
tangible illustration of what “not doing science” is in Prum and colleagues studies
further on in the chapter.
The self-contradictory threat that you are not doing science if you do not see
what these people insist you ought to, is a reminder of the pair of hoodwinking tai-
lors in Hans Christian Anderson’s satirical short story The Emperor’s New Clothes
in which the shysters promised the emperor a new set of fine clothes that would
be invisible to those too stupid or incompetent to hold office—only one little boy
who had not been indoctrinated cried out while the king was on parade that he was
stark naked (Fig. 7.1).
The present arguments in general concerns ethical questions relating to the
debate on bird origins and evolution seen largely from a personal perspective.
Although I have no strong views on either side of the debate mentioned above, yet,
if I am polarized, it has been forced upon me by an almost complete breakdown of
scientific ethics in those supporters of Birds are Dinosaurs with whom I have had
contact over the years.
In 1999 in a letter to the Vertebrate Paleontology Mailing List (http://vrtpa
[email protected], 17 September, 1999, see Olson 1999), the University of Southern

Fig. 7.1  Hoodwinking
tailors: “Sire, only those
who are too stupid and
incompetent will not see the
fine clothes we have made
for you!” Based on Hans
Christian Andersen’s, The
Emperor’s New Clothes
7.3  The Birds are Dinosaurs Debate 303

California mailing website, with a very wide following (see Feduccia 2012),
Henry Gee, a senior editor at Nature defined his stance with respect to the debate
on the origin of birds.
“I’m surprised that there’s still any argument over bird origins. The point that
seems to have been missed (in more recent postings anyway) is that any hypoth-
esis of phylogeny must be rooted in cladistics. Cladograms don’t give you access to
The Truth, but they are at least the testable hypotheses that science demands. They
do not rest on unsupportable speculations about the possible biological functions
of characters in long-dead creatures. At the moment cladistics suggests that birds
makes their nests among theropods. This is not surprising given the large number
of consistently arrayed features to support this view. This will not be overturned
by notions that Megalancosaurus had a bird-like head, or Longisquama had scales
that looked like feathers (sort of). Cladistics consistently places these animals
well outside dinosaurs and so on current evidence they have nothing to do with
birds. Significantly, those fond of flying Triassic archosaurs aren’t fond of cladis-
tics, either, and prefer to take their science in the form of untestable bedtime stories
rather than rigorous and transparent hypotheses. Yes, the debate is over. There is a
more interesting task ahead than fruitless, stale debates about whether birds and
dinosaurs are closely related. We’ve passed that stage. The task ahead is to resolve
the branching order in the currently dense and tangled part of the cladogram around
Archaeopteryx. Such a resolution will help us understand the order in which birds
acquired their features, so we can build up a picture of the evolution of the fascinat-
ing functional complex that is bird flight. Waffling about ancient lizards falling out
of trees will never do this and should be banished to the entertaining world occu-
pied by Santa Claus, the Tooth Fairy and educational conferences in Kansas.”
The above letter is a defining moment in the downward spiral of Nature’s
attitude toward any questioning related to the subject of Birds are Dinosaurs.
Gee’s above letter was in response to a highly critical open letter that Storrs
Olson, Curator of Birds (now Emeritus Curator) at The National Museum of
Natural History and one of the most eminent ornithologists in the world, had
written in 1999 to Peter Raven, then chairman of the Committee of Research
and Development for National Geographic. Gee’s statement ‘the debate is over’
(Feduccia 2012) as far as the pages of Nature are concerned received a strong
rebuttal from Storrs Olson (1999), “[w]hy should I, who have spent 30 years
collecting, identifying, and describing fossil birds, seek you out to discuss your
views? You, and apparently everyone else at NATURE, seem to have overlooked
the fact that you are not supposed to HAVE a view?” This must be seen in the light
that Henry Gee is a professional editor, not a working scientist or even working
scientist editor.
Gee’s remarks are pure censorship—the suppression or attempted suppression of
something regarded as objectionable and clearly demonstrates his intentionality and
motivation of bias (MacCoun 1998). Along with the purple prose, Henry Gee’s remarks
as an editor of arguably the most prestigious and influential science journal in the world,
can only be thought to have had a detrimental effect on how young scientists around the
world perceive science, and what is fair and what is not. Nevertheless, my intention is
304 7  The Last Best Hope

Fig. 7.2  Hatter (irritated): “Not the same thing a bit! Why, to say Cladistics is Science, is not the
same thing at all as saying Science is Cladistics!” Adapted from Lewis Carroll’s Alice in Won-
derland (1865)

where possible to move away from the polemics to the science and to question Gee’s
interpretations of cladistics (a discipline I am familiar with as a “working scientist” i.e.
when I was involved in taxonomy (e.g., Lingham-Soliar 1992)), and the notion that it
is synonymous with science. The latter strident indoctrination by adherents of Birds
are Dinosaurs was satirized by geneticist John Avise (2007) through some of Lewis
Carroll’s characters in an article entitled Cladists in Wonderland in which, as here, cari-
cature and wit are used in an attempt to bring about improvement in society, an artistic
form going at least as far back as Aristophanes (Fig. 7.2).
7.3  The Birds are Dinosaurs Debate 305

In the above excerpt, one needs to understand why Henry Gee shifted the focus
from biological investigations to taxonomic, “[c]ladograms …are at least the test-
able hypotheses that science demands.” Similar comments were made by Kevin
Padian who stated in 2000 shortly after Gee’s outbursts above (see Feduccia 2012,
p. 10) that cladistics “is fully accepted by the scientific community” and that the
cladistics method is endorsed by the National Science Foundation, major peer
reviewed journals and “the majority of experts” and therefore criticisms of the
bird–dino hypothesis “ceased to be science more than a decade ago.” Cladistics is
not on trial so why was the debate reduced to this simplistic argument that labeled
opponents as “anti birds are dinosaurs”, “anti cladistics” as “unscientific” given
that the definition of what is scientific or unscientific has never been defined in this
way before. Let us look at how science is defined.

7.3.2 Science and the Falsifiability Criterion

Professor Sir Karl Popper, described by Nobel laureate, Peter Medawar (1980;
also see Mulkay and Gilbert 1981) as “incomparably the greatest philosopher of
science”, proposed (e.g., Popper 1959, 1972) that testability should be accepted as
a criterion of the scientific character, i.e., a criterion of demarcation between state-
ments that belong to the empirical sciences and that those comprising untestable
statements relegated to metaphysics, e.g., religion. In contrast to metaphysics, sci-
ence (and any discipline within it) is dependent on the criterion of falsifiability and
while cladistics may be science, science is not cladistics despite proclamations by
people such as Gee and Padian (Fig. 7.2).
More to the point, we get an idea of why Gee and Padian and others have
shifted the focus to cladistics as a demarcation of science and not testability.
Henry Gee, in pronouncing Birds are Dinosaurs as the testable hypothesis, has
failed to understand what testability involves, i.e., the criterion of falsifiability,
which in fact without fail they reject in practice in favor of confirmatory bias.
There is not a single instance in the debate supporting the protofeather hypoth-
esis that shows research designed to falsify the findings (Fig. 7.3). They are all
based on verificationist (confirmatory) evidence based on positive results, of which
more will be said later. In fact Henry Gee has shown that he will simply not enter-
tain any critical study in the field in Nature (or even consider for external review).
Olson (1999) in his reply to Gee, remarked, “[p]erhaps manuscripts presenting
data or ideas contrary to your ideas have not been submitted to NATURE in the
past. But do you think that your words have created an environment in which sci-
entists who have such contrary views would now select NATURE as their first
option for presenting their ideas?” Naively, it would seem then, I can confirm
sending a number of papers with reports contrary to Gee’s ideas, but not a single
one was ever sent to external review. Those studies were subsequently published
by other leading journals and consistently demonstrated that certain characters
considered unique to theropod dinosaurs are in fact found in a host of unrelated
306 7  The Last Best Hope

Fig. 7.3  Tweedledum
(confidently): “If it ain’t
Cladistics it ain’t Science,
nohow.” Tweedledee:
“Contrariwise. If it ain’t
falsified it ain’t SCIENCE. If
it was so, it might be; and if
it were so, it would be; but as
it isn’t, it ain’t. That’s logic!
Recall it?” Tweedledum
(meekly): “Oh, yeah.” Text
modified from Through the
looking glass (Carroll 1871)
and image redrawn from
Tim Burton’s film Alice in
Wonderland (Disney 2010)

animals, e.g. , ichthyosaurs and dolphins (Lingham-Soliar 2003a, b; Lingham-

Soliar et al. 2007), i.e., findings that falsify the hypothesis. We will see the irony of
this through Gee’s own actions later on.
Mahoney (1997) pointed out that the ironic feature of confirmatory bias is the
fact that it is fundamentally illogical. Positive-result and negative-result experi-
ments are not equivalent in their logical implications. Numerous authors have
shown that it is not positive confirmation of a hypothesis but only negative-result
(contrary-to-prediction) experiments that carry logical implications (cf. Popper
1972; Mahoney 1977) (Fig. 7.3). Despite this clear mandate for logic, paleonto-
logical publications supported by Gee at Nature continue in their verificationist
tradition and their appeal to popular science (see Bacon 1621).
A rigorous study on decomposing dolphin tissue, which received global attention
(Lingham-Soliar 2003b; one of the papers sent to Nature and rejected immediately
at internal review) demonstrated frayed feather-like structures of the dermis that fal-
sify the protofeather hypothesis. On publication it was rejected out-of-hand by Mark
Norell (2005, p. 233) curator of dinosaurs at the AMNH, one of the many supporter
of the dinosaurian origin of birds. Quite bizarrely, he dismissed as “flawed” evidence
the findings that collagen fibers (Lingham-Soliar 2003b) showed virtually iden-
tical appearance to the alleged protofeathers in dinosaurs. His argument was, “the
sort of collagen fibers found in the dolphin are associated with aquatic skin types”
(Norell 2005, p. 233). Yet, any worker familiar with collagen will know that there is
no such thing as “aquatic skin type” collagen. The type 1 collagen found in dolphins
(Pabst 1996) is a dominant protein of most vertebrates, found in, e.g., shrews to ele-
phants, in fish (Lingham-Soliar 2005a, b), extant terrestrial reptiles (Feduccia et al.
2005), extinct marine reptiles (Lingham-Soliar and Wesley-Smith 2008) and birds
7.3  The Birds are Dinosaurs Debate 307

(Stettenheim 2000) to name just a few groups of animals. Ironically, Mark Norell is a
curator associated with vertebrates in one of the great museums of the world. To add
to the irony, dolphins are only secondarily aquatic (see Volume 1 and Chaps. 1 and 2,
here), i.e., they are marine mammals that are terrestrial in origin—in geological time
relatively recently. Hence, dolphins are constrained even in gross levels of biology
by a terrestrial physiology (air-breathing, live birth), behavior (pods, parental care),
and biomechanics (e.g., vertical fluke movements associated with a terrestrially
adapted spinal column), etc., let alone in finer structure such as collagen type. Yet,
one can reasonably speculate if Dr. Norell were to have been a referee of my paper
(Lingham-Soliar 2003b) he would have dismissed it on the basis of his highly flawed
reasoning above. Benno Muller-Hill (1993) pointed out in numerous examples,
the unevenness of the playing field when individuals from lesser institutions have
to compete with those from higher ones. He warned of two Max Planck Institutes,
which, “were not as good as they pretended to be, and yet they were likely to destroy
competitive university research if their growth went unchecked.” Many editors are
blindsided by the status of referees to the real problems, e.g., in the case of Norell
(2005), a deeply flawed knowledge of tissue histology (Feduccia et al. 2005). We
saw this exact failing in the latest allegations of feathers in a Siberian dinosaur
(Godefroit et al. 2014a, b; see Chap. 6). Yet, rejection is made time and again by such
powerful people who sit on numerous editorial boards on the flimsiest of arguments
or of a constant widening of the goalposts. To add insult to injury they then state that
most scientists support their view, which ironically dominates “primetime” maga-
zines. The regime in apartheid South Africa also said that most people in the country
supported its ideology—the fact that most opponents were prevented a voice seemed
a tiny, insignificant detail not worth considering. Again, Benno Muller-Hill, “[a]t pre-
sent most of the manuscripts coming from my own laboratory [Institut für Genetik
der Universität zu Köln] are rejected when they are submitted to a journal for the first
time. When we present in vivo data, the referees want to see in vitro data too. When
we present in vitro data the referees want either in vivo data or other in vitro data
supplied by techniques that are really not applicable.” Similar to when I presented
to one of the top journals the most revolutionary and explicit images of fiber micro-
structure in the feather via SEMs, a referee asked why I had not done any TEMs (yet,
workers had got the fiber microstructure hopelessly wrong based on TEMs). Another
referee asked why I had not investigated the chemistry of the surrounding matrix.
Another example of Dr. Norell and colleagues idiosyncratic dismissal of nega-
tive evidence is one that has been widely employed by proponents of the dinosau-
rian origin of birds (Currie and Chen 2001; Norell 2005; Norell and Xu 2005; Xu
et al. 2009; Zheng et al. 2009). Norell (2005) says, “…the integumental structures
in the Liaoning animals are clearly not internal and extend far from the body.” The
implication here is that the structures, despite being preserved only as a corona dor-
sally, have to be feathers and not collagen or even keratin support fibers. Yet, rep-
tilian crests and frills are not internal, how can they be since they are for display.
Hence, such structures must invariably be external to the body surface. Dinosaurs
after all were the “glorious reptiles.” Everything including numerous textbooks tells
us that many dinosaurs were adorned with crests and frills, which of course would
308 7  The Last Best Hope

be strengthened by masses of collagen and/or keratin fibers in smaller dinosaurs and

bone in behemoths such as Triceratop. Modern-day reptiles, despite being a poor
and diminished representative of their glorious past, possess all forms of external
adornments, including dorsal frills, head crests, throat flaps, spikes, etc. In theropods
on the other hand frills rather than feathers suddenly becomes an inconvenient idea
not even worthy of mention. These studies are circumscribed by a pervasive men-
tal heuristic dominated by scientific processing via a positive test strategy (Klayman
and Young-Won 1987), whereby hypotheses are tested by exclusively (or primarily)
searching for events or structures that occur when the hypothesis says they should
occur. A classic case is the observations of only those integumental structures that
might support the idea of protofeathers (sort of) by Currie and Chen (2001) while
ignoring or being oblivious to the vast majority of the soft tissue that is unfavorable
to their own view (Lingham-Soliar 2011; see Chap. 6). Some of the filaments found
in the Liaoning fossils may indeed be feathers as, e.g., in the 160 million-year-old
Anchiornis (literally, early bird), whose position as dinosaur or bird is debated (see
e.g., Feduccia 2012), but on which I have no particular view. However, to work on
the assumption that all fossil filaments are protofeathers or feathers, e.g., based on
positive confirmatory bias while rejecting falsifying evidence, is unscientific accord-
ing to Popperian logic.
A detailed analysis published in Proceedings of the Royal Society of London pro-
duced new evidence that the filaments in Sinosauropteryx were probably structural
fibers of the skin and frill rather than protofeathers (Lingham-Soliar et al. 2007). This
was another paper rejected by Nature at the internal review stage. It was well received
by the global scientific community (the BBC, British, French, Chinese and US
press, Nature online and National Geographic). A National Geographic news story
of the paper (Lovgren 2007) included, among others, comments by Kevin Padian (a
former editorial board member of Proceedings of the Royal Society, but not during
my submission) of the University of California, Berkeley who stated “These people
have been flogging the same horse for a long time. It is appalling that Proceedings
B chose to publish this nonsense.” Padian’s style of rhetoric regrettably is not dis-
similar to that of Henry Gee’s. However, within months of that vitriolic response, he
did a complete turnaround more dramatic and sudden than Paul’s conversion on the
road to Damascus. Padian (2007), in his testimony during the Kitzmiller v. Dover
trial (challenge in the US court against a public school district policy that required
the teaching of Intelligent Design (ID)—Creationism in wolf’s clothing) stated, “The
first occurrence of protofeathers is not entirely clear. Recent reexamination of the skin
of Sinosauropteryx (Lingham-Soliar et al. 2007), a relative of Compsagnathus, indi-
cates fossil structures originally thought to be protofeathers are more characteristic of
collagen fibers.” On the basis of this, Padian (2007) excluded Sinosauropteryx from
his accompanying cladogram. One may wonder about Dr. Padian’s dramatic change
of heart in the space of just a few months with this new, evenly tempered analysis
compared to, “It is appalling that Proceedings B chose to publish this nonsense.” Was
this because evolution was in the spotlight and he wished to show how balanced and
rational evolutionary theory is and that internal criticisms (i.e., falsifying evidence)
rather than weakening it, are the very ethos of science—in striking contrast to ID?
7.3  The Birds are Dinosaurs Debate 309

Does he really thinks that Creationists are so naïve, even stupid, that they don’t read
the papers on bird and feather origins, attend the conferences or follow, e.g., his and
Henry Gee’s and the entire tribe’s highly biased and unscientific outbursts on, e.g.,
National Geographic websites (Lovgren 2007, see reference in National Geographic
website) and virtually everywhere else—and that they swallow this charade he puts
up for them but that in reality the dogma and hypocrisy of his sermonizing is no
better (perhaps worse) than that of the Creationists? One can see why Storrs Olson
labeled Padian years earlier, the Elmer Gantry (a hypocritical preacher in the film of
the same name) of paleontology (Feduccia 2012).
Jonathan Wells, a Creationist with a Ph.D. in religious studies from Yale and a
second doctorate in molecular and cell biology from Berkeley (so no slouch when
it comes to science), had written about the fiasco in which scientists at a symposium
(Graves Symposium) had claimed to have extracted DNA from Triceratops that was
similar to turkey DNA—which as it turned out was turkey DNA, i.e., a contamina-
tion. Wells, given the Triceratops DNA Fiasco, singled out Kevin Padian, who had
preached on what is and is not science (in a nutshell that science is cladistics), came
away from the Graves Symposium and wrote, “This isn’t science. This isn’t even
myth. This is comic relief” (Feduccia 2012). While there are many scientists, myself
included, who rightly fight against the idea of Creation or ID being taught in schools
(a growing problem in South Africa), people like Dr. Padian with their reduction of
science to evangelical preaching and biblical-like hell and damnation for nonbeliev-
ers, make that task increasingly hard. If Padian’s born-again balanced view (Padian
2007) is only to be exhibited on show for the sake of the Creationists, then in reality
Dr. Padian’s dogmatic opinions as a person of influence can serve as proxy for us
to be less sanguine about the current state of the peer review system in the hands of
such privileged individuals. It is an urgent domain for equality to conquer so that the
sole boundaries to progress are the limits to human capacities to think clearly and to
promulgate those thoughts coherently (Dunn 2005).
Gee’s pronouncement “the debate is over” on issues related to the origin of birds
and feathers from dinosaurs should logically mean that this does not refer to just nega-
tive or falsifying evidence but to confirmatory evidence as well. In Gee’s own words,
[t]here is a more interesting task ahead than fruitless, stale debates about whether
birds and dinosaurs are closely related. We have passed that stage. The task ahead is
to resolve the branching order in the currently dense and tangled part of the cladogram
around Archaeopteryx.” Yet, 10 years later (Nature, 25th February 2010) Gee could
hardly contain his euphoria in his Editor’s Summary regarding a paper (Zhang et al.
2010) in which the authors claimed to have identified melanosomes in filaments of
the dinosaur Sinosauropteryx, as he declares “[b]ut it has been suggested that some
of the structures that are not obviously feathers might actually be strands of collagen
from under the skin. Zhang et al. refute this notion [the perpetrators of that “notion”
are as Zhang et al. cite in the papers summary, Lingham-Soliar (2003a, b), Feduccia
et al. (2005) and Lingham-Soliar et al. (2007)] by demonstrating the presence in
these structures of melanosomes— the characteristic bodies that give feathers their
colors. Not only do they show that the feather-like structures of dinosaurs such as
Sinosauropteryx really are akin to feathers, but also they can speculate in an informed
310 7  The Last Best Hope

way about their color.” Clearly, the debate is not over when confirmatory ideas
(Zhang et al. 2010) in support of the old notion of protofeathers in Sinosauropteryx
(Chen et al. 1998) apparently surfaces despite, in Gee’s own words, “[w]e’ve passed
that stage.” Thus, “the debate is over” on this exact topic, namely Sinosauropteryx’s
status as a feathered dinosaur, only when falsifying evidence is presented against
protofeathers. Not only is it contrary to the testability criterion of science, which clad-
istics according to its text-book methodology is meant to embody by his own admis-
sions in the pages of Nature have moved past debating the question of feathers in
dinosaurs. Nevertheless, what of the question of melanosomes allegedly discovered
in Sinosauropteryx? As polarized as Nature’s stance may be, can there be at least
some level of justification for Gee’s (2010) euphoric editorial, i.e., if the finding of
melanosomes is correct then the filaments are indeed protofeathers? Alas, it seems
not as we discovered in Chap. 6—the notion of melanosomes in the filaments of
Sinosauropteryx was shown to be “without scientific merit” (Lingham-Soliar 2011).

7.3.3 Birds are Dinosaurs and Cladistics

Let us look at claims we met earlier that if one is not doing cladistics one is not
doing science. The cladogram is a branching diagram of classification based on
phylogenetic relationships and the evolutionary history of groups of organisms
(see Volume 1 for a brief history). The testability referred to concerns the analyses
of characters whether it is for taxonomic reasons or purely biological. Analyses in
paleontology, as opposed to neontology, are based almost exclusively on very lim-
ited external morphological characters, virtually restricted to bone morphology,
which to make matters worse are fossilized and frequently over hundreds of mil-
lions of years old and poorly preserved. Understanding fossilized tissue requires a
more than sound knowledge of tissue histology in living vertebrates. We will look
at these problems. One of the crucial problems of cladistics involves distinguishing
homologous characters, those with a similar evolutionary history, from those that
are analogous, i.e., similar in appearance and function but with a different evolu-
tionary history (convergent evolution, a common phenomenon). This problem was
of great concern to Willi Hennig (1966), the father of Cladistics or Phylogenetic
Systematics, particularly when attempting to interpret characters restricted to fossil
bones. Thus, in a field where evidence and data is needed most, given such char-
acter restrictions, as Dobson (2000) notes, from stratigraphy, embryology, ecology,
and biogeography that could otherwise be employed to bring maximum evolutionary
coherence to biological data, cladistics systematically excludes.
As we saw in Volume 1, the serious problems of cladistics was in determining
true homologous characters from those arising through convergent evolution. James
and Pourtless IV (2009 and references therein) in a major cladistics’ analysis on the
origin of birds recently attested, “Primary homology statements that are not inde-
pendently testable, when used as characters and later regarded as corroborated state-
ments of secondary homology (i.e., synapomorphies), can be misleading. If the data
7.3  The Birds are Dinosaurs Debate 311

are ambiguous, they lead to unjustified confidence in the phylogeny. Given such
anticipated problems eminent biologists such as Erik Jarvik (see Volume 1) and
Ernst Mayr, a major contributor to the neo-Darwinian synthesis, were unable to rec-
oncile themselves with cladistics systematics. In Mayr’s (1982) book The Growth of
Biological Thought the concept of the uniqueness of biological individuals makes it
clear how difficult it is to delineate animal characters even within species and how
seriously exacerbated it would be when restricted to purely osteological distinctions
alone. As Alan Feduccia (2012) notes because of Ernst Mayr’s drawing attention to
such pitfalls he was defamed by supporters of cladistics and the dinosaurian origin
of birds in a manner reminiscent of Lysenkoism in the Soviet Union. We also saw
in Volume 1 how Erik Jarvik had been the butt of the attack by the cladists in the
search for tetrapod ancestors and was scathingly blamed for a failure to see lungfish
relationships developed directly from comparisons among living gnathostomes with-
out as they put it “interruption by futile paleontological searches for ancestors” and
delaying the solution to the problem by decades (Gardiner et al. 1979). Pertinently,
Jarvik (1981) retaliated by pinpointing the problem that has been the Achilles heel
of cladistics, he accused the cladists of arbitrarily picking out unreliable characters
from a list without checking their reliability…’’ Jarvik had put his finger on the pulse
and in that single sentence overturned the nonsense that cladistics per se is science,
let alone science is cladistics (Fig. 7.2). As it turned out Jarvik was subsequently
shown to have been right and the cladists at the time, who were highly critical of
him, wrong, something considerably downplayed today (see origin of tetrapods in
Volume 1). This underscores the fact that cladistics per se is not the sacred cow of
science but that its reliability depends, on how the characters that ultimately decides
the accuracy (or not) of the cladogram are tested, whether by positive confirmation
or by falsification (Fig. 7.3).
Thus, we see that the cladogram that Gee, Padian, and others promote as the only
true science actually fails to take account of the fundamental tenet of what it, along
with any other taxonomic methodologies or any other scientific disciplines gener-
ally, entail—the falsifiability criterion. The testability of cladistics lies as we have
seen in the careful analyses of the characters, exactly what Jarvik had pointed out.
Before that analysis, the characters must be determined by morphology, anatomy,
biochemistry, biomechanics molecular biology, etc., i.e., nothing whatsoever to do
with cladistics per se. The cladogram hinges on the validity of the characters, which
in paleontology as we must constantly be reminded, Willi Hennig warned, is among
the hardest to determine. If as Gee and Padian claim it is a testable hypothesis then
by that very statement the characters are refutable (Popper 1959). Yet, when pre-
sented with any criticism of the validity of a character, it has usually been dismissed,
often with the comment that no more parsimonious alternative has been presented
with cladistic methodology, which of course is not true (James and Pourtless 2009).
To take one powerful alleged line of support for the theropod origin of birds namely
Caudipteryx, Maryanska et al. (2002) in an exhaustive cladistic analysis showed that
rather than a theropod dinosaur as proposed by some cladistics studies, Caudipteryx
is a flightless bird. This finding remains undisputed.
312 7  The Last Best Hope

James and Pourtless (2009) investigated the hypothesis that birds are manirap-
toran theropod dinosaurs (the “BMT hypothesis”) because of its wide acceptance
by both paleontologists and the general public and given that criticism has usually
been dismissed, as they say, often with the comment that no more parsimonious
alternative has been presented with cladistic methodology. Their character matrix
included taxa from throughout the Archosauria. When the ambiguous characters
were excluded, parsimony analyses with bootstrapping and successive pruning
retrieved a weak clade of birds and core maniraptorans (oviraptorosaurs, troodontids,
and dromaeosaurs) that also contained the early archosaur Longisquama and was
not unambiguously associated with other theropods. When the ambiguous charac-
ters were included but coded as unknown where appropriate, the results were virtu-
ally identical. Kishino-Hasegawa tests revealed no statistical difference between the
hypothesis that birds were a clade nested within the Maniraptora and the hypothesis
that core clades of Maniraptora were actually flying and flightless radiations within
the clade bracketed by Archaeopteryx and modern birds (Aves). Additional statistical
tests showed that both the “early archosaur” and “crocodylomorph” hypotheses are
at least as well supported as the BMT hypothesis (Fig. 7.4).
These results show that Theropoda as presently constituted may not be mono-
phyletic and that the verificationist approach of the BMT literature may be produc-
ing misleading studies on the origin of birds. Further research they believe should
focus on whether some maniraptorans belong within Aves, and whether Aves
belongs within Theropoda or is more closely related to another archosaurian taxon.
The authors (James and Pourtless 2009) note that at present, uncertainties about the
hypothesis that birds are maniraptoran theropods are not receiving enough attention.
While this is a powerful indictment on the assertions by Gee and Padian and
others in like vane it also exposes a philosophy of science by default, i.e., that it is

Fig. 7.4  Origin of Birds. If
core maniraptoran theropod
dinosaurs (Dromaeosauridae,
Troodontidae, and
Oviraptorosauria) were
actually flying and flightless
birds that were more derived
toward modern birds than
Archaeopteryx, then the
hypothesis that birds are
maniraptoran theropod
dinosaurs would lose most of
its current support, and the
origin of birds would have to
be evaluated in the light of at
least four other hypotheses
(see Fig. 3, p. 6 in James and
Pourtless 2009). Figure used
by permission of James and
Pourtless (2009)
7.3  The Birds are Dinosaurs Debate 313

perfectly acceptable to make grand, even outrageous claims when all that is required
by the authors is that they counter any criticism by saying, “Prove it is not.” Thus the
burden of science is shifted to anyone who dares to question a statement, however,
incredulous and ridiculous and lacking in basic scientific procedure it may be. This
is exactly the way for instance the protofeather notion is dealt with by proponents
of Birds are Dinosaurs,” i.e., “prove it is not.” Ridiculous? Yet it is exactly what a
referee of one of my papers said, who for the sake of publishing protocol (confiden-
tiality) both he and the editor must remain anonymous here. He states, “It is use-
less to remind him [Lingham-Soliar] that there are actually tests by which one can
recognize and distinguish keratin from collagen even in fossil organisms.” Note,
the rare claim of being able to distinguish β-keratin by immunological reactivity in
feather-like structures (Schweitzer et al. 1999) is highly questionable, particularly
with respect to distinguishing α-keratin from β-keratin and it has not been recog-
nized as a legitimate technique since. But, this aside, the theory that these structures
are feathers, hence β-keratin, requires tests by supporters of Birds are Dinosaurs and
not pointing of the finger at critics. Yet, in not a single dinosaur species from the
Chinese Jehol biota was a single such alleged test done. The only ‘test’ was based on
a wholly unsupported speculation made by Mayr et al. (2002) that keratin could be
distinguished from collagen by shining an ultraviolet lamp (with no specifications)
on the fossilized material, which as we saw in Chap. 6 was shown to be impossi-
ble by medical researchers using the most sophisticated solid state lasers as excita-
tion sources. Ironically, according to other supporters of Birds are Dinosaurs (Zhang
et al. 2010), keratin does not preserve in the Jehol biota, only melanosomes or mela-
nosome-reinforced β-keratin (Chap. 6).
The integrity of this same reviewer can immediately be assessed in the open-
ing sentence of his review, with an attack on the author (argumentum ad hominem)
rather than reviewing the manuscript, “The author of this paper might be taken more
seriously if he did not show such contempt for all other work done on the subject,
if he did not ignore all other lines of evidence that he pretends his particular inves-
tigation is overthrowing, and if he did not appear so injured by the refusal of the
scientific community to recognize his genius.” This apoplectic attack is for no other
reason than that I oppose poor science which happens to be in support of alleged
protofeathers (my Ph.D. advisor, Beverly Halstead, would say, when people stoop
that low, you know you have won). That this was a personal assault did not concern
the referee and shamefully was wholly supported by the editor-in-chief of a nota-
ble US biological/science journal, with the words, “referees are only human.” So
was Jack the Ripper! The referee’s ranting goes from the ridiculous to the infinitely
ridiculous which I shall not mention any further here except to say that this type of
tirade of abuse and false statements by referees is the rule rather than the exception
when it comes to anyone who dares criticize flawed studies by Birds Are Dinosaurs
(Fig.  7.5). This is in complete violation of the CSE recommendation with respect
to responsibilities by editors and referee in Nonfinancial Conflict of Interests: “A
reviewer with strong feelings on a controversial topic might be partial to or biased
against a manuscript on the topic and want to publish or reject it regardless of scien-
tific merit.” We will see this in more explicit examples further on.
314 7  The Last Best Hope

Fig. 7.5  Stayne, knave of hearts (cowed, holding out something squiggly around his finger):
“Your Majesty, Alice says it’s not a feather (Red Queen slaps him. Stayne faltering) … and it’s
not red.” The Red Queen (slapping Stayne again, apoplectic): “Off with her head!” Redrawn and
rewritten from Tim Burton’s film Alice in Wonderland (Disney 2010)

7.3.4 “Prime Time” Journals: Does the Bite Match

the Bark?

Concern regarding poor quality of refereeing had been noted by a number of

editors (Devries et al. 2009; Godlee et al. 1998) but the Birds are Dinosaurs
debate must surely introduce a new low to the problems. Add bias and sim-
ple incompetence, particularly in controversial topics, and we have not just an
ailing peer review system (Dvoskin 2008), but one that is on the way to the
crematorium.
The impact factor of journals such as Nature and Science is used as a
proxy measurement for the quality of the individual articles (Jansen 2011).
Unfortunately, journals such as Science and Nature have a simple three-fold
policy—of rejection, request for revision based on reviews, and acceptance
­
(Godlee 2009)—certainly inadequate in today’s world of intense scientific com-
petition. In other words if the decision by the journal editor of these journals is
to reject the manuscript, there is very little come back for an author. On the other
hand if the quality of refereeing is of clearly a very high standard and demonstra-
bly impartial and honest with accepted papers going through rigorous critiques
then, perhaps, we can rest a little easy. One has the distinct feeling that in this field
referees recommendations are regarded as sacrosanct, and that this may be more
due to referee status than refereeing ability or impartiality. We will look at this in
the next section.
7.4  COPE’s Proposals on Fraud in Science 315

7.4 COPE’s Proposals on Fraud in Science

Of great concern in the scientific publication process is the serious question of fraud.
The COPE Report (1999) in an article on Coping with Fraud made specific refer-
ence to “Intention[al] distortion of the research process by fabrication of data, text,
hypothesis, or methods from another researcher’s manuscript form or publication.”
The operative word is ‘intention,’ i.e., intention to deceive, rather than unintentional
or accidental. These are legalistic issues that cannot be decided here. However, in
the examples presented below, the readers must decide in their own minds whether
or not there was intentional distortion of the research process for scientific gain or
credibility of a major and/or controversial hypothesis. In fairness, the reader must
also decide whether or not the misrepresented data are either so ambiguous or “lost
in translation” or as part of long, turgid papers, or in an obscure publication that they
could have genuinely been overlooked or misquoted—not just by the author/s but
by all persons (referees, editors) involved in the articles publication. In the cases
presented here involving evolutionary theory, it goes beyond the ordinary, i.e., of
science as a part of society—it is the very heart of our society because it involves
the legitimacy of our arguments and justifications for maintaining secular democ-
racies, which was one of the founding principles of the American Revolution and
the French Revolution. The demise of tolerance for contradictory views in evolution-
ary studies (frequently better supported by evidence), reduces evolutionary theory to
metaphysics and is the greatest threat to the secular state (hence why Kevin Padian
put on a very different show in the Kitzmiller v. Dover trial above, rather than his
usual intolerance). The insincerity will not go unnoticed by Creationists. Evolution,
like Caesar’s wife, must be above suspicion.

7.4.1 Should the Status of the Institution or Individual

Make Fraud More Palatable?

Richard Millhous Nixon when asked by British TV producer David Frost why
he considered that his actions (Watergate break-ins) were not illegal, answered,
“When the President does it, that means that it is not illegal.” Yet, we may brand
him, albeit rightly, but let us not forget that he simply voiced, if somewhat naively,
a philosophy held by many powerful people whether in politics, commerce or
science (we are/should be interested in the latter). However, while it was a dark
moment for any of us who value the ideals of Western Democracies, there was a
shining ray of hope—the illegalities were exposed by a free press (The Washington
Post), Abraham Lincoln’s (1863) “last best hope” (Parrish and Dent 1993). Yet,
where else is a free press more needed and where else should a Nixonian philoso-
phy be purged out off than science?
In a paper in Nature, Xu et al. (2001), refer to a model by one of the paper’s
­coauthors, Richard Prum (1999), which “predicts a transition series of feather mor-
phologies from the first hollow, cylindrical feather through all modern feather
316 7  The Last Best Hope

structural diversity14” (superscripted 14 refers to Prum 1999). Xu et al. further

state that in the present study “The two appendage morphologies observed in
Sinornithosaurus are exactly congruent with the Stage II and Stage IIIa morphologies
predicted by this model.” They add, “Furthermore, the shorter, unbranched integumen-
tal appendages of Sinosauropteryx2, a basal coelurosaur, are also congruent with the
predicted Stage I feather morphology.” Note, the superscripted 2 refers to Chen et al.
(1998) who they cite as making that critical description namely that feather morphol-
ogy in Sinosauropteryx are “UNBRANCHED” [my emphasis] as support for their
model. Given Sinosauropteryx’s basal dinosaur status this is probably the most criti-
cal part of Xu et al.’s (2001) model. However, the reality is that Chen et al. (Nature,
1998, p. 152) said nothing of the kind—quite the opposite. They describe the filamen-
tous structure in Sinosauropteryx quite unambiguously as “MULTIBRANCHED” (my
emphasis) and even in the penultimate line of the paper, the only other place they men-
tion the morphology, they describe them as “branched structures.” Have I exaggerated
the importance of their allegations? First, they are proposing a scientific model, how
much more important can it get? Second, it is not just my stated view but theirs, for
Xu et al. (2001) in the self-same paper endorse the importance of getting these critical
issues right, “Confirmation of the theropod origin of feathers requires documentation
of unambiguously feather-like structures in a clearly non-avian theropod.” If we can-
not get right the crucial issue of whether they are branched or unbranched by falsify-
ing (OED, misrepresent, distort, (a fact, etc.)) another author’s work (see Cope Report
above) to suit a hypothesis/model, then the authors and referees of the paper must
choose, either they are grossly incompetent scientists (“not doing science” in Prum‘s
own words; see above) or they are guilty of serious deception in science. Attention was
drawn to these highly misleading, contradictory statements (Lingham-Soliar 2010,
pp. 194–195) although there has been no subsequent explanation or response of any
kind from the authors. In a subsequent paper (Lingham-Soliar 2011, p. 570), it was
necessary to reaffirm the seriousness of Xu et al.’s (2001) “mischaracterisation” with
the appeal that “[s]uch mischaracterisations of vital characters in a model, no less, of
feather evolution do not engender confidence in this controversial field.” To date, the
authors (Xing Xu, Richard Prum and Zhonghe Zhou) have felt no scientific obligation
to answer (or even apologize for) this mischaracterization. Surely this seriously erodes
the very basis of scientific protocol, accountability? Or is this just another example of
highly placed individuals and institutions being above the rules of science that the rest
of us are bound by—the Nixonian philosophy of being above the law?
The unlikely possibility that the above mischaracterization was accidental (given
it fails to meet some of the possible exonerating conditions mentioned above),
becomes even more unlikely when we examine remarks by Xing Xu and colleagues
(2009) published in PNAS (note, Xing Xu was the same lead author in Xu et al.
(2001, above). In this latest publication they record what they allege is the first single
or unbranched filament congruent with stage 1 of the model—in a nonavian basal
theropod dinosaur Beipiaosaurus. So what of Xu et al.’s (2001) earlier statement
that the filamentous structures in Sinosauropteryx are “unbranched” and conform to
stage 1 of the model (a full 8 years earlier)? Not only did they never apologize for
that “mischaracterization” but, quite astonishingly, it is as if they had never made it
7.4  COPE’s Proposals on Fraud in Science 317

at all. Now they state, “All reported feathers in nonavian theropods are composite
structures formed by multiple slender filaments1, 5−7” and quite astonishingly they
include their earlier paper in the citations of those reports (note, in the latter super-
scripted citations, citation 6 is Xu et al. (2001)). And here is where the waters get
muddier. Xu et al. (2009) now actually cite Xu et al. (2001) as confirmation that
the latest claim (Xu et al. 2009) is a “first” for unbranched feather filaments despite
previously (2001, p. 203) saying that the feather filaments in Sinosauropteryx were
unbranched even to the extent of making a false citation of Chen et al. (1998) to
justify their allegation of support for the stage 1 of their model. Let us be gener-
ous and accord them a further benefit of doubt and ask could they have repented
the false claim (Xu et al. 2001), retracted it in conscience, or even forgotten about
it, or even made it in error in the first instance, given that 8 years had elapsed to the
present claims in PNAS (Xu et al. 2009)? Well, try as one will that does not work
either. For, just months after this latest paper in PNAS (2009), Xing Xu along with
his present PNAS co-author Xiaoting Zheng, published another paper in Nature,
alleging protofeathers in the dinosaur Tianyulong (Zheng et al. 2009, March) in
which they say, “[i]n both Tianyulong and Sinosauropteryx, the filamentous struc-
tures are singular and unbranched.” Yet, 3 months earlier (PNAS January 2009) the
same authors had stated that the filamentous structures in Sinosauropteryx were
branched and 8 years earlier (Xu et al. 2001) that they were unbranched, by mischar-
acterizing 3 years before Chen et al. (1998), who had said they were branched—all
in Nature with the one exception in PNAS. If this endorses one thing, it is that Xu
et al. (2001) have not recanted the false claim throughout the 9 years in support of
a highly important part of their model (Stage 1). The falsifications, as I have shown
all on record, coincide very much with the particular hypothesis at a given time and
its apparent usefulness for “primetime” newsworthiness by a constant changing of
the same character to suit the occasion in the different papers (Fig. 7.6). The most

Fig. 7.6  Humpty Dumpty
(scornfully): “When I use
a word, it means just what
I choose it to mean–neither
more nor less.” Alice
(appalled, turning to leave):
“The question is, whether
you CAN make words
mean so many different
things.” Humpty Dumpty
(with increased scorn): “The
question is which is to be
master—that’s all.” Text in
parenthesis from Carroll’s
(1871) Through the looking
glass. Alice redrawn from
Tim Burton’s Alice in
Wonderland, (Disney 2010)
318 7  The Last Best Hope

disturbing part of this to scientists such as myself is that underlying such ‘mischarac-
terization’ upon ‘mischaracterization’, in such a crucial area of feather evolution, is
the feeling of complete impunity and a law unto themselves these authors must feel
in the current climate of scientific publishing.
We have gone from Yale to the Academy of Sciences in China and the journey
does not stop there with respect to similar ‘mischaracterizations’ (let us be gener-
ous) in the pages of leading journals with respect to critical issues in the Birds are
Dinosaurs debate.
At the very least, what of the incompetence and/or bias of the referees and edi-
tors whose responsibilities are to ensure basic standards of quality in addition to
scientific competence in the field? As mentioned above, underscoring this con-
temptuous regard for science by these authors there seems to be a knowledge that
they will never be held accountable for their falsifications, not by the journals, not
by the editors and not by the referees they do business with, not to mention the
huge following Birds are Dinosaurs have among the populace. These are gross vio-
lations in crucial hypotheses that should have been noted by any reasonably com-
petent referee—it is not as though PNAS, Nature and Science are obscure journals
and that the referees have any excuse for not having those manifestly short and
simple papers word perfect. Worryingly, not only do these workers mischaracterize
claims with respect to the text of other workers but contradict their own published
statements to whatever suits the moment or allegation (all on record). A referee
understandably cannot know or check every publication—but these citations and
allegations involve pivotal and fundamental support for the hypothesis. Such fail-
ure as a consequence of inability and/or bias are enabling a spate of high-profile
publications of grossly technically flawed papers, which also breach some of the
most serious rules of behavior in science as laid out in COPE’s Code of Conduct.
Currie and Chen (2001, pp. 1724, 1721) within weeks of the Xu et al. (2001)
paper, presented a description of the same specimens of Sinosauropteryx and
confirmed the original findings by Chen et al. (1998). They stated that the integ-
umentary structures comprise “central shafts and plumulaceous barbs” and have
a “simple branching structure.” Given that Xu et al.’s (2001) only reference to
Sinosauropteryx is in its support for stage one of their model i.e. an unbranched
filament then it is quite extraordinary that Currie and Chen (2001), given their
own diametrically opposed description above, actually state with respect to
Sinosauropteryx, “the integumentary structures match his [Prum’s] model’s pre-
dictions of the form for early feathers (Xu et al. 2001),” which at the risk of being
repetitive—is according to the latter authors—an unbranched filament! It seems
the entire function is to support the ‘cause’ (Birds are Dinosaurs) regardless of the
evidence—even their own that is diametrically opposed. Could we blame Jonathan
Wells if he were to say, “This isn’t science. This isn’t even myth. This is comic
relief” (Feduccia 2012)?
If for no other reason than to stem the mythology surrounding Sinosauropteryx,
which continues—the latest speculation according to an article in Science
(McKellar et al. 2012; see below) is of this apparently ubiquitous Chinese dino-
saur’s protofeathers being preserved in Canadian amber. McKellar et al. (2012) in
7.4  COPE’s Proposals on Fraud in Science 319

response to technical comments by Dove and Straker (2012) included comments

with respect to measurements made by Lingham-Soliar et al. (2007), i.e., that they
were internal. This is a mischaracterization of the latter study by McKellar et al. to
justify their own conclusions. Lingham-Soliar et al. (2007) said the measurements
taken from a number of internal sites “were consistent for the other sites,” which
not only included the external sites (2, 3, and 4 in Fig. 1), but Lingham-Soliar
et al. also figured them (2007, p. 1827 and Figs. 1, 2c, 3c, d). Lingham-Soliar et al.
(2007) intention is impossible to misinterpret i.e., they emphasize that filaments
found internally and probably collagenous were no different to those external
and previously shown to be only coronal (external). Furthermore McKellar et al.
(2012) say if they “were indeed collagen fibers (internal structures), their measure-
ments have no bearing on our study of integumentary structures.” This is a straw
man because as demonstrated (Lingham-Soliar et al. 2007) the measurements for
both internal and external collagen filaments “were consistent.” McKellar et al.
contest the sizes cited by Dove and Straker (2012), i.e., that they are not “an order
of magnitude smaller” than their filaments and add that the measurements by, e.g.,
Currie and Chen (2001) were estimates and that their own filaments are from the
tips. But what this really indicates is that their measurements have no factual or
reliable reference base in Sinosauropteryx let alone on how diameter diminishes
from mid filament to tip—in a speculative protofeather. It has no scientific basis
whatsoever. Next they say that “subsequent work13 [Zhang et al. 2010] indicated
that many of the filaments surrounding Sinosauropteryx and Sinornithosaurus
were pigmented and thus cannot be dismissed as collagen fibers.” This is selective
citation of choosing only the literature that suits their cause. They conveniently
exclude the fact that the study was rejected (Lingham-Soliar 2011) using the fal-
sifiability criterion and that Zhang et al. (2010) rufous color of Sinosauropteryx
was labeled “without scientific merit.” Next, if the structures in Sinosauropteryx
are packed with phaeomelanosomes (Zhang et al. 2010), or even filament debris
(Lingham-Soliar 2011), they have no bearing on McKellar and colleagues’ sug-
gested related amber filaments—there are no reported melanosomes in the amber
sample—thus they do not share this character they endorse, hence evidence of
color and hence evidence of being a feather. Lastly, Mckellar and colleagues say
their filaments are hollow. There is no single filament showing hollowness (OED,
an internal cavity, an empty space) in Zhang et al. (2010) (nor has there ever
been any tangible evidence in the past (see Feduccia et al. 2005). The characters
Mckellar et al. (2011, 2012) choose to suggest similarity actually proves quite the
opposite. For McKellar et al. (2012) to make such a quantum leap of even suggest-
ing that their isolated filaments has any connection with Sinosauropteryx is irre-
sponsible science given the evolutionary implications.
This is yet another example of a clear failure in journals such as Science and
Nature to ensure a fair and efficient refereeing system. Rather, such articles are
a clear appeal to sensationalism and the masses (Bacon 1621; Mahoney 1977;
MacCoun 1998), i.e., simply mentioning Sinosauropteryx or protofeathers gives it
“primetime” news status for Science and Nature regardless of how implausible or,
as shown above with respect to Xu et al. (2001), how falsified the evidence may
320 7  The Last Best Hope

be. Mckellar et al.’s. (2011, 2012) conclusions in almost every way have nothing
whatsoever to do with the properties of the world under study but rather the prod-
ucts of their personal investigative disposition (MacCoun 1998). Mohoney (1997)
drew attention to a similar problem in the social sciences of confirmatory bias, i.e.,
the tendency to emphasize and believe experiences that support one’s views and
to ignore or discredit those that do not and its tragic effects, e.g., of understanding
the processes and parameters of human adaptation.
In Chap. 5, in the section on Archaeopteryx, I discussed a paper by Nudds and
Dyke (2010) published in Science in which they proposed a model for determining
flight capabilities in fossil birds. Despite, their generally poor biomechanical inter-
pretations as demonstrated in my original critique (Lingham-Soliar 2014a) and
in reply (Lingham-Soliar 2014b) to an acrid response by one of their colleagues,
Palmer (2014) at the University of Bristol, in defense of Nudds and Dyke (2010).
Nevertheless, despite the acridity, debate represents the ethos of science. Nudds
and Dyke were entitled to their hypothesis as were the authors who supported and
opposed it, but it had to have been within the tenets of normal scientific protocol,
which it was not. As we saw above the study had monumental potential signifi-
cance with respect to their allegation that Archaeopteryx was incapable of flapping
flight—and of equal importance that their findings represented a model that could
be used to determine the flight capabilities of all other fossil birds/protobirds.
Huge claims that no journal, no editor and no referee should take lightly. Besides,
seriously flawed science, Nudds and Dyke (2010) were guilty of a severe mischar-
acterization in support of their measurement data that, as with Xu et al. (2001),
incriminated another author’s work, an expert in the field, Elzanowski (2002).
First, Nudds and Dykes (2010) study upon which their whole hypothesis (and
model) was based, hinged on a diameter and length measurement of a single rachis
of Archaeopteryx. A competent/unbiased referee, given the important implications
(above) and given the journal concerned is Science, would have thrown out the
paper on that point alone with the words—go and measure more samples. That
did not happen. Second, apparently to add some sort of proxy statistical support,
Nudds and Dyke (2010) stated that their measurement data for the rachis (length
129 and diameter 0.75 mm) for the longest primary of the Munich Archaeopteryx
were “consistent with measurements by Elżanowski (2002).” Elzanowski (2002)
made no such measurements—he did not report the all critical rachis diameter
data for Archaeopteryx at all (not a single specimen), nor did he present a single
length for the rachides of the Munich specimen (Lingham-Soliar 2014a, b). The
longest primary that Elzanowski did present measurements for was 145 mm in the
Berlin specimen and an estimation of more than 150 mm in the London speci-
men, nothing like the longest primary of 129 mm by Nudds and Dyke—irrelevant
anyway because there were no associated thickness measurements, the crucial fac-
tor in Nudds and Dyke’s analysis. Here again, the competence of a specialist ref-
eree on pivotal and yet basic knowledge is severely challenged. If the referee was
not immediately aware of this data then he was obliged to check because Nudds
and Dyke’s own measurements involved just one feather. If he was not going
to throw it out on that alone, then the authenticity of the proxy measurements
7.4  COPE’s Proposals on Fraud in Science 321

becomes paramount. This paper was published in the journal Science and fails on
the most basic level of refereeing let alone the highest quality expected of such a
high impact journal. While I respect Gareth Dyke’s (see Willemse 2014) response
to my critique (Lingham-Soliar 2014a), “I think Dr. Lingham-Soliar’s work is
super and an advance on ours. This is how science works!”, it does not exonerate
them for the false data and least of all, Science, which failed on basic publishing
standards. What if my critique never happened? To its credit Science does have a
Technical Comments section in which workers may reply to matters of concern
in published research. But that is no excuse for letting through seriously flawed
papers that in any event get far greater attention than the Technical Comments,
and in addition the authors have the last word with their own reply to Technical
Comments. Nevertheless, the latter is a step in the right direction albeit with room
for improvement (see below). This, however, is a completely separate issue from
poor refereeing quality. Nudds and Dyke (2010) is yet another example of mis-
characterized (actually non-existant) data with respect to crucial evidence in sup-
port of a model in the Bird Are Dinosaurs saga—and of the ever-growing body of
such cases in the pages of Science and Nature.
The most recent paper in Science on the subject of Birds are Dinosaurs and
protofeathers, by Godefroit et al. (2014a, b) is so faulty with respect to the most
basic scientific standards in biology and taphonomy (Lingham-Soliar 2014b; dis-
cussed in Chap. 6) that again one must question the refereeing and editorial quality
in this illustrious journal with respect to this field of study. If it demonstrates one
thing, each paper declaring protofeathers is like the Hydra’s head of Greek myth,
chop off one and another two more terrible spring up in its place.
We will go back a few years in an attempt to see whether or not one is over-
reacting. A sensational paper by Schweitzer and colleagues (2007) was published
in Science. The ensuing media hype, included “Tyrannosaurus Rex, basically a big
chicken,” and The New York Times reported that such investigations opened the
way for the “exploration of molecular-level relationships of ancient, extinct ani-
mals.” The widespread skepticism and criticisms that followed were encapsulated
in three major rebuttals that appeared in Science. Perhaps, the most damning was
by Pevzner and colleagues (2008) suggesting contamination and a demand for the
full spectra. When only under duress (it is usual to provide such data readily) one
of the authors of the original paper, Asara, posted all 48,216 spectra, Fitzgibbon
and McIntosh (2009) were able to test them and confirm contamination when they
discovered a hemoglobin peptide in the spectra normal to ostriches (Asara also
worked with ostrich proteins in his lab).
This again raises the question of competence and partiality of the referees.
Science had, as reported (Feduccia 2012), not used some of the top people, e.g.,
Buckley and colleagues and Pevzner and colleagues. Although, these authors were
presented the opportunity for a rebuttal in Science’s forum ‘Technical Comments’,
in which they did publish strong rebuttals, Salzberg (2008), director of the Center
for Bioinformatics and Computational Biology at the University of Maryland was
strongly critical, writing, “What I find most reprehensible on their [the editors
of Science] part is that they published both the Buckley et al., and Pevzner et al.
322 7  The Last Best Hope

critiques as ‘Technical Comments’—which means they appear online only, not in

the print edition. Both the Asara and Schweitzer articles, by contrast appeared in
the print edition, which means they would be read more widely. If Science truly
cared about getting this story right, they would publish the critiques just as promi-
nently as the original article.”

7.5 National Geographic

The National Geographic Society with more than 9 million members in the mid-
1990s is the world’s largest scientific and educational society. It was founded in
Washington, D.C., by a small group of eminent explorers and scientists “for the
increase and diffusion of geographic knowledge.” However, in 1999 the Society’s
principle publication organ National Geographic Magazine came under severe
criticism from a leading expert on the evolution of birds, Storrs Olson, of the
Smithsonian Institution. In an open letter to Peter Raven (mentioned above), Olson
(1999), also Feduccia (2012) wrote, “With the publication of ‘Feathers for T. rex?’
by Christopher P. Sloan in its November issue, National Geographic has reached
an all-time low for engaging in sensationalistic, unsubstantiated, tabloid journal-
ism.” The heart of the article concerns Sloan’s categorical endorsement of the now
generally acknowledged fossil fraud Archaeoraptor, which has joined the ranks
of paleontological folklore notoriety on a par with Piltdown man. However, the
real embarrassment concerning Sloan’s article is that he had apparently convinced
himself as well as the editorial board of NGM that his role went beyond that of
that of a journalist (cf. Henry Gee). Olson (1999, http://[email protected]) showed
how confused Sloan was when he decided first, that it was appropriate for a jour-
nalist to differentiate a taxon new to science and second that evidence claiming to
support the new taxon could be presented in a nonpeer reviewed magazine. The
serious consequence is that “the name Archaeoraptor liaoningensis Sloan is now
available for purposes of zoological nomenclature as of its appearance in National
Geographic (International Code of Zoological Nomenclature, Article 13a, i).”
If it shows nothing else it is how blurred the lines between journalistic articles
and scientific articles in Science and Nature connected with the dinosaurian origin
of birds are—the eclectic style of many related papers, e.g., in Nature, Science and
PNAS must take responsibility for this confusion more than any other single factor.
Olson (1999) summed up the fiasco when he wrote “The idea of feathered dino-
saurs and the theropod origin of birds is being actively promulgated by a cadre
of zealous scientists acting in concert with certain editors at Nature and National
Geographic who themselves have become outspoken and highly biased proselyt-
izers of the faith. Truth and careful scientific weighing of evidence have been
among the first casualties in their program…. If Sloan’s article is not the crescendo
of this fantasia, it is difficult to imagine to what heights it can next be taken.”
Given, his central position in the Archaeoraptor fraud (dubbed the Piltdown dino-
saur), one might think it would have spelt the end of Sloan’s days as an editor
7.5  National Geographic 323

of NGM or, at the very least, time for considered reflection. Quite the contrary!
In an article, Dinosaurs: In Full Color for the First Time, based on the study by
Zhang et al. (2010) alleging feather-like color organelles in its central character,
the theropod dinosaur Sinosauropteryx, Sloan (2010) wrote, “I feel particularly
privileged to have been behind the scenes on the story that broke today showing
the first scientifically established color on nonavian dinosaurs. I visited China two
times last year to meet Chinese scientists working on this study and visited with
Mike Benton of the University of Bristol at the Society of Vertebrate Paleontology
annual meeting there last winter. These scientists were on the brink of doing some-
thing once thought impossible. As we talked, the excitement among them was
palpable. This is just the very first glimpse of the color of the prehistoric world,
like sun rays just peeking over the horizon at dawn. Hold on to your seats. There
will be much, much more to come!” As we have seen above with Archaeoraptor
(Olson 1999), Dr. Sloan, does not seem to have mellowed. As with Archaeoraptor,
the exuberant euphoria involving the chief dinosaur of this story, Sinosauropteryx
and the red or rufous color of its feathers (also seen in an artists’ impression in The
New York Times) has, as demonstrated (Lingham-Soliar 2011), no scientific merit
(also see Chap. 6).
Given the impact of NGM globally, the society has an enormous responsibil-
ity to the public. Foremost in this responsibility is the urgency for appropriate and
objective editors and writers and to choose responsible editors rather than sensa-
tionalist. Yet, I am partly sympathetic with Dr. Sloan and National Geographic
generally, given that the society is also constrained by its scientific advisory panel,
some members of which I have already commented upon above (e.g., Mark Norell
and Kevin Padian), and by prestigious publications. It may be a case of “shooting
the messenger” for bringing the bad news.
It seemed that in a paper by Lawrence Witmer (2009) there was still hope.
In a spirited criticism of the status quo he argued against the dangers of rhetoric
and concocting ‘‘complicated scenarios for feather evolution’’ based on the mis-
conception all along by most workers that it is a ‘‘seemingly simple question”
but rather that it is ‘‘surprisingly hard to answer,’’ citing the papers of workers on
both sides of the debate (including quite prominently those by myself and col-
leagues). In the process he had a nice publication in Nature. However, hope was
short lived. Commenting in The New York Times (Zimmer 2010) on the paper by
Zhang et al. (2010) on fossil melanosomes, Dr. Witmer, with the rhetoric he had so
recently and fervently denounced, declared ‘‘the study decisively closes the case
on whether the whiskers are feathers or collagen.’’ Here, was an absolute endorse-
ment of a study (on the day of its first appearance online), by Dr. Witmer, preempt-
ing any need to carefully weigh the paper’s merits let alone test the claims. Is
that not the definition of science, testability? Yet another example of how review-
ers’ of scientific papers on the dinosaurian origin of birds respond when their pet
hypothesis is presented for appraisal—exactly the kind of unbridled enthusiasm
from prominent workers that journals such as Nature and Science thrive on—never
mind the quality feel the width (title of an old British comedy set in the Jewish tai-
loring profession). The accuracy of the science is quite secondary. In all this time
324 7  The Last Best Hope

not once did a request for a review from either Nature, Science or PNAS come
to me—yet it is my work that such studies have had to answer even if merely as
an irritation and, occasionally, triumphantly as seen when Henry Gee, armed with
his own self-fulfilling prophecy, could hardly contain himself when melanosomes
were allegedly found in Sinosauropteryx (Gee 2010), albeit short lived (Lingham-
Soliar 2011, and Chap. 6).
There seems little doubt, as Benno Muller-Hill demonstrated, that the weight
of the institute has a heavy bearing in what is published in the top journals and
what is not. This is not the enlightenment expected of the twenty first century but
a return to Victorian values. Those values, of sexism, elitism and class prejudice,
personified by men such as Richard Owen, Thomas Henry Huxley fought against
his whole life and in so doing helped to elevate the place of science in modern
society (Desmond 1982, 1997). It is worth considering how Darwin’s Origin of
Species which “struck the Victorian solar plexus like a steam hammer” (Dawkins’
2010), would have fared if left to the majority of powerful men of science of the
day (many in the clergy, another sphere of dogma)—and had he not gained the
support of a few intellectuals such as Joseph Hooker and Thomas Huxley to his
cause—the work many now regard as the greatest single idea of humankind.

7.6 Education and Freedom in Apartheid South Africa

Perhaps many in the West have had democracy for so long that they take it for
granted and have become blasé. On the other hand the majority of us as black peo-
ple in SA who have lived through terribly inhumane times see any assault upon
our hard-won freedom more sharply. I have seen members of my own family
pay a heavy price for the freedom we have today, which is just 20 years old. Yet,
whether gained 200 years ago or yesterday it should not matter because every free-
dom or right that anyone has wherever in the world today, from the most mun-
dane to the most profound, we owe to someone who put themselves on the line
for it. The notable paleontologist Zofia Kielan-Jaworowska, who I met in Poland
not long after she had won the prestigious Romer-Simpson Medal (awarded a
few years before to my own Ph.D. adviser Richard Estes), recalled how as a
19-year-old in the Polish resistance, when her country was in the grip of the Nazi
terror, she lived with her medical books at one hand and a rifle at the other. The
Human Rights Charter came into being in 1948 because that terror that she and
millions of others fought against aroused humanities conscience the way noth-
ing had before. Yet, at precisely that time in 1948 a new government (hereafter,
regime) was instated in South Africa led by the Afrikaner Nationalist Party (NP)
but supported by many English-speakers—believing that the NP alone ensured
white domination. New laws would immediately come into effect that would deny
85 % of the people (labeled by the regime by the offensive negative term “non-
whites,” i.e., white being the definitive criterion; hereafter, referred to as black) of
virtually every human right and dignity (see Slye 1999, Crime against Humanity;
7.6  Education and Freedom in Apartheid South Africa 325

Landsberg and Mackay 2006) newly enshrined in the Human Rights Charter (see
Appendix)—identical in almost every way to the laws in 1930s Germany against
Jews, which had laid the ground for the holocaust.
Among the new laws in South Africa would be denial of access by blacks to
the country’s tertiary institutions (as had for years before been established for
primary and secondary institutions). Rather, blacks would attend purpose built
“ghetto” universities controlled by the Afrikaner Broederbond (secret society with
an extreme racist ideology, at work to this day)—one for each of the designated
racial groups, Indian, African and Colored). This was designed to shut the doors
completely against blacks to the historically white universities of South Africa, as
compared to the limited and highly segregated access previously. It marked the
Afrikanerization policies that radically changed Afrikaner demographics in SA
and ultimately led to the brink of economic ruin and civil war—and to the irrecov-
erable loss of generations of black talent. The NP’s monopolizing of the country’s
wealth ensured that poor, uneducated, rural Afrikaners enjoyed the most extreme
affirmative action in history, filling posts in the cities’ railways, POs, and state cor-
porations while the Broederbond ensured that relatively educated Afrikaners filled
the most influential positions in universities, media and senior civil service—many
ill-qualified (Adam and Adam 2011). In this land of milk and honey, corruption
largely went unnoticed in a pre-1994 civil service shrouded in secrecy (Klaaren
2006). Just as Muller-Hill (1993) noted in Nazi Germany, white academics, men
and women in South Africa, including in the medical profession, which is now
“acknowledged as generally shameful” (Williams 2000), accepted gladly all the
benefits of the new laws (see Peter Hain 2014, http://familylink.com/SouthAfrica).
Indeed, white academics who visited institutions or came to live in South Africa
from Europe and the US (high immigration levels helped the white population to
increase by 50 percent between 1963 and 1972 (US Library of Congress)), were
also untroubled by the fact they were enabling the regimes’ racist policy of deny-
ing blacks the academic roles they were filling or, simply by doing business with
its racist institutions, they were giving whites the intellectual exchange (denied to
blacks) and respectability that they needed from the West.
The beginning of the end came in the most remarkable way from the unlikeliest
of sources—not from great leaders (not even Nelson Mandela, although he was a
symbol of freedom), not from violence, not from terrorism, not from trade unions,
not from the ANC but, almost literally, from out of the mouths of babes and chil-
dren. When Verwoerd, Minister of Bantu Affairs (later Prime Minister), introduced
in Parliament the Bantu [a collective term created by the regime for the indigenous
black peoples of South Africa] Education Act of 1953, he sought to justify the infe-
rior education of blacks by invoking the system of job reservation, ‘jobs for whites
only’ except the most menial (hence the importance of white immigrants) which was
imposed by law on the black community (African, ‘coloreds’ and Indians) as part of
the apartheid system. Its most devastating function was to keep the indigenous black
majority in a total state of subservience as implicit in his words, “The school must
equip the Bantu to meet the demands which the economic life … will impose on him.
…What is the use of teaching a Bantu child mathematics when he cannot use it in
326 7  The Last Best Hope

practice?… Education must train and teach people in accordance with their opportu-
nities in life” (van der Vyver 2011; Ndlovu 2014). Underscoring this, school spend-
ing per black child was about 5 percent of spending on a white child (Hazlett 1988).
Then when it looked as if things could not get worse, they did. Black school chil-
dren were singled out in 1976 to be taught predominantly in Afrikaans rather than
in English (the main medium in white schools). Punt Janson, the Deputy Minister of
Bantu Education at the time, was quoted as saying: “A Black man may be trained to
work on a farm or in a factory. He may work for an employer who is either English-
speaking or Afrikaans-speaking… Why should we now start quarreling about the
medium of instruction among the Black people as well? … No, I have not consulted
them and I am not going to consult them. I have consulted the Constitution of the
Republic of South Africa” (van der Vyver 2011; Ndlovu 2014). This was the culmi-
nation of a Broederbond secret document on the importance of imposing Afrikaans
on blacks as part of the ideology of racial subjugation (Ndlovu 2014). Besides the
intense practical difficulties for children having to learn difficult course work sud-
denly in a foreign tongue (not to mention teachers badly versed in Afrikaans), the
decree was resented deeply by blacks, because Afrikaans was widely viewed—in the
words of Archbishop Emeritus Desmond Tutu (Sparks and Tutu 2011)—as “the lan-
guage of the oppressor.”
On the morning of 16 June 1976, between 10,000 and 20,000 black students
walked from their schools in Soweto to Orlando Stadium for a rally to protest
against having to learn through Afrikaans in school (Ndlovu 2014). One has to
understand the brutality of the police who regarded and treated blacks as less than
human to get even a glimmering of how brave these children were. It is a day that
is now celebrated as a public holiday (Youth Day) in South Africa. Crass stupidity,
racism and bigotry chose to attack and demoralize the weakest of our society, chil-
dren, but instead awakened a sleeping giant, which would spell the end of apart-
heid. Never before in the annals of human history did a people, children, rise up,
not for food (desperate enough in itself), but in the name of education. Figure 7.7
shows a photo of a young woman leading fellow students on that day and it imme-
diately reminded me of Eugene Delacroix’s painting of Liberty Leading the People
(1830) to commemorate the July Revolution in France (inset, detail), transforming
his allegory into touching modern-day reality (Delacroix would have been proud).
Soweto 1976 is our country’s finest moment, the historic watershed. Tragically,
many children gave up their lives that day, almost certainly hundreds (Reuters news
agency), a number of which as young as 11 years old (Fig. 7.8). Even more shock-
ing, most of the children were killed by the police in cold blood the next day when
they tried to enter their schools that had been barricaded by the white authorities.
The tragedy of Soweto, 1976 did little to affect the white vote in South Africa.
Many commentaries note that as in their resistance to democracy in the past there
are elements today that would gladly return to a pre-1994 SA implicit in the
strongest opposition to the merest hint of any redress (e.g. in black land restitution,
trade unions, education, housing etc.) for the gross injustices during apartheid—
with demeaning chants that ‘blacks must move on’ or of ‘blacks playing the race
card’. Truly, the pot calling the kettle black!. South African Nobel laureate, JM
7.6  Education and Freedom in Apartheid South Africa 327

Fig. 7.7  The Soweto
Uprising. The student protest
in 1976 against being taught
predominantly in Afrikaans

Coetzee, at a speech on receiving his second Booker Prize (1999, for Disgrace)
said that despite all the rhetoric of the rainbow nation, South Africa is a country
terminally damaged by the evils of apartheid. However, for the state the uprising
marked the most fundamental challenge yet to apartheid, and the economic and
political instability it caused was heightened by the strengthening of the interna-
tional boycott in which now the young people in free societies in the world, in sol-
idarity with the youth of Soweto, would play a prominent part. Oliver Tambo, the
African National Congress (ANC) president-in-exile, declared how ill-prepared
the ANC had been for this dormant power that had been unleashed, “[w]ithin
a short period of time it propelled into the forefront of our struggle millions of
young people … It brought to our midst comrades many of whom had very little
contact with the ANC, if any…” (Ndlovu 2014). There was no going back. One
of the banners held aloft by the children of Soweto (Fig. 7.7, top) said it all, “For
freedom we shall lay down our lives. The struggle continues” (Ndlovu 2014).
While apartheid may have gone (at least legally), more subliminal forms of
racism, like the malignant Cheshire cat's grin in Alice in Wonderland, linger on.
In opposing black affirmative action many whites (frequently in high positions
including in academia), with the same lack of humanity that made “human rights
violations an art form” during apartheid (Landsberg and Mackay 2006), demand
‘the past must remain in the past’. Yet, the only way for SA to rebuild a just future
328 7  The Last Best Hope

Fig. 7.8  Hector Pieterson,
the 12-year-old schoolboy
killed by police, whose
lifeless body is held in the
arms of a traumatized older
schoolboy who could not
speak for some time after
the incident. Alongside is
Hector’s sister

is through dialogue, which would be vacuous if it did not confront the evils of the
past. I have raised the specter of apartheid in South Africa for two reasons. The
first, as Muller-Hill (1993) tried to show, that we need to get away from the mind-
set that integrity and humanity are synonymous with high personal academic and/
or institutional status—the German and South African experience tells us other-
wise—no louder than in the latter where those who put high academics/officials to
shame turned out to be schoolchildren. The second, as in Germany, there were few
exceptions in SA to people happy to accept the ill-gotten privileges, but one such
academic stands out in my mind, Prof Colin Kaplan, who as one of the world’s
leading virologists at Groote Schuur Hospital in Cape Town, fled South Africa
despite his privileged position, because he could no longer serve an evil regime.
I  was privileged to study virology under him at Reading University.

7.7 The US Constitution’s First Amendment

Pertinently, editors of some of our leading journals need to remove their rose-tinted
spectacles and do greater service to the ideologies of a free press for which our fore-
fathers fought and for which people at this very moment are fighting for in different
parts of the world. The example of the children of Soweto 1976 who defied one of
7.7  The US Constitution’s First Amendment 329

the most powerful and evil regimes in the world and took their fate into their own
hands with the words, “[f]or freedom we shall lay down our lives” should serve as
a reminder to students and young scientists around the world to choose their role
models in science (or wherever) wisely, regardless of their scientific beliefs. In mat-
ters of strong contention it is imperative that both sides of an argument are heeded
with equalness regardless of status, geography (which contains a multitude of sins),
gender, and institution. If unfairness and dishonesty are the only ways to propagate
ideas then there is surely something seriously wrong. The preceding sections should
have made that clear. Let us be perfectly clear here, the present discussion is not
against peer review but against gross unfairness in the peer review system. Some,
may be motivated by what they have read, others, regrettably not—as the American
wit, Dorothy Parker wrote, “[y]ou can’t teach an old dogma new tricks.”
Supporters of Birds are Dinosaurs frequently misconstrue studies such as mine
that question poor structural and anatomical interpretations of fossilized soft tissue in
critical areas of the debate as an attack on the Birds Are Dinosaurs hypothesis, which
is not the case (Lingham-Soliar et al. 2007, p. 1923; Lingham-Soliar 2010b, p. 569).
This is simply convenient as it is easier for supporters including editors and referees
to ridicule opposition by labeling it as “anti cladistics” and “not doing science” or
“poisoning the well” (see Feduccia 2012). This is exactly analogous to opponents
of apartheid in SA being labeled “communists” and “terrorists” because they were
easier to denounce by enflaming passions in the absence of logic and reason, ironi-
cally by a regime that practiced the very tactics of terrorists and of communist states.
David Dinges (2010) refers to comments by the CSE namely that “scientific jour-
nals have responsibilities to the public [and] the scientific community as a whole.”
Editorial professionals such as Goldsmith et al. (2006) also recognize the responsible
role they have to play in the peer review system, paraphrasing the words of Juvenal,
“Quis custodiet ipsos custodes?”—guarding the guardians in all aspects of commu-
nities, including scientific. We can be lulled into a false sense of security into think-
ing that the problems discussed with respect to violations in scientific publications are
minor or rare exceptions, which can be brushed aside as atypical and as extreme exam-
ples that portray a false impression. This is not so, rather it has got dangerously worse
in my own recollections over the last 15 years, pushing the boundaries of intolerance
and prejudice with every passing year without the majority of people even noticing
(nor some wanting to). During the US’ anticommunist hysteria of the 1950s, the use of
loyalty oaths was widespread, and many teachers who refused to take them were dis-
missed without due process. It was this period that also saw one of the greatest assaults
on the Bill of Rights (1791) in US history when thousands of the Hollywood film
fraternity were hauled before the House Un-American Activities Committee. Many
conformed but some did not. One of the latter was the distinguished actor and human-
ist Gregory Peck who said something that was both insightful and salutary, “There is
more than one way to lose your liberty—it can be torn out of your hands by a tyrant—
but it can also slip away, day by day, while you’re too busy to notice.”
Henry Gee at Nature, by his own words and actions has abused the mandate of
fair scientific publishing. His verbal intransigence and intolerance (above) reminds
me of the words of the Deputy Minister of Bantu Affairs, Punt Jansen (1976), pre-
ceding the Soweto Uprising (above). Storrs Olson wrote in 1999 (http://vrtpaleo@
330 7  The Last Best Hope

usc.edu; see Olson 1999) in reply to Henry Gee’s intemperate letter (above), “[t]he
very fact that you still have a job is an inexhaustible source of wonder on this side
of the Atlantic, where most scientists proceed under the assumption that editors of
scientific journals are under some small obligation at least to preserve the appear-
ance of maintaining objectivity.” I am sorry to have to say to Storrs Olson that
the disease has spread to his side of the Atlantic—I mentioned earlier the shame-
ful behavior of an editor of a US journal with a wide biological readership, who
regrettably must remain nameless because of confidentiality protocol. Many have
just not shown their hand the way Henry Gee has. On the other hand with respect
to poor editorial processes, rather than a deliberate skewing of the process (let us
be generous), in the field of Birds are Dinosaurs, Science and PNAS have pandered
to popular views by allowing publication of some of the most overtly scientifically
flawed paleontological studies, as demonstrated above, with no apparent end in
sight. All the evidence points to the fact that in Birds are Dinosaurs only potentially
favorable referees are chosen. With respect to opposition, Devries et al. (2009)
indicated the potential for negative bias which may reflect “the bias of the associ-
ate editor who may seek to subject the submission (for whatever reason) to a more
intense review process by choosing reviewers with a reputation for intensely criti-
cal assessment.” Couple this with editorial boards in this field that often are made
up solely of supporters of Birds are Dinosaurs and we have a highly compromised
‘free press’. Chiappe (2012) mocks Feduccia (2012) for what he calls his lectures
on the morality of science, “Feduccia scolds editors about how “scandals are sen-
sational, but uncritical editing that permits careless and flawed articles to appear
in esteemed journals is more troubling.” Of course, most beneficiaries of flaws
in systems, as we saw in the grander scale in Nazi Germany and apartheid South
Africa, are hardly likely to “buck” the system, but for a few principled individuals.
Dr. Chiappe and supporters frequently claim that most people support their views,
and use it to mock and revile others who do not. Well, they should enjoy that right
because it is enshrined in the US Constitutions’ First Amendment, and is a right
fought for by other people in the US as far back as Thomas Paine (1791) who was
also mocked and alienated by self-centered men of the day with personal agendas
and for more than a century after his death. But, later the tide turned. On Jan. 30,
1937, The Times of London referred to Thomas Paine as “the English Voltaire,”
and on May 18, 1952, Paine’s bust was placed in the New York University Hall
of Fame. Our own Nelson Mandela was during his years of incarceration reviled
by most South African whites who held the whip hand at the time, yet ostensibly
revered by them today, ironically, for exactly the same values of a free and just
society he had expressed and was hated for in his “I am prepared to die” speech at
the Rivonia Trial in 1964 (Rosen and Widgery 1991). Strange are the ways of folk.
It is no accident that the US constitution’s first amendment is freedom of speech.
How long must we wait and how long can we continue to have pride in the hard-
fought-for values of democratic societies when those who should uphold our most
valuable freedom, the freedom of the press, our “last best hope” lets us down in this
way? Publishing Houses and Societies in democracies owe their very existence to the
ideology and practice of free speech. Will highly biased editors and referees, who do
7.7  The US Constitution’s First Amendment 331

nothing but harm to the profession, ever be brought to book or have to face a modern-
day Thomas Cromwell (1653) with the words, “[y]ou have sat too long for any good….
Depart, I say; and let us have done with you… you shall now give place to better men?”
Note in Press. The tragic events in France concerning Charlie Hebdo and Press
Freedom is a reminder of those who put their lives on the line for the rights we
enjoy in democratic and secular societies—in the words of the children of Soweto,
“the struggle continues.” France’s stance against being blackmailed by totalitarian
states and terrorists must be applauded lest we become like them.

Appendix

Universal Declaration of Human Rights

I have asterisked all rights that blacks, i.e., Africans, Coloureds (mixed race), and
Indians, were denied in South Africa until 1994, by the consensus of the white vote.
*Article 1
All human beings are born free and equal in dignity and rights. They are
endowed with reason and conscience and should act towards one another in a
spirit of brotherhood.
*Article 2
Everyone is entitled to all the rights and freedoms set forth in this Declaration,
without distinction of any kind, such as race, colour, sex, language, religion, political
or other opinion, national or social origin, property, birth or other status. Furthermore,
no distinction shall be made on the basis of the political, jurisdictional or international
status of the country or territory to which a person belongs, whether it be independent,
trust, non-self-governing or under any other limitation of sovereignty.
*Article 3
Everyone has the right to life, liberty and security of person.
Article 4
No one shall be held in slavery or servitude; slavery and the slave trade shall be
prohibited in all their forms.
*Article 5
No one shall be subjected to torture or to cruel, inhuman or degrading treatment
or punishment.
*Article 6
Everyone has the right to recognition everywhere as a person before the law.
*Article 7
All are equal before the law and are entitled without any discrimination to
equal protection of the law. All are entitled to equal protection against any dis-
crimination in violation of this Declaration and against any incitement to such
discrimination.
332 7  The Last Best Hope

*Article 8
Everyone has the right to an effective remedy by the competent national tribunals
for acts violating the fundamental rights granted him by the constitution or by law.
*Article 9
No one shall be subjected to arbitrary arrest, detention or exile.
*Article 10
Everyone is entitled in full equality to a fair and public hearing by an independ-
ent and impartial tribunal, in the determination of his rights and obligations and of
any criminal charge against him.
*Article 11
1. Everyone charged with a penal offence has the right to be presumed innocent
until proved guilty according to law in a public trial at which he has had all the
guarantees necessary for his defence.
2. No one shall be held guilty of any penal offence on account of any act or
omission which did not constitute a penal offence, under national or international
law, at the time when it was committed. Nor shall a heavier penalty be imposed
than the one that was applicable at the time the penal offence was committed.
*Article 12
No one shall be subjected to arbitrary interference with his privacy, family,
home or correspondence, nor to attacks upon his honour and reputation. Everyone
has the right to the protection of the law against such interference or attacks.
*Article 13
*1. Everyone has the right to freedom of movement and residence within the
borders of each state.
*2. Everyone has the right to leave any country, including his own, and to
return to his country.
*Article 14
*1. Everyone has the right to seek and to enjoy in other countries asylum from
persecution.
2. This right may not be invoked in the case of prosecutions genuinely arising
from non-political crimes or from acts contrary to the purposes and principles of
the United Nations.
*Article 15
*1. Everyone has the right to a nationality.
*2. No one shall be arbitrarily deprived of his nationality nor denied the right to
change his nationality.
*Article 16
*1. Men and women of full age, without any limitation due to race, national-
ity or religion, have the right to marry and to found a family. They are entitled to
equal rights as to marriage, during marriage and at its dissolution.
*2. Marriage shall be entered into only with the free and full consent of the
intending spouses.
Appendix 333

*3. The family is the natural and fundamental group unit of society and is enti-
tled to protection by society and the State.
*Article 17
*1. Everyone has the right to own property alone as well as in association with
others.
*2. No one shall be arbitrarily deprived of his property.
*Article 18
Everyone has the right to freedom of thought, conscience and religion; this
right includes freedom to change his religion or belief, and freedom, either alone
or in community with others and in public or private, to manifest his religion or
belief in teaching, practice, worship and observance.
*Article 19
Everyone has the right to freedom of opinion and expression; this right includes
freedom to hold opinions without interference and to seek, receive and impart
information and ideas through any media and regardless of frontiers.
*Article 20
*1. Everyone has the right to freedom of peaceful assembly and association.
2. No one may be compelled to belong to an association.
*Article 21
*1. Everyone has the right to take part in the government of his country,
directly or through freely chosen representatives.
*2. Everyone has the right of equal access to public service in his country.
*3. The will of the people shall be the basis of the authority of government; this will
shall be expressed in periodic and genuine elections which shall be by universal and
equal suffrage and shall be held by secret vote or by equivalent free voting procedures.
*Article 22
Everyone, as a member of society, has the right to social security and is entitled to
realization, through national effort and international co-operation and in accordance
with the organization and resources of each State, of the economic, social and cul-
tural rights indispensable for his dignity and the free development of his personality.
*Article 23
*1. Everyone has the right to work, to free choice of employment, to just and
favourable conditions of work and to protection against unemployment.
*2. Everyone, without any discrimination, has the right to equal pay for equal work.
*3. Everyone who works has the right to just and favourable remuneration
ensuring for himself and his family an existence worthy of human dignity, and
supplemented, if necessary, by other means of social protection.
*4. Everyone has the right to form and to join trade unions for the protection of
his interests.
*Article 24
Everyone has the right to rest and leisure, including reasonable limitation of
working hours and periodic holidays with pay.
334 7  The Last Best Hope

*Article 25
*1. Everyone has the right to a standard of living adequate for the health and
well-being of himself and of his family, including food, clothing, housing and
medical care and necessary social services, and the right to security in the event
of unemployment, sickness, disability, widowhood, old age or other lack of liveli-
hood in circumstances beyond his control.
*2. Motherhood and childhood are entitled to special care and assistance. All
children, whether born in or out of wedlock, shall enjoy the same social protection.
*Article 26
*1. Everyone has the right to education. Education shall be free, at least in the
elementary and fundamental stages. Elementary education shall be compulsory.
Technical and professional education shall be made generally available and higher
education shall be equally accessible to all on the basis of merit.
*2. Education shall be directed to the full development of the human person-
ality and to the strengthening of respect for human rights and fundamental free-
doms. It shall promote understanding, tolerance and friendship among all nations,
racial or religious groups, and shall further the activities of the United Nations for
the maintenance of peace.
*3. Parents have a prior right to choose the kind of education that shall be given
to their children.
*Article 27
*1. Everyone has the right freely to participate in the cultural life of the com-
munity, to enjoy the arts and to share in scientific advancement and its benefits.
2. Everyone has the right to the protection of the moral and material interests
resulting from any scientific, literary or artistic production of which he is the
author.
*Article 28
Everyone is entitled to a social and international order in which the rights and
freedoms set forth in this Declaration can be fully realized.
*Article 29
1. Everyone has duties to the community in which alone the free and full devel-
opment of his personality is possible.
2. In the exercise of his rights and freedoms, everyone shall be subject only to
such limitations as are determined by law solely for the purpose of securing due
recognition and respect for the rights and freedoms of others and of meeting the
just requirements of morality, public order and the general welfare in a democratic
society.
3. These rights and freedoms may in no case be exercised contrary to the pur-
poses and principles of the United Nations.
*Article 30
Nothing in this Declaration may be interpreted as implying for any State, group
or person any right to engage in any activity or to perform any act aimed at the
destruction of any of the rights and freedoms set forth herein.
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Index

Page numbers followed by “f” and “t” refer to figures and tables respectively
A cine film of, 45f
Aerial behaviors, 105, 128, 214 dermis, 99–100
diversity of, 106f swimming mode of, 47f
Aerofoil, 27 Anguilliform swimmers, 99
force acting on, 27f eel dermis, 99–100
Agama utricollis (agamid lizard), 270f, 289 Anguilliform swimming. See Axial undulatory
Alca torda (Razorbill), 228 (anguilliform) swimming
Alternaria species, 241 Anhinga rufa (African darter or snakebird), 201f
Amphibians, gliding, 110–112 Apartheid South Africa, 307
Amphiporus lactifloreus, worm cuticle, 67f education and freedom in, 324–327
Anas undulata (yellow-billed duck) African National Congress (ANC), 327
banking, 190f Soweto Uprising, 327–322, 327f, 328f
beating motion of wings, 196f Aquatic locomotion, 43–55. See also Anguilla
formation flying in, 237f anguilla
landing on water, 199, 202f axial suboscillatory swimming, 46–51, 48f,
Anchiornis (early bird), 179, 300 49f, 50f
Angle of attack, 157 digital particle image velocimetry
aerodynamic conditions of, 109f (DPIV), 47
alpha, 51, 111f, 194 axial undulatory swimming, 45–46, 43f, 44f
of Anas undulata, 190f, 202f Bernoulli’s theorem, 46–46, 43f, 44f
constant, 43, 53, 90 swimming categories, 44
control of, 75, 77 oscillatory swimming, see Oscillatory
flight and fluid mechanics, 32, 33f swimming
optimal, 196 Archaeopteryx, 11, 163–178, 254, 255, 300,
Pennycuick’s theoretical angle 320
of attack, 205 feather evolution, 178–181
of pied flycatchers, 210f flight
positive, 49, 194 in birds, see under Birds
of Tyto alba, 220f hypothetical stages, 167f
Anguilla anguilla (eel), 44 gliding, 127
anguilliform movement, 45, see also ground-up or trees-down origin of flight,
Anguilliform swimmers 167f, 166–178
anguilliform swimming, 62f, 99–100 claws, 167–170, 169f, 171f
axial undulatory swimming, 45–46, 43f, powered or unpowered flight, 170–178,
44f 172f, 174f

© Springer-Verlag Berlin Heidelberg 2015 339

T. Lingham-Soliar, The Vertebrate Integument Volume 2,
DOI 10.1007/978-3-662-46005-4
340 Index

localities of specimens, 165f silent flight, 218–220, 219f, 220f

specimens of, 164f slow-flying, wingbeat kinematics in,
Argentavis (extinct giant vulture), 149 208–209, 208f
Ascaris lumbricoides, worm cuticle, 64f costs of bird flight, offsetting
Asian gliding frogs, 111 bounding flight, 221
Aspect ratio (AR), 33, 34, 34f flying in formation, 237–239, 237f, 238f
AR wings soaring, 221–237, 222–229f, 231–235f,
with pointed tips, 35–37, 36f, 37f 233t
with slotted tips, 37–38, 38f feather evolution, 178–181, 179–181f
of caudal fin, 53 flapping flight phenomenon, 192–202
Auxiliary wing, 36f, 37 departures and arrivals, 199–202,
Avian wing musculature, anatomical organiza- 200–202f
tion of, 184, 184f early observations of, 192–193, 193f,
Axial subundulatory swimming , 46–51, 194f
48f, 49f, 50f. See also Aquatic understanding, 193–198, 195–198f
locomotion flight control center, 187–192, 189–191f
Axial undulatory (anguilliform) swimming , birds brains, 189–192, 191f
45–46, 43f, 44f, 62f.See also Aquatic β-keratin, influence on bird evolution
locomotion feather biomechanics at microstructural
level, 247–257, 250f, 253f
feather microstructure, 241–247, 242f,
B 243f, 245–249f
Basiliscus plumifrons (Jesus lizard) feather structure at angstrom and
collagen in integument, 270f molecular levels, 239–241, 240f
crest in, 269 power of flight, 199–207
Bats, 39, 105, 127, 149 power curve, 203–205, 204f, 205f
aerodynamics, new developments in, wake vortices, 205–207, 207f
153–159, 155f unique flight apparatus of, 182–187
and pterosaurs, comparison, 133–134 flight feathers, 185–187, 185–187f
wing structure and mechanics, 139, 140f, flight muscles, 182–185, 184f
150–159, 151f, 152f, 154f wing structure, 182, 183f
in Cynopterus brachyotis, see Birds are Dinosaurs (BAD) debate, 300–314
Cynopterus brachyotis (short-nosed cladistics and, 310–314
fruit bat) origin of birds, 301–304, 312f
hand wing, special arrangements, prime time journals, 314
150–151 science and falsifiability criterion,
in Rousettus aegyptiacus, 151f, 152f, 305–309
see also Rousettus aegyptiacus Boundary layer
(fruit bat) over aerofoil, 40–41
Beipiaosaurus (theropod dinosaur), 316 concept of, 20
elongated broad filamentous feathers drag function, 30
(EBFFs) in, 274 in flying upside-down, 39
features of, 274–276, 275f and Reynolds number, 152–153
and fundamental rules of scientific Thompson’s theorem, 28
methodology, 276–277 wing, airflow on, 154f
Bernoulli equation, 19–20, 20f, 21, 23 wind-tunnel research, 203
drag force, 29–30 Bounding flight, 208f, 221
for lift process, 38–39 Bound vortex, 27–29
Birds. See Bats gliding experiment, 28
Archaeopteryx, 163–178, 164f, 165f, 167f, trailing vortices, 29f
169f, 171f, 172f, 174f Bubo africanus, cross-fiber architecture, 247f
behavior Buteo rufofuscus (jackal buzzard)
hovering, 209–217, 211f, 212f, 215f, flight strokes of, 195f
217–219f fundamental motions, 194
Index 341

C conditions affecting, 264

Cantilever system, 8f, 9 degrading experiments, 267, 268f, 283
I-beams, 7–9 in Ichthyosaurus, 283f
nonuniformly distributed load, 9f fossilized, 254
in vertebrates, 10f in Jurassic ichthyosaurs, 266
Carcharhinus falciformis (silky shark), 62 in Kulindadromeus zabaikalicus, 287, 288
Carcharhinus limbatus (blacktip shark), 62 in Gallus gallus (chicken), 290f
placoid scale in, 63f, 64 subdermal connective tissue
Carcharias taurus (ragged-tooth sheath (SDS), 73
shark), 44, 83 tuna dermis, 70–71
dorsal fin of, 79, 82f type I, 266f
sub-anguilliform swimming, 62f in vertebrate (mainly reptile) integument,
Carcharodon carcharias (white shark), 49 270–271f
caudal fin of, 84, 85 in Xianglong’s patagium surface,
dermal fibers of, 87–88, 87f, 88f 124, 125f
dorsal fin of, 77, 79–83, 80f, 82f, 83 Columba livia (rock dove), 172
hierarchical fiber architecture, 92 power curve, 203–204
integumentary fibers in, 267 wake vortices, 205, 207f
oscillatory swimming, 50, 52f, 62f Compsognathus (theropods), 168, 170
rachis and barbs epicortex, cross-fiber Computational fluid dynamics (CFD), 23–24
architecture of, 254 Conservation of momentum, 25, 39
stratum compactum fibers of, 88–89, 89f COPE (Commission on Publication Ethics)
Caretta caretta (turtle), 269 Report, 315–316
collagen in integument, 270f Codes of Conduct for Editors and
Caudal fin dermal fibers, 84–89, 85–89f Publishers, 299
Carcharodon carcharias, see Carcharodon Coping with Fraud, 315–321
carcharias (white shark) Coragyps atratus (black vulture), 230, 233f
cross-sections of, 86f Corvus brachyrhynchos (American
dermal fibers of stratum compactum, 85 Crow), 172
fiber organization in, 84 Costs of bird flight, offsetting
functional interpretations, 88–89 bounding flight, 221
tensile load tests, 86–87 flying in formation
Caudal peduncles, 54f variable shape, of bird flocks,
collagen fibers in, 55 238–239
Chiloscyllium punctatum (bamboo shark), V formation, of bird flocks, 237–238,
vortex patterns of, 48 237f, 238f
Chrysopelea paradisi (ribbon-flat paradise tree soaring, 221–237
snake) mechanisms of, 222–225, 222f
gliding, 112–115, 113–116f. See also slope, 223–224, 223–225f
Snakes wing shapes and, 226–230, 226–229f,
Cladistics, 303, 304, 309 231f, 232f
and Birds are Dinosaurs debate, 310–314 wing tip shapes and, 230–237,
anti cladistics, 329 233–235f, 233t
Claws, 167–170 Cosymbotus (parachuting geckos), 116
in Archaeopteryx, 169f, 171f Critical Griffith crack length, 6
Coelurosauravus elivensis (fossil reptilian Crocodilus niloticus, collagen in integument,
reptile), gliding, 117, 117f, 122, 123 271f
Collagen fibers, 65, 68 Culugos, gliding, 120–122, 121f
architecture, 269 Cynocephalus (cat-sized Asiatic glider), glid-
in Ascaris lumbricoides, 64f ing, 120
in caudal peduncle Cynopterus brachyotis (short-nosed fruit bat),
in dolphins, 54 155, 156
in shark, 252 PIV analysis of, 158f
in thunniform shark, 84 wind tunnel experiments, 155, 156
342 Index

D E
Daption capensis (cape pigeon), 227f Elastic constants, 3–7
Desmodus rotundus (vampire bats), 145, 146, fracture, 4–6
149 Poisson’s ratio, 3–4
Diamond-shaped shoals, 56 shear modulus, 3
Digital particle image velocimetry (DPIV), stiffness, 3
47–49, 50f, 84 Elastic deformation, 3
Dimensionless theorems, 14–18 Elongated broad filamentous feathers
Froude number, 17 (EBFFs), 274
Prandtl number, 17 in Beipiaosaurus, 274–277, 275f
Reynolds number, 15–17 features, 275–276
Strouhal number, 18 Energy saving devices, in vertebrate
Dimorphodon, 131, 132 swimming
Dino-fuzz, 138 diamond-shaped shoals, 56
Dinosaur porpoising, 56–58, 57f, 58f
Birds are Dinosaurs debate, 300–314 reverse von Kármán vortex street, 55–56,
cladistics and, 310–314 55f
origin of birds, 301–304, 312f Eomys quercyi (fossil mammal), 126, 126f
prime time journals, 314 Epaxial muscles, in evolution of, 75, 76f
science and falsifiability criterion, Euler equation, 19
305–309 in aquatic locomotion, 43
feathered dinosaurs into mid-Triassic, beam theory, 7, 175, see also I-beams
pushing in foundation of hydrodynamics, 15
Beipiaosaurus, 274–277, 275f number, 15f
Psittacosaurus, 277–279, 278f Extant reptiles, dermis in, 269–271
ornithischian, 289, 289f collagen in vertebrate integument,
rufous-colored, 279–284, 281f, 283f 270–271f
Diomedea chrysostoma (grey-headed alba-
tross), 227f
Diomedea exulans (wandering albatross) F
skeletons, 144f Falco peregrinus (peregrine falcon)
slope soaring, 226, 227, 227f, 229f, 236 flight feathers in, 186f
Diomedea melanophris (black-browed alba- flight microstructure in, 243f
tross), 37f, 227f rachis epicortex, 246f
Dolphin(s) Falco tinnunculus (kestrel)
death of, 266–269 feather microstructure, 243f
dermis, 72–77, 73f, 74f, 76f, 77f wake vortices, 206, 207f
humpback dolphin, caudal peduncle of, 75, Feather(ing), 194
77, 77f biomechanics at microstructural level,
integumentary fibers in, 266–269, 247–257
268–269f crack-stopping, 248–250, 250f
longissimus muscle, 74f ductile tearing, 254
oscillatory swimming, 53 evolution of birds and, 254–257
porpoising, 57, 58f stiffness, ductility, and buckling, 251,
scombrid myomere, 73f 253f
superficial tendon, 74f torsion and flexion, 252–254
Dorsal fin, 78–83, 80f, 82f, 83f evolution, 178–181, 179–181f
Draco, gliding, 115–118, 117f, 122–123, 125 fiber microstructure, 241–247, 242f, 243f,
Drag, 29–32 245–249f
coefficient, 15f structure at angstrom and molecular levels,
on golf ball, 41, 42f 239–241, 240f
Dsungaripterus, 132 Fibers, 241–247. See alsounder Feather(ing)
Dynamic similarity, 18–19, 19f Ficedula hypoleuca (flycatchers), 157
Index 343

Fish. SeeAnguilla anguilla (eel); Dolphin(s) Fracture energy. See Work of fracture
aquatic locomotion, see Aquatic Freedom of expression, 295–296
locomotion Fregata magnificens (magnificent frigate bird),
axial subundulatory to suboscillatory 228, 230, 233f
swimming, 46–51 Friction drag, 20
caudal fin in tiger shark, 48f Froude number (Fr), 15f, 17
cine film of young eel, 45f Fulmarus glacialis (fulmar petrel), 227
horizontal swimming in shark, 49f
hydrodynamic purpose of asymmetric
tail shape, 46 G
oscillatory motion of tail, 50f Galeocerdo cuvier (tiger shark)
swimming mode of eel, 47f axial suboscillatory swimming, 46f
thunniform swimmers, 50f dorsal fin of, 80f, 82f, 83
oscillatory swimming, see Thunniform during steady horizontal swimming, 49f
sharks; Thunniform swimmers sub-carangiform or sub-oscillatory swim-
Fixed wings, concept of, 192 ming, 62f
Flapping flight, evolution of, 127–129 vortex wake, 50f
arboreal habitat, complexity, 129 Galeopterus variegatus (Malayan colugo),
landing process, principles, 127–128 121f
non-equilibrium glides, 129 Gallus domesticus (domestic chicken), 269
transition from steady state to unsteady collagen in integument, 270–271f
state gliding aerodynamics, 128–129 Gallus gallus (chicken), 172
Flapping flight phenomenon, 192–202 cross-fiber architecture, 247f
departures and arrivals, 199–202, 200–202f feather rachis of, 242f, 243f
early observations of, 192–193, 193f, 194f rachis epicortex, 245f, 246f
understanding, 193–198, 195–198f ribbon-like fibers in tibia, 290, 290f
Flight and fluid mechanics, 25–38 Geronticus eremita (northern bald ibises), 238f
aerofoil, 27, 27f Glaucomys sabrinus (northern flying squir-
angle of attack, 32, 33f rels), 120
bound vortex, 27–29 Gliding, 105–129
drag, 29–32 aerodynamics of, 107–110, 107f, 109f
wing planform, 33–38 amphibians, 110–112
Flight by membrane, 131–159 definition of, 105
bats, 149–159 equilibrium, 107
pterosaurs, 131–148 flapping flight, evolution of, 127–129
Flight control center, 187–192, 188–190f fossil gliders, 122–127, 124–126f
birds brains, 190–192, 191f mammals, 118–122, 119f, 121f
Flight feathers, 185–187, 185–187f reptiles, 112–118, 113–117f
Flight muscles, 182–185, 184f Glossophaga soricina (Pallas’ long-tongued
Fluid, definition of, 13–15 bats), 157, 158f
Fluid mechanics, 13–25 Gravitational gliding, 222–225
dimensionless theorems, 14–18 dynamic soaring, 224
dynamic similarity, 18–19, 19f slope-soaring
fluid responses, 19–25 Procellaria aequinoctialis, 223f
flight and, 25–38 Thalassarche caute, 224f, 225f
Fluid responses, 19–25 soaring flight, 222f
Bernoulli equation, 19–20, 20f Great lateral tendon (GLT), 75
structures in fluid motion, shape Griffiths fracture, 4, 6
of, 20–24 Ground-up or trees-down origin of flight, 167f,
Navier-Stokes equation, 25 167–178
Flying upside-down, 39 Archaeopteryx, seeArchaeopteryx
Foam, 241–247 claws, 167–170
Forces acting on materials, 2–7 Gypaetus barbatus (cape bearded vulture),
Fossil gliders, 122–127, 124–126f 234, 234f
344 Index

flapping flight cycle of, 235f Psittacosaurus, 277–279, 278f

Gyps caprotheres (cape vulture), 234, 234f ichthyosaur soft tissue, see Ichthyosaur
with slotted wing tips, 38f soft tissue
Gyps fulvus (Eurasian griffon vulture), 236 Kulindadromeus zabaikalicus, 287–291
Gyps rüppelli (Rüppell’s griffon vulture), 226, rufous-colored dinosaur, 279–284, 281f,
236 283f
Isurus oxyrinchus (mako), 62, 64
dorsal fin of, 77, 78f
H oscillatory swimming, 50, 52f
Haliaeetus vocifer (African fish eagle,), 189f
Harm principle, 296
Hatzegopteryx (azhdarchid), 144f J
H-beams. See I-beams Jeholopterus (pterosaur), 138, 142
Helical fiber system, non-thunniform sharks,
66–68, 69f
Hemidactylus species (geckos), 117 K
Hovering, 209–217, 211f, 212f, 215–219f. See Katsuwonus pelamis (Norfolk spot), 70, 71f,
also under Hummingbirds 72
Hummingbirds β-keratin, influence on bird evolution
backward flight in, 214–216 feather biomechanics at microstructural
flight musculature and muscle activity in, level, 247–257
216, 217f crack-stopping, 248–250, 250f
hovering, 209–218 ductile tearing, 254
aerodynamics, 216–217, 218f evolution of birds and, 254–257
wing beat cycles in, 216–217, 219f stiffness, ductility, and buckling, 251,
wing vortex systems in, 212f 253t
Humpback dolphin, caudal peduncle of, 74, torsion and flexion, 252–254
77, 77f feather microstructure, 241–247, 242f,
Hydrobates pelagicus (sooty black petrel), 226 243f, 245–249f
feather structure at angstrom and molecular
levels, 239–241, 240f
I Kuehneosaurus species (extinct gliding rep-
I-beams, 7–9, 7f tiles), 117f, 118, 122, 123
Icarosaurus seifkeri (fossil reptilian reptile), Kulindadromeus zabaikalicus ((ornithischian
gliding, 117f, 118, 122, 123 dinosaur). See Collagen fibers
Ichthyosaur dermis, 89–99, 90–94f, 96–98f integumentary fibers in, 287–291
in biomechanics, 94 Kutta-Joukowski theorem, 39
crossed-fiber architecture, 90–91
problems, 90
soft tissue preservation, 92, see also L
Ichthyosaur soft tissue Lagging, 194
Ichthyosaur soft tissue, 263–266, 265f Laminar flow
Ichthyosaurus in horizontal surface, 22
collagen fibers, decomposition of, 283f in straight pipe, 20
fiber architecture in, 95 of water from faucet, 16f
specimen, GLAHM V1180a, 91, 92f, 97f Lamnid shark dermis, 77–89
Integumental taphonomy, 263–291 caudal fin dermal fibers, 84–89, 85–89f
dolphin death of, 266–269 dorsal fin, 78–83, 80f, 82f, 83f
extant reptiles, dermis in, 269–271, Law of inertia, 12
270–271f Leiostomus xanthurus (skipjack tuna), 70,
feathered dinosaurs into mid-Triassic, 71f, 72
pushing Leptonycteris yerbabuenae (long-nosed bats),
Beipiaosaurus, 274–277, 275f 157, 158f
Index 345

Lift Oscillatory swimming , 50–55, 52f, 53f.

Bernoulli equation for, 38–39 See also Thunniform swimmers
coefficient, 15f caudal fin
-to-drag ratio, 107, 107f, 110 aspect ratio (AR) of, 53
Newton’s laws of motion for, 38–39 of thunniform sharks, 52f
Lizards, gliding, 115–118, 117f. See also in dolphins, see Dolphin(s))
Agama utricollis (agamid lizard) lift-based swimming mode, 51
Basiliscus plumifrons (Jesus lizard); Otus leucotus (white-faced owl), native
Reptiles medullary pith of, 253f

M P
Macrelaps microlepidotus (black snake), 269 Pachyptila desolata (dove prion), 227f
collagen in integument, 270f Particle image velocimetry (PIV) , 156, 158f.
Macronectes (giant petrel), 227f See also Digital particle image velo-
shoulder lock, 229 cimetry (DPIV)
Macrotus (bats), 149 Peer review, 296–300
Mammals, gliding, 118–122, 119f, 121f areas of conflict of interest, 299
culugos, 120–122 peer censorship, 296
Malayan colugo, 121f recommendations, 299
squirrels, 118–120 rivalry and bias in science, 300
flying squirrel, 119f system, change in, 297
Mecistotrachelos (diapsid lizard-like lepido- Universal Declaration of Human
saur), 123 Rights, 296
Merops apiaster (bee-eater), 208, 208f Pelecanus occidentalis (brown pelican),
Modulus of elasticity. See Young’s modulus 228, 230
Modulus of rigidity. See Shear modulus aspect ratio and wing tip effects in, 233f
Molurus bivittatus (Burmese python), 269 Pelicans, 232
collagen in integument, 271f energy saving, 237
Montanazhdarcho (azhdarchids), 132 flight of, 194f
Morus capensis (Cape gannet) Petaurillus (dwarf flying squirrel), 119
landing, 202f Petaurista leucogenys, 110
slide-soaring, 236 gliding, 119f
taking-off, 198–200, 200f Phalacrocorax atriceps (blue-eyed
Movable wings, 192 shag), 228
Phoebetria palpebrata (light-mantled
N sooty albatross),
National Geographic Society, 322–330 227f, 229
apartheid South Africa, education and Pigeon, taking-off, 147f
freedom in, 324–327 Placoid scale, 61
US Constitution’s First Amendment, Poephila guttata (zebra finch) , 290
328–330 Pointed tips, high AR wings with,
Navier-Stokes equation, 22–25, 201 35–37, 36f, 37f
Newton’s laws of motion, 11–13, 206 Poisson’s ratio, 3–4
for lift, 38–39 Porpoising, 56–58, 57f, 58f
Non-thunniform sharks Power curve, 203–205, 205f
deeper dermis of, 65–70 induced power, 204f
helical fiber system, 66–68, 69f U-shaped, 203, 205, 207, 226
torsional stiffness, 68–70 using trained pigeons, 203
Powered flight, 170-178, 172f, 174f,
203–207
O power curve, see Power curve
Oceanites oceanicus (Wilson’s petrel), 228 wake vortices, 205–207, 207f
constant wing span, 227f Prandtl number (Pr), 15f, 17
346 Index

Pressure drag, 20–21 myomere, 73f

Procellaria aequinoctialis (white-chinned Norfolk spot, 71f
petrels), 228 skipjack tuna, 71f
constant wing span, 227f Seabirds, 147
slope-soaring, 223f versus vultures, 230, 232
Protofeathers, 264 wing tip shapes and sharing, 230, 233f
Psittacosaurus (ornithischian dinosaur) Seagulls, 131
integumentary fibers in, 274, 277–279, flight of, 194f
278f wing revolution, 193f
ornithischian dinosaur, 287, 289f Sharovipteryx (pterosaur precursor), 146
Pteranodon (giant ornithocheiroid), 132, 142, gliding, 123, 124
143, 144f Sharovipteryx mirabilis (flying reptiles), 123
male and female, 133f Shear modulus, 3
skeletal reconstruction of, 145f Shear stress, 4f
Pterodactylus kochi, 132f Silent flight, 218–220, 219f, 220f
Pterosaurs, 131–148 Sinomis santensis (perching bird), 168
body size, 142–147 Sinornithosaurus, integumental appendages
feeding behavior, 147–148 of, 179f
patagium, 141 Sinosauropteryx (basal theropod), 138, 167,
pteroid bone in, 139, 139f 301, 316–319
wing, 133–142 death by volcano, 284–287, 285f, 286f
cross-fiber architecture, 136, 137f, 138f ordeal by fire, 286–287, 286f
structure of, 135f integumental appendages of, 179, 179f,
Ptychozoon (parachuting geckos), 116, 117 180f
integumentary fibers in, 264–266, 265f,
Q 271–274, 272–273f, 288, 290
Quetzalcoatlus northropi (pterosaur), 132, rufous-colored dinosaur, 279–284, 281f,
142, 143, 144f 283f
Slotted tips, broad low AR wings with, 11f,
37–38, 38
R Slow-flying, wingbeat kinematics in, 208–209,
Reptiles 208f, 210f
extant, dermis in, 269–271, 270f, 272f Snakes
gliding, 112–118, 113f–117f gliding, 112–115, 113–116f
lizards, 115–118 body cross-section for, 113f
snakes, 112–115 paradise tree snake, 113f
body cross-section for gliding, 113f Soaring, 221–237
movement through air, 114f animal platforms, comparison of, 144f
paradise tree snake, 113f mechanisms of, 222–225, 222f
Reverse von Kármán vortex street, 55–56, 55f slope, 223–224, 223–225f
Reynolds number (Re No), 15–17, 15f, 21 wing shapes and, 226–230, 226–229f,
Rhacophorus dulitensis (tree frog), 111 231f, 232f
Rousettus aegyptiacus (fruit bat) wing tip shapes and, 230–237, 233–235f,
air flow on wing, 154f 233t
forces acting on digit, 152f Sordes pilosus (pterosaur), 136, 138, 141, 143
wing structure and mechanics, 150–153, Spanning, 194
151f, 152f Squirrels, gliding, 118–120, 119f.See also
Rufous-colored dinosaur, 279–284, 281f, 283f Mammals, gliding
Rynchops nigra (skimmer), 148, 148f Stenopterygius quadricissus (extinct Jurassic
ichthyosaur), 44, 77, 90, 90–92f
dorsal and caudal fin crossed-fibers in,
S 94–96, 94f, 96f
Scansoriopteryx (fossil), 180–181 hierarchical fiber architecture, 92–93, 93f
Scombrid, 70, 75 integumentary fibers in, 264, 265f
Index 347

thunniform swimmers, 50f V

Stiffness of material, 3 Velocimetric particle imaging (VPI), 23
Stokes number, 15f Vertebrates
Strain, 2–3 epaxial muscles, in evolution of, 75, 76f
Stress, 2, 3f swimming, see Vertebrate swimming
Strouhal number (St), 15f, 18 Vertebrate swimming, 61–64
Structures in fluid motion, shape of, 20–24, cuticle
21f, 22f of Ascaris lumbricoides, 64f
Sturnus vulgaris (European Starling), 172f, of Amphiporus lactifloreus, 67f
238 different lifestyles and swimming poten-
Subdermal connective tissue sheath (SDS), 73, tials, 62f
74, 74f, 268f energy saving devices in
Sub-oscillatory swimming, 62f diamond-shaped shoals, 56
Galeocerdo cuvier, 62f porpoising, 56–58
Supercomputers, turbulence and, 40–42, 42f reverse von Karman vortex street,
Sylvia atricapilla (blackcap), 157, 209 55–56
functional findings, 68–70
helical fiber system, 69f
T marine vertebrates, deeper dermis of
Taeniopygia guttata (zebra finch), 221 anguilliform swimmers, 99–100
Tensile strength, 5 non-thunniform sharks, 65–70
Thalassarche caute (shy albatross), 224f, 225f thunniform swimmers, see Thunniform
Thin-walled cylinders, 9–11, 11f swimmers)
Thunniform sharks placoid scale, 63f
caudal fin of, 52f V formation, of bird flocks, 237–238, 237f,
oscillatory swimming, 50–55, 53f, 62f 238f
Thunniform swimmers Viscosity
dolphin dermis, 72–77, 73f, 74f, 76f, 77f definition of, 14
ichthyosaur dermis, 89–99, 90–94f, 96–98f Newton’s law of, 14
lamnid shark dermis, 77–89 von Kármán vortex street, 22, 23f
caudal fin dermal fibers, 84–89, 85–89f reverse, 55–56, 55f, 205
dorsal fin, 78–83, 80f, 82f, 83f Vortex/vortices
tuna dermis, 70–72, 71f bound, 27–29
Tianyulong (dinosaur), 317 trailing, 29f
Torsional stiffness, non-thunniform sharks, Vultures, 226
68–70 and seas birds, 232–237
Triakis semifasciata (leopard shark), 48 wing tip shapes and sharing, 230
Triangular attachment area (TAA), 73f
Tuna dermis, 70–72, 71f
Turbulent flow, 24f W
and supercomputers, 40–42, 42f Wake vortices, 205–207, 207f
of water from faucet, 16f Wing(s)
Type I collagen fibers, 266f beat frequencies, in flying animals, 213f
Tyto alba (barn owl), 220f feather configurations, 197, 198f
silent flight in, 218–221, 220f fixed, 192
loading, 33–34, 34f, 35f
motions of, 193
U movable, 192
Unique flight apparatus, of bird, 182–187 planform, 33–38
flight feathers, 185-187, 185–187f shapes, and soaring, 226–230, 226–229f,
flight muscles, 182–185, 184f 231f, 232f
wing structure, 182, 183f structure, of bird, 182, 183f
US Constitution’s First Amendment, 328–330 tip shapes, and soaring, 230–237,
Unpowered flight, 105. See alsoArchaeopteryx 233–235f, 233t
348 Index

Wing/air currents, 222–225 Y

Winglet. See Auxiliary wing Young’s modulus, 3
Work of fracture, 4–7, 4f, 5f, 6f

Z
X Zheijangopterus (azhdarchid), 146
Xianglong zhaoi (gliding lizard), 123, 282
holotype, 124f
wing loading of, 125
Xiaotingia, 179, 300