14 Handbook of Avian Medicine - Tully _ Dorrestein _ Jones - 2nd Edition

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1 – The development of avian species 1
2 – Basic anatomy, physiology and nutrition 25
3 – The physical examination 56
4 – Clinical tests 77
5 – Imaging techniques 85
6 – Nursing the sick bird 101
7 – Psittacine Birds 138
8 – Passerines 169
9 – Raptors 209
10 – Cranes 243
11 – Ratites 258
12 – Waterfowl 275
13 – Galliformes 309
14 – Ramphastids 335
15 – Pigeons 350
16 – Seabirds 377
17 – The Management of a Multi-species Bird Collection in 404
a Zoological Park
Appendix I - Haematology/Biochemical reference ranges 437
Appendix II - Conversions to Système International (SI) units 447
Appendix III - Adult bird weights 449
Appendix IV - Scientific names of common psittacine species 451
Index 455
Table of Contents
vii
Acknowledgements
It is satisfying as editors to have a work be well received 
by the veterinary community after the intense effort 
of compiling the material. Our goal in editing the first 
edition was to produce a basic avian medical text that 
brought forth the collective knowledge and expertise 
of a respected group of international authors. Based 
on the response through multiple printings and a 
request to publish a second edition we believe the goal 
was attained. We as editors also know that veterinary 
medicine and in particular avian veterinary medicine 
is a moving target as scientific discoveries and medical 
advances are frequently achieved. As with the first edi-
tion, we have called upon many of the original authors 
as well as new contributors to exceed the expectations 
of the veterinary community regarding a basic avian 
medicine text. We wish to thank existing authors for 
their continued commitment to this text as well as those 
participating for the first time. To our colleagues in the 
Association of Avian Veterinarians, we thank you for 
contributing to and demanding quality avian medicine. 
The advances noted in this book can be directly attrib-
uted to the enthusiastic members of this worldwide 
organization.
Again the support staffs for the three editors were 
invaluable assets: at LSU, Harry M. Cowgill, medical 
photographer, and Michael L. Broussard, graphic artist, 
who aided in figure development; at the NOIVBD labo-
ratory, Marianne van der Zee for photographic sup-
port. We are also grateful to the collegial support from 
associates and staff members that is so important on a 
daily basis, but never more so than when working on a 
medical textbook: Drs Javier Nevarez, David Guzman, 
and Shannon Shaw at LSU; Gail and the two Emmas at 
Dr Alan Jones’ Clinic; and Anita Visser at the NOIVBD 
laboratory and Tonnie van Meegen (NOP) were all 
instrumental in their support during the formulation 
and completion of this text.
The editors would also like to thank our publish-
ers Elsevier for their commitment to a second edition. 
As always, patience and support are cornerstones to 
publisher/editor/author sanity during the writing proc-
ess and we were fortunate to work with the best: Joyce 
Rodenhuis, Commissioning Editor Veterinary Medicine; 
Rita Demetriou-Swanwick, Development Editor; and 
especially Ewan Halley, our Development Editor, who 
guided the book through the majority of the editing 
process. Thank you for the early mornings, long days, 
and late nights, not to mention the continual stimula-
tion for results!
Two of the editors would be remiss for not thanking 
a colleague and friend who has contributed more than 
his share of editorial duties, Dr Alan Jones. Alan, thank 
you for joining this group in a project that we feel is a 
labour of love; your work was professional, first class, 
and added significantly to the timely production of the 
book.
Finally, a heartfelt thank you for the unswerving loy-
alty of our wives Susie Tully and Elaine Jones, partner 
Marianne van der Zee, plus our families who accept our 
professional ambitions to advance avian medicine in the 
face of added stress associated with editing an interna-
tional avian medical text.
CHAPTER 12: BASIC ANATOMY, PHYSIOLOGY AND NUTRITION
ix
Foreword
…look into the clear bright eyes of the bird whose 
body equals yours in physical perfection, and whose 
tiny brain can generate a sympathy, a love for its mate, 
which in sincerity and unselfishness suffers little when 
compared with human affection.
William Beebe,
The Bird 1906
Birds have long enthralled the human race and thereby 
influenced diverse cultures and civilizations. Thousands 
of years ago the Incas in South America and the then 
denizens of Mesopotamia (present-day Iraq) kept birds 
of various types. At about the same time, the Ancient 
Egyptians were probably the first to collect birds; in 
1500 BC Queen Hatshepsut organised an expedition 
to add new species to her private collection. A thous-
and years or so later Greek and Roman scholars such 
as Aristotle, Pliny and Varro studied birds, including 
parrots, and published detailed observations on their 
biology. Science flourished under Arab scholars dur-
ing the so-called Dark Ages in Europe and this period 
spawned seminal writings on numerous aspects of the 
natural world, including birds and other animals, as 
well as medicine, geology and astronomy. With the 
Renaissance came renewed scientific interest in Europe 
and Leonardo da Vinci, followed by anatomists in 
England, Germany, Italy and the Netherlands, carried 
out painstaking dissections of many animal species. 
These and others produced scholarly descriptions and 
drawings of birds that are, in many respects, unequalled 
today. In the 18th century John Hunter, the great sur-
geon, anatomist and champion of the veterinary profes-
sion, explored the links between structure and function 
in animals. Amongst many other great discoveries, 
Hunter described the air-sac system of birds and studied 
avian matters as diverse as the production of crop-milk 
in pigeons, the seasonal development of the gonads in 
sparrows and the healing and misalignment of fractures 
in an eagle.
Neither is medical care for birds a novel concept. In 
1486 in England, for example, advice on the diagnosis 
and treatment of diseases of trained hawks was given 
in the Boke of St Albans. This was written by Dame 
Juliana Berners; a reminder of the prominent role played 
by women in avian science, even 500 years ago! The 
popularity of the sport of falconry in Europe over the 
succeeding three centuries ensured that publications on 
raptors continued to appear. There was also a growth of 
interest in the keeping of pigeons, parrots, finches, crows 
and other birds as pets. Much affection was often lav-
ished upon these birds, even during periods when the 
human population was beset by rumours of war and 
social unrest, as exemplified by the following entry in 
one of the famous diaries (1665) of Samuel Pepys:
This night when I came home I was much troubled to 
hear that my poor Canary Bird, that I have kept these 
three or four years, is dead.
It was not, however, until the 19th and early 20th cen-
turies, with the genesis of the understanding of patho-
gens, that serious attention started to be paid in Europe 
and North America to the diagnosis and control of dis-
eases of captive birds. Even so, progress was slow and 
the input by veterinarians remained limited.
The situation has now changed beyond recognition 
and over the past three decades our knowledge and 
understanding of bird diseases has advanced extraordi-
narily. Much of the credit for this is owed to the ‘pio-
neers’ of avian medicine, amongst them the editors and 
many of the contributors of this book, who have helped 
to transform avian medicine into a bona fide, state-of-
the-art, scientific discipline.
I was honoured to be asked to write the foreword to 
the first edition of this book in 2000 and am delighted 
to have been invited to do so again for the second, 
in 2009. As before, my first comment on the book is 
to applaud its international orientation. The editors 
hail from three different countries and the twenty con-
tributorsfrom seven. This spread – Australia, Europe 
and North America – is not global but it is an impor-
tant reminder of the international significance of avian 
medicine, in terms not only of treating individual sick 
birds but also of monitoring and promoting the health 
of wild (free-living) populations. The latter is a pressing 
x
FOREWORD
need for a number of reasons, not least because of curr-
ent concerns about avian influenza and other diseases 
that are a threat to the health of humans and domestic 
stock. In addition, of course, there is a desperate need 
for more information about the part that infectious and 
non-infectious diseases play in the regulation of num-
bers of wild birds, particularly those that are under 
pressure for other reasons. It is now widely accepted 
that veterinarians and others with specialist knowledge 
of avian health and host/parasite relations can play a 
vital part in the conservation of endangered and threat-
ened species. Their contribution in this respect is much 
enhanced if they have an understanding of aviculture 
as well as sound professional knowledge of pathology, 
parasitology, medicine or surgery. In my own work 
overseas over four decades I have witnessed many such 
contributions to conservation. For example, the survival 
and recovery of the Mauritius kestrel (Falco punctatus), 
the pink pigeon (Columba mayeri) and other Indian 
Ocean species, the populations of which were in a par-
lous state in the 1970s, owe much to close, unselfish, 
collaboration between veterinarians and biologists, 
some of them self-funded. There have been similar suc-
cesses in avian species-conservation elsewhere and I 
have been fortunate to have seen some of these projects 
for myself – in New Zealand, for example, where many 
endemic birds are now relatively safe. It is encouraging 
that young people, some with a veterinary background, 
some from other disciplines, want to involve themselves 
in such conservation projects and thereby contribute to 
the protection of wildlife and their habitats. This usually 
means serving in different, sometimes difficult, parts of 
the world and being willing and able to collaborate with 
local communities. Examples of such enterprise are to 
be found documented in various publications, including 
Notes from the Field in the Journal of Avian Medicine 
and Surgery and project reports in the Bulletin of the 
British Veterinary Zoological Society.
The editors and authors of this book are familiar 
names to those who keep or treat birds. They are all 
veterinarians but, without exception, have a personal 
affinity for birds as animals and an awareness that those 
from other backgrounds, such as animal behaviourists, 
ecologists and nutritionists, can also contribute to avian 
health, welfare and conservation.
Those of us who keep or tend members of the class 
Aves owe Tom Tully, Gerry Dorrestein and Alan Jones 
a debt of gratitude for compiling this work and bring-
ing together such a talented team of contributors. In 
so doing, they have helped to promote a better under-
standing of birds and the requirements of these unique 
animals if they are to remain healthy in captivity or in 
the wild. Their book will do much to encourage others 
to contribute to the challenging, but exciting, field of 
avian medicine.
John E. Cooper, DTVM, FRCPath, FIBiol, FRCVS
The University of the West Indies, 2009
CHAPTER 12: BASIC ANATOMY, PHYSIOLOGY AND NUTRITION
xi
Contributors
Brian H. Coles BVSc, FRCVS, Dipl ECAMS
4 Dorfold Way, Upton, Chester, Cheshire, UK
Lorenzo Crosta DVM, PhD
Clinica Veterinaria Valcurone, Missaglia, Italy
Luis A. Cruz-Martinez DVM
Post-Doctoral Fellow, The Raptor Center, Veterinary 
Clinical Sciences, University of Minnesota, St Paul, 
Minnesota, USA
Peter De Herdt DVM, DVSc
Professor of Veterinary Medicine, University of Ghent, 
Director of Clinic for Poultry and Special Animal 
Diseases, Merelbeke, Belgium
Gerry Dorrestein Prof Dr, Dr hc, DVM
Director, Dutch Research Institute for Avian and Exotic 
Animals (NOIVBD), Veldhoven, The Netherlands
Nigel Harcourt-Brown BVSc, FRCVS, Dipl ECAMS
30 Crab Lane, Bilton, Harrogate, North Yorkshire, UK
Don J. Harris DVM
Avian and Exotic Animal Medical Center, Pinecrest, 
Florida, USA
Alan K. Jones BVetMed, MRCVS
Alan K. Jones & Associates, Avian and Exotic 
Veterinary Practice, Sussex & Kent, UK
Maria-Elisabeth Krautwald-Junghanns PD Dr Med Vet, 
Dr Med Vet Habil, Dipl ECAMS FTA
Clinic for Birds and Reptiles, University of Leipzig, 
Leipzig, Germany
Patricia Macwhirter BVSc (Hons), MA, FACVSc
Principal, Highbury Veterinary Clinic, Burwood, 
Victoria, Australia
Glenn H. Olsen DVM, MS, PhD
Veterinary Medical Officer, US Department of Interior, 
US65 Patuxent Wildlife Research Center, Laurel, 
Maryland, USA
Frank Pasmans DVM, PhD, MSc
University of Ghent, Belgium
Michael Pees DrVetMed, Dipl ECAMS
Clinic for Birds and Reptiles, University of Leipzig, 
Leipzig, Germany
Patrick T. Redig DVM, PhD
Associate Professor and Director, The Raptor Center, 
University of Minnesota, St Paul, Minnesota, USA
Ian Robinson BVSc, Cert. SAP, MRCVS
International Fund for Animal Welfare–UK, London, UK
Andrew Routh BVSc, MRCVS
Senior Veterinary Officer, Veterinary Department, 
London Zoo, Regents Park, London, UK
Stephanie Sanderson MA, VetMB, MRCVS
Veterinary Manager, Chester Zoo, Upton-by-Chester, 
Cheshire, UK
Linda Timossi DrVetMed
Clinica Veterinaria Valcurone, Missaglia, Italy
Thomas N. Tully, Jr BS, DVM, MS Dipl ABVP (avian), 
ECAMS
Professor Zoological Medicine, School of Veterinary 
Medicine, Louisiana State University, Baton Rouge, 
Louisiana, USA
Amy B. Worell DVM, Dipl ABVP (avian)
Director, All Pets Medical Centre, West Hills, California, 
USA
xiii
Introduction
The editors and authors are pleased to bring you this 
2nd edition of the Handbook of Avian Medicine. In the 
introduction to the 1st edition, we stated that the specific 
purpose of the text was to provide a resource for the vet-
erinary student, general practitioner and allied staff who 
have an interest in treating the avian patient. We, as 
contributors, feel that this goal was accomplished, but 
much has happened regarding the advancement of avian 
medicine in the 8 years since the publication of that 1st 
edition.
What has not changed in that 8 years is the never-
ending need for up-to-date basic information for the 
increasing number of veterinary students, veterinarians 
and allied staff seeking expertise in the field of avian 
medicine. Advances in this edition are the inclusion of 
all colour images and clinician’s notes. Colour images 
are not only pleasing to the eye but often are important 
in evaluating patients and sample materials collected. 
Clinician’s notes are important highlighted tips (indi-
cated by the flying bird icon in the margin) that will 
give the reader rapid access to information relevant to 
the case in question. More tables, highlighted by col-
our background, are resources to make text referencing 
quick and easy.
We have tried to fulfil a need with this text by calling 
on the worldwide expertise of our authors and editors. 
The multi-authored content utilizes the international 
expertise of the avian veterinary community. This clini-
cally oriented text again focuses on the basic compo-
nents of avian medicine at the beginning, progressing to 
group-specific chapters. If a veterinarian treats birds it is 
very likely that the specialty is not confined to one order: 
this text covers canaries to ostriches. As an underlying 
teaching text it allows for teaching and practice of sound 
avian medicine.
There is a new chapter in this edition that goes into 
the development of avian species. The first chapter will 
give readers an understanding of the formation of these 
wonderful animals. The next five chapters cover the 
basic medical information needed to treat avian spe-
cies in a veterinary hospital. Again this information has 
been updated to incorporate the latest in technologicaland scientific advances. As stated in the first edition, 
the focus of the text is on introductory material and the 
average companion animal practice. If you are a veteri-
nary student or see between one and five birds a week, 
this text is for you. The information in this book will 
allow the veterinarian a comfort zone of knowledge in 
order to evaluate, treat, and/or refer.
Only through knowledge and confidence in the vet-
erinary skills provided will the general public trust 
in medical care for their birds. Competent veterinary 
skills start with the basics, knowing what one can do 
and what one’s limitations are regarding avian practice. 
We hope this book provides a resource of avian medical 
information for veterinarians to formulate the educated 
medical decisions that the bird-owning public has come 
to demand.
Our wish is for this book to reach veterinarians, 
allied technical staff, and veterinary students, who need 
it the most. It has been a pleasure compiling the infor-
mation contained in the 2nd edition of the Handbook 
of Avian Medicine, and we feel the authors have pro-
vided the veterinary community with the most up-to-
date basic avian information for the successful hospital.
Thomas N. Tully, Jr
Gerry M. Dorrestein
Alan K. Jones
xiii
1
CHAPTER 1: THE DEVELOPMENT OF AVIAN SPECIES
The development of avian species
Fossil evidence since the 1800s has suggested that birds 
are descended from reptilian ancestors. More recent evi-
dence places avian species as descendants of the thero-
pod dinosaurs, the bipedal group that also gave rise to 
the iconic predators Velociraptor and Tyrannosaurus. 
Based on phylogenic criteria birds should be considered 
a subgroup of the class Reptilia, albeit a specialized and 
very successful subgroup, rather than being a class of 
their own. A working knowledge of the ongoing debate 
on how birds evolved is helpful in making sense of the 
ways in which modern birds are structured, how they 
function and the diseases they contract.
If a species is to survive and multiply, evolutionary 
change needs to confer immediate advantage for the 
next generation. Key events in the emergence of birds 
from reptiles have included the development of feath-
ers along with changes in thermoregulation, reproduc-
tion, nesting behaviour, respiration, renal function, 
vision and musculoskeletal structure. Bird bones are 
fragile and do not preserve well, so it is not surpris-
ing that there are gaps in the fossil record, particularly 
from the Mesozoic era. Currently known and dated 
bird fossil species do not grade linearly from one to 
another in stratographic context. However, workers 
have analysed primitive and more modern features 
of Mesozoic birds (Chatterjee 1997) and in so doing 
have constructed a cladogram based on a single, most 
parsimonious tree (Fig. 1.1). By comparing this clado-
gram with dated fossils it is possible to construct a 
broad picture of avian evolution with some confidence. 
Knowledge about the palaeogeographical history of 
the earth, the species and ecosystems existing when 
early birds began to emerge, and the biomechanics of 
flight are all important in understanding bird evolu-
tion (Table 1.1; Figs 1.2, 1.3, 1.4, 1.5; Boxes 1.1, 1.2). 
Key sources for the model described here are listed in 
the references, but this is an active area of research 
and details are changing and becoming refined as more 
material emerges.
The amniote egg
Since multicellular organisms first emerged on earth 
some four billion years ago, periods of gradual diversifi-
cation of life-forms have been punctuated with periods of 
abrupt extinctions (De Duve 1995). In the Carboniferous 
period (Fig. 1.2), from around 360 mya, crocodile-
shaped amphibians called labyrinthodonts dominated 
Patricia Macwhirter 1
a landscape vegetated with primitive psilophytes and 
horsetails. The continent of Laurasia, which included 
Europe and parts of North America, had emerged from 
the sea, moved south and coalesced with the southern 
continent of Gondwana to become a single land mass, 
Pangaea. Life-forms between the two land masses inter-
mingled, enabling a vastly increased pool of natural vari-
ation and selection pressures that favoured organisms 
able to reproduce independently of an aquatic environ-
ment. In this context the amniotes emerged. These were 
vertebrates that produced eggs containing specialized 
membranes that provided the developing embryo with a 
liquid environment, gave oxygen in exchange for carbon 
dioxide, stored food as yolk and isolated nitrogenous 
waste (Box 1.3).
The earliest amniotes were anapsids without any lat-
eral openings on the side of the cranium posterior to the 
orbit. Tortoises and turtles have been traditionally clas-
sified as members of the Anapsida. Independently from 
primitive anapsids the synapsids (mammals) evolved 
with a single lower opening on the skull posterior to the 
orbit and the diapsids (reptiles) evolved with two lateral 
openings, one above the other. These openings allowed 
for larger, more powerful jaw muscles for chewing and 
capturing prey. Birds subsequently evolved an avidiap-
sid cranium in which the two lateral cranial openings 
merged into a single opening, allowing for cranial kine-
sis (i.e. movement of the upper jaw relative to the brain 
case) (Figs 1.9 and 1.10).
Mesozoic birds
Approximately 250 mya, a wave of global extinctions 
occurred, wiping out large amphibians over most of 
Pangaea and marking the end of the Palaeozoic era 
(Table 1.1). Descendants of the small reptiles survived 
and evolved to fill a wide range of ecological niches 
as the warm humid climate of the Mesozoic era pro-
gressed. These included the progenitors of turtles, liz-
ards and snakes as well as the archosaurs, a group that 
gave rise to the crocodile family, the pterosaurs and the 
dinosaurs (Box 1.4; Fig. 1.13).
Precisely when ‘birds’ first emerged is an open ques-
tion. Molecular evidence (Table 1.2), places the emer-
gence of birds at around 183 mya, a date consistent 
with most fossil finds, except for Protoavis texensis, a 
Texan bird fossil putatively dated c. 225 mya. Whatever 
the outcome of this debate, timing would depend on 
HANDBOOK OF AVIAN MEDICINE
2
which features were included in the definition of ‘bird’. 
Phylogenetic analysis and analysis of fossils with pos-
sible pro-avian features suggest that birds are embed-
ded in the bipedal dinosaur class Theropoda, probably 
descendant from the Maniraptora, a group that also 
gave rise to dromaeosaurs. A dromaeosaur with a bird-
like furcula (clavicle) has been found in Montana but 
theropod dinosaurs occurred across Pangaea, and there-
fore a Eurasian or American origin for the earliest birds 
could both be consistent with existing fossil evidence 
(Chatterjee 1997, Martin 2002) (Fig. 1.14).
Possible evolutionary steps between ectothermic rep-
tiles and the wide diversity of endothermic, flighted and 
non-flighted avian species of today have generated much 
speculation. Critical bio-geographical events since the 
early Mesozoic era when feathered reptiles made their 
first appearance in the fossil record have included:
 l the gradual break-up of Pangaea and Gondwana 
due to tectonic plate movement
 l the expansion of winged insects and emergence of 
flowering plants, c. 120 mya
Protoavis 
Enantiornithes 
Hesperornithiformes 
Ichthyornithiformes 
Neornithes 
Archaeopteryx 
Aves 
Ornithothoraces 
Pygostylia 
Ornithurae 
Carinatae 
1 
2 
3 
4 
5
Fig 1.1 Aves cladogram.
3
CHAPTER 1: THE DEVELOPMENT OF AVIAN SPECIES
 l the Cretaceous–Tertiary (‘K-T’) boundary disaster 
that marked the end of the Mesozoic era, possibly 
due to a meteor crash near present-day Mexico, c. 
65 mya
 l La Grande Coupure – the separation of South 
America and then greater Australia from 
Antarctica with resultant circumpolar currents, 
global cooling and increased winds, c. 33 mya
 l the establishment of the Panama land bridge, 
c. 2.5mya, reconnecting North and South 
America
 l ongoing sea level changes
 l fluctuating climates
 l the emergence and global expansion of 
mammalian species, especially pinnipeds, felids, 
canids and humans.
For any species, evolution is not linear but rather 
a continuum of a much-branching tree. Genome, life-
time behaviours (‘flock culture’) and landscape weave 
together to create a future that, in time, becomes the 
past. Some signposts along the journey may be marked 
in the fossil record. Evidence of other changes comes 
from current geographical distribution, anatomy, physi-
ology and behavioural patterns of present-day species. 
Stages in the emergence of modern birds that have been 
reflected in the fossil record are described below.
Stage 1 – a bipedal stance, swivel wrist joint and 
long forelimbs (Maniraptora/Dromaeosaurs)
Members of the Maniraptora family, the prime ancestral 
dinosaurs for modern birds, were small agile carnivores 
that probably hunted in packs and were adapted for 
running and climbing. This was reflected in the bipedal 
stance they shared with other theropod dinosaurs as well 
as unique characteristics including swivel wrist joints, 
lengthened forelimbs and caudally directed pubic bones. 
Their rigid stiffened tails could be used as a prop when 
climbing vertical trunks while skin folds on their fore-
arms might assist in clinging to branches when ascend-
ing trees or if parachuting down from branches to other 
Table 1.1 Earth’s palaeogeological timeline (authorities vary 
regarding exact dates)
Geological 
era
Period Epoch Commenced – 
million of 
years ago
Cenozoic Quaternary Holocene 0.01
Pleistocene 1.6
Tertiary Pliocene 5
Miocene 23
Oligocene 36
Eocene 53
Palaeocene 65
Mesozoic Cretaceous 145
Jurassic 205
Triassic 250
Palaeozoic Permian 290
Carboniferous 360
Devonian 405
Silurian 436
Ordovician 510
Cambrian 560
Proterozoic
Siberia China 
P
angaea
Fig 1.2 Late Carboniferous circa 290 million years ago. The joining of land masses to form the single continent of Pangaea may have favoured the 
emergence of reptiles from amphibians around this time. Reptiles, including their descendants the birds, utilize insoluble uric acid as their key waste 
product in the protein breakdown and lay amniote eggs containing specialized membranes to keep toxic waste products away from the sensitive 
developing embryo. These developments, which are fundamental to both reptile and bird physiology, allowed reptiles to hatch eggs away from water 
and to take advantage of new land-based ecological niches.
HANDBOOK OF AVIAN MEDICINE
4
branches or to the ground (Fig. 1.15). Dromaeosaurs 
are currently known only from Cretaceous fossils but 
are considered to be of greater antiquity. They had 
skeletons with these additional basic features:
 l skull – numerous teeth, a rigid upper jaw, diaspid 
openings on their skull
 l vertebral column – tall neural spines on their 
cervical vertebrae, a flexible thorax and a 
long tail
 l pelvis – separate ilium, ischium and pubis and a 
broad, footed pubis
 l pectoral girdle – broad scapula, fused 
scapulocoracoid, short coracoid, flat sternum
 l forelimb – separate carpal and metacarpal 
bones with 3 digits and a phalangeal formula 
of 2-3-4
 l hindlimb – separate tibia, tarsal and metatarsal 
bones.
Compared with other theropod dinosaurs, dromaeo-
saurs were small and the pubic foot of the pelvis was 
caudally, rather than cranially, directed. Compared 
with their larger, more land-bound relations, these fea-
tures may have been adaptations that helped them to 
climb and manoeuvre up trees and shrubs which would 
have better enabled them to escape predators and take 
advantage of a rich, emerging aerial food source, the 
G
o n d w
a n a
L a u r a s i a
Fig 1.3 Late Jurassic circa 150 million years ago. Most molecular and fossil evidence points to the emergence of feathered birds in the Jurassic period, 
probably less than 185 mya. Primitive fossil finds have come from marine and freshwater wetlands in Europe (Archaeopteryx) and Asia (Confuciusornis). 
The single exception is a controversial fossil, Protoavis from Texas, a bird with remarkably advanced features but putatively dated to over 220 million 
years ago, in the Triassic. See text.
Tethys Sea
Fig 1.4 Late Cretaceous circa 65 million years ago. Birds were present globally before the K-T boundary extinction event of around 65 mya. 
Enantiornithines, Hesperornithiformes and Ichthyornithiformes were wiped out, along with all other dinosaurs, except for the Neornithes, the group 
to which all modern bird families belong. Fossil and molecular evidence suggests that the southern hemisphere was probably the place of origin of 
the Neornithes and that, for most bird orders, global repopulation and expansion in the Tertiary originated from this region. Land connections from 
Antarctica to South America, to Australia and, via island chains, to Africa were critical in this repopulation.
5
CHAPTER 1: THE DEVELOPMENT OF AVIAN SPECIES
Fig 1.5 Oligocene circa 30 million years ago. La Grande Coupure, the great cut of around 35–33 mya saw South America and then Australia unzipped 
from Antarctica and circumpolar currents beginning to flow. This was associated with global cooling and increased winds. While almost all orders of 
modern birds had emerged before this time, these climatic conditions would have favoured endothermic metabolism and flight and facilitated global 
expansion of modern birds.
flying insects. The flat-toed, digitigrade structure of 
both dromaeosaurs and early fossil birds suggests they 
leaped, waded, walked or ran on two legs rather than 
perched on small branches as practised by their more 
curved-toed avian descendants. In common with other 
theropods, most birds have the phalangeal formula of 
2-3-4-5 with absence of the fifth digit.
Stage 2 – add feathers for insulation and 
gliding (Troodontids/Aves/Archaeopteryx)
In general, ectotherms are at an advantage in hot cli-
mates where food sources are scarce. Endotherms 
perform better when the climate is cooler and food is 
abundant. Winged insects pre-date the emergence of 
birds. Such insects, along with aquatic creatures, could 
have provided an abundant food source for birds in the 
warm wetlands of the Triassic and Jurassic periods (Fig. 
1.3). In the swampy areas where early bird fossils have 
been found, they perhaps leaped or hang-glided, using 
long necks and faces, with their mouths still contain-
ing reptilian teeth, to catch flying prey. Their forelimbs 
remained free to balance and perform other functions. 
Aerial agility and acute vision would both have been 
advantageous to feathered proto-avian species such as 
the troodontids (Long & Schouten 2008) (Fig. 1.16).
Feathers do not appear to be modified scales but 
rather emerged among the theropod dinosaurs as inde-
pendent tubular structures that became progressively 
more complex. Feathers, hair, nails and scales all grow by 
proliferation and differentiation of keratinocytes which 
die and leave behind deposited masses of keratin, fila-
ments of protein that polmerize to form solid structures. 
Feathers are made of beta-keratins, which are unique to 
reptiles and birds. Skin and the outer sheath of growing 
feathers are made of alpha-keratins, which are found in 
all vertebrates (Figs 1.17, 1.18).
Insulation, balance and perhaps buoyancy, rather 
than flight, may have been key initial benefits that feath-
ers provided. This is demonstrated in the wide diversity 
of species of feathered theropod dinosaurs that have 
recently emerged from the fossil record in China (Prum & 
Brush 2004) (Fig. 1.19).
Archaeopteryx, a bird that lived on the islands that 
comprised Europe around 150 mya, is one of the earliest 
HANDBOOK OF AVIAN MEDICINE
6
Giardia is a flagellate parasite associated with ‘cow plop’ 
diarrhoeal syndromes in birds and mammals. The two 
 ‘eye-like’ nuclei that can be seen when examiningthe protozoan 
microscopically are haploid, each containing a single complement 
of chromosomes (Fig. 1.7). This contrasts with the double 
complement of chromosomes typically seen in a single nucleus 
when meiosis, sexual reproduction, has been fully completed.
Meiosis, sexual reproduction, was an important evolutionary step 
that emerged over 600 million years ago (mya) and facilitated 
Box 1.1 Biomechanics of flight
For birds or planes there are four forces involved in flight: 
lift, weight, thrust and drag. An aerofoil, such as a wing, has 
a cambered or convex upper surface with a concave, less 
cambered or flat lower surface. It is thicker at the front or leading 
edge and narrows towards the rear or trailing edge. As the 
aerofoil moves through air, relative airflow is created across the 
top and bottom surfaces. Because the top surface is convex the 
air travelling over the top surface must travel a greater distance 
relative to that of air travelling under the wing. The pressure on 
the top surface of the aerofoil is therefore reduced, producing 
the upward force lift to oppose the downward force of weight 
produced by gravity acting on the airframe or bird’s body.
Thrust is the force that moves the airframe forward. In 
planes it is produced by the propeller; in birds it is produced 
by the downstroke of the wing, with the outer primary feathers 
being twisted and tilted downward and outward in relation 
to the direction of the airflow and ‘swimming’ through the air. 
Thrust is opposed by drag, the force produced by resistance 
of the airframe, or bird’s body, to the airflow. In volant 
(flying) birds an evolutionary trend has been toward 
design features that facilitate flight by improving lift and 
thrust while reducing weight and drag (Fig. 1.6 – aerofoil 
wing).
Relative airflow 
Dynamic 
pressure 
Chord line 
Static pressure 
Downwash 
Bemoulli’s Theorem: 
Dynamic pressure + static pressure = total pressure 
As dynamic pressure increases, static pressure decreases
Fig 1.6 Aerofoil cross-section (see Box 1.1).
Box 1.2 Emergence of sexual reproduction
avian fossils identified; its features were transitional 
between the Maniraptora and birds and it is thought to 
be a relic species. Critically, it had typical flight feath-
ers, each with a long, tapering central shaft (rachis) and 
broad, flexible, asymmetric vanes. The vane on the leading 
edge of the feather was thicker but narrower than the 
vane on the trailing edge, giving a typical aerofoil shape. 
The tail was long and bony but feathered bilaterally. 
7
CHAPTER 1: THE DEVELOPMENT OF AVIAN SPECIES
In pectoral girdle structure, relative to the non-flying 
dromaeosaurs, Archaeopteryx’s scapula was strap-like 
and formed a flexible joint set at an acute angle with a 
larger, caudally reflexed coracoid. The glenoid cavity was 
located laterally and the biceps tubercle was large and 
cranial. There was no sternum, rather a series of gastralia 
behind the coracoids, but there was a rudimentary fur-
cula (‘wish bone’) (Fig. 1.20).
Dromaeosaurs, troodontids and Archaeopteryx all 
had swivel wrist joints and two long and one shorter 
finger on their hands. All had teeth and long bones with 
thin cortices (see Fig. 1.27). In Archaeopteryx the brain 
mixing of genetic material between organisms and vastly 
increased variation from one generation to the next. In birds, 
females are heterogametic (XY or ‘ZW’), while males 
are homogametic (XX or ‘ZZ’). Avian sperm, such as the 
budgerigar sperm illustrated in Figure 1.8, often have elongated 
heads and may be seen in droppings. They should not be 
mistaken for flagellates.
Fig 1.7 Giardia (see Box 1.2). Fig 1.8 Budgerigar sperm (see Box 1.2).
Box 1.3 Which came first, the chicken or the egg?
The first amniote eggs were laid some 300 million years before 
the first chickens hatched out. The novel use in the amniote 
egg of a partially pervious, calcium-impregnated shell along 
with insoluble uric acid as the key metabolic pathway to isolate 
nitrogenous waste has had far-reaching effects on the anatomy, 
physiology and disease processes in birds and reptiles compared 
with other vertebrates. Although modern bird eggs have harder 
shells, the internal structure of the egg has remained much the 
same as that of early eggs studied from the fossil record.
Figs 1.9 and 1.10 Jugal bar fixation in a sulphur-crested cockatoo. Streptostyly is a sliding action of the quadrate bone pushing the jugal bar cranially which 
in turn pushes the upper jaw so that it pivots around a craniofacial hinge joint and opens the upper jaw independently of the lower. In this bird the jugal bar 
dislocated, preventing the bird from closing its upper jaw. The problem was resolved by extending and manipulating the beak around a soft rod.
HANDBOOK OF AVIAN MEDICINE
8
Tarsal joint structure is an important distinguishing feature 
between the Crurotarsi group from which crocodiles descend 
and the Ornithodira from which pterosaurs, theropod dinosaurs 
and birds descend (Fig. 1.11). The former have a rotary crurotarsal 
joint between the astragalus (tibiotarsal) and calcaneum (fibular 
tarsal) bones with a heel on the calcaneum and a plantigrade 
stance. In the Ornithodira, the astragalus and calcaneum are 
fused and form the proximal end of a mesotarsal hinge joint 
opposing the distal tarsal bones. Stance is digitigrade (standing 
on the toes, without a heel) (Fig. 1.12).
was enlarged and the ascending process of the jugal bar 
reduced so that there was partial confluence of diapsid 
openings on the lateral skull allowing for large eyes sur-
rounded by a ring of scleral ossicles and partial stereo-
scopic vision. Probably to help cushion landings, the 
femur was 80% of the size of the tibia, and the tibia, 
fibula and proximal tarsal bones were partially fused, 
as were the distal tarsal and metatarsal bones. The 
hallux (first digit) was reversed. Pectoral girdle struc-
ture did not allow for a triosseal canal through which 
the supracoracoideus muscle could pass to elevate the 
wing. Consequently Archaeopteryx could run and glide 
freely but manoeuvrability would have been poor, 
powered flight rudimentary and taking off from the 
ground would have been difficult.
Confuciusornis, a pigeon-sized bird fossil found in rock 
formations in north-east China dating to the Jurassic–
Cretaceous boundary (c. 145 mya), showed contour feath-
ers, suggesting that the bird was endothermic. In common 
with Archaeopteryx, Confuciusornis had a retroverted 
pubis and a reversed hallux. It also had a large premax-
illa with a nasofrontal hinge and an edentulous (toothless) 
Fig 1.12 Pododermatitis. Because birds stand on their toes and do not have a ‘heel’, they can be prone to pressure sores, calluses and secondary 
infections on their feet and legs. These most commonly occur on the interdigital pad or (if the bird ‘squats’) the plantar surface of the intertarsal joint 
(see Box 1.4). Walking or perching on rough or hard substrates, obesity, restricted exercise and diets low in vitamin A are predisposing factors that 
should be avoided.
Astragalus
Tibia Tibia
Heel
Calcaneum
Calcaneum
Calcaneum
Digits
i
ii iv
iii
v
Crurotarsal (rotary) joint (Crocodyliformes) Mesotarsal (hinge) joint (theropod dinosaurs and Aves)
Distal tarsal
Fibula
Femur
Tibia Tibiotarsus
Astragalus
Digits
i
ii iv
iii
v
Calcaneum
Distal tarsal Tarsometatarsus
Fibula
Femur
Plantigrade stance
Digitigrade stance
A B
Fig 1.11 Comparative tarsal joint structure (see Box 1.4).
Box 1.4 Tarsal joint structure in the Crurotarsi and Ornithodira
9
CHAPTER 1: THE DEVELOPMENT OF AVIAN SPECIES
beak. Its hands showed unfused carpal elements, long 
fingers and long curved claws, suggesting it was a good 
climber. Its tail was short with long tail feathers allowing 
increased manoeurability in flight.
Stage 3 – add stereoscopic vision, brain 
development and asupracoracoideus pulley for 
rudimentary powered flight (Ornithothoraces/
Protoavis)
While fossilized bird remains are sparse, possible tracks 
dating to the late Triassic and early Jurassic have been 
found in Africa, Europe and North America, suggesting 
that birds may have been global species before 
Archaeopteryx. Protoavis, a species that lived in North 
America, controversially dated c. 225 mya, was ahead 
of its time when compared with Archaeopteryx and 
other Mesozoic bird fossils, so much so that some scien-
tists doubt its validity. It had a spring-like furcula joined 
ventrally by a hypocleidium, dorsally directed glenoids, 
strut-like coracoids and a sternum. Rudimentary trios-
seal canals formed at each shoulder at the confluence of 
the furcula, coracoid and scapula, through which could 
pass the pulley-like supracoracoideus muscles which 
were used to elevate the wings. These features all sug-
gest that this bird was capable of limited powered flight 
(Fig. 1.21). Fossil feathers for Protoavis have not been 
found but knobs identified on the ulna suggest they 
existed in life. There were three carpal and four sepa-
rate metacarpal bones.
Protoavis had large eyes, stereoscopic vision, a par-
tially toothed beak and an avidiaspid cranium that 
allowed a nasofacial hinge joint to open by the action 
of the quadrate bone pushing the jugal bar, much as it 
does in modern birds. Olfactory lobes were reduced but 
the cerebrum, optic lobes and cerebellum were increased 
and a visual Wulst bulge (thought to be involved with 
prehensile abilities and eye–foot coordination) could 
be identified on the dorsal cerebrum. Also like modern 
birds, the number of cervical vertebrae was increased, 
bones were pneumatic and the bodies were saddle-
shaped (heterocoelous), enabling the head to be moved 
in all directions and the beak to be used as a univer-
sal tool. At rest the neck was S-shaped so that the head 
could be retracted back close to the centre of gravity 
(Figs 1.22 and 1.23). The tail was long, enabling 
control of pitch and roll on a level course of flight but 
making turning, climbing or diving difficult.
Fig 1.13 An extended family gathering: a great egret (Ardea alba), plumed whistling ducks (Dendrocygna eytoni) and a crocodile, on the banks of the 
Yellow River, Kakadu, Northern Territory, Australia. Archosaurs gave rise to crocodilians, pterosaurs and dinosaurs. Birds descend from dinosaurs. As 
pterosaurs and non-avian dinosaurs became extinct around 65 million years ago, crocodiles are now birds’ closest living relative.
Table 1.2 Dating estimates for early avian divergences based 
on molecular data calibrated with penguin/stork fossils at 62 mya 
(after Harrison et al 2004)
Groups mya
Palaeognaths/neognaths 101
Ratite/tinamou 84
Ostrich/other ratites 75
Gallianseres/Neoaves 90
Magpie goose/duck 1 goose 66
Owl/other neoavians 80
Passerines/other neoavians 80
Oscines/suboscines 70
Falconiformes/parrot 72
Shorebirds/penguin, stork 74
Penguin/stork 62 (fixed)
Birds/crocodilian 183
Archosaurs/turtles 199
HANDBOOK OF AVIAN MEDICINE
10
Protoavis showed fusion of the ilium and ischium 
caudally, features that would have strengthened the pel-
vis and helped to withstand the impact of landing from 
a height. There were renal fossas indicating that the kid-
neys were streamlined into the pelvis. The ischium and 
pubis were open ventrally without a symphysis, which 
would allow the passage of large, hard-shelled eggs. On 
the tibia there was a cranial cnemial crest as in modern 
birds, but the tibia was not fused with fibula and proxi-
mal tarsal bones to form what we call the tibiotarsus. 
The distal tarsal bones were not fused with the metatarsal 
bones. The foot was ansiodactyl with a large, opposable, 
Allosaurs 
Ornithomimosaurs 
Dromaeosaurs 
Archaeopteryx 
Other birds 
Ceratosaurs 
Theropoda 
Tetanurae 
Coelurosauria 
Maniraptora 
Aves 
1 
2 
3 
4 
5
Fig 1.14 Cladistic relationships of the major groups of theropod dinosaurs (after Gauthier 1986).
11
CHAPTER 1: THE DEVELOPMENT OF AVIAN SPECIES
fully reversed hallux indicating Protoavis had a grasping 
foot with a capacity for both walking and climbing.
Stage 4 – add a locked coracoid-scapula, a 
carpometacarpus, an alula and a pygostyle for 
manoeuvrability (Pygostylia/Enantiornithines)
This group of birds first appeared in the fossil record in 
Cretaceous times around 120 mya (Fig. 1.4). The proximal 
coracoid formed a peg to fit into the socket of the scap-
ula, locking in a solid airframe configuration against 
which wings could flap. The tail was reduced to a short 
pygostyle from which tail feathers emerged. The carpal 
and metacarpal bones fused to form major and minor 
carpometacarpi and the alula (Fig. 1.24). Pelvic forma-
tion utilized the ilium and ischium fused posteriorly to 
enclose a large ilioischiadic fenestra. This constellation 
of features improved manoeuvrability and capacity for 
powered flight and controlled landings.
By the time Enantiornithines became widespread, 
Pangaea had fractured and the continents were moving 
apart. However, these birds were not confined to single 
land masses as they would have been able to use their 
ability to fly, wade and/or swim across water to reach 
other land masses. Some genuses included: Enantiornis 
leali, the type species from Argentina, Avisaurus from 
North America, Iberomesornis from Europe, Nanantius 
from Australia and Gobipteryx from Mongolia. Nests 
of Gobipteryx have been found, showing that some of 
these birds hatched precocial chicks from eggs incu-
bated in the ground.
Flightless land birds allied with the Enantiornithines, 
such as Patgopteryx from Patagonia, also emerged in 
the fossil record from the late Cretaceous period. The 
wings were highly atrophied; the ilia formed a pelvic 
shield with the synsacrum while posteriorly the ilia and 
ischium separated without enclosing an ilioischiadic 
fenestra. A large antitrochanter was present on the rim 
of the acetabulum, the femur was robust and the distal 
tarsal and metatarsal bones fused to form the tarsometa- 
tarsus. These features resemble present-day ratites.
Stage 5 – add ossified uncinate processes to the 
ribs to strengthen the ‘fuselage’ and more pelvic 
fusion (Ornithurae/Hesperornithiformes)
The Hesperornithiformes were flightless, foot-propelled 
diving birds whose stronghold was an inland sea that 
bisected North America in late Cretaceous times. The 
Hesperornithiformes and several other species of toothed 
birds were first described in 1880 by O.C. Marsh in an 
excellently illustrated text that attracted Charles Darwin’s 
praise (Fig. 1.25). Hesperornis, the best-known genus, 
parallels modern loons and grebes in many skeletal fea-
tures and the possession of salt glands. It was a much 
larger bird than its modern counterparts, about 2 metres 
long, covered with soft, hair-like plumaceous feathers. 
Like many subsequent species that evolved in geographi-
cally isolated areas in the absence of predators, it did not 
fly. The uncinate processes on the ribs were ossified. The 
Fig 1.15 A goanna (Varanus varius) climbing vertically up a tree trunk. 
Pro-avian dinosaurs had long tails and long fingers on their hands. 
As demonstrated by this goanna in a picnic ground in South Eastern 
Australia, these anatomical features could have enabled them to climb 
up tree trunks with ease. A patagial fold between the wrist and the 
shoulder in pro-avians may have served as an elastic band to keep the 
animal close to the trunk when climbing upwards as well as slowing 
speed and softening their landing if parachuting down from a height.
Fig 1.16 A darter (Anhinga melanogaster) with wings outstretched, 
Kakadu, Northern Territory, Australia. Early birds could have also used 
this behaviour for camouflage, protecting their nests or drying feathers 
before advances in barbule configuration in the feathers improved 
waterproofing. Warm wetland areas, suchas this, are the habitat in which 
early birds are believed to have evolved.
HANDBOOK OF AVIAN MEDICINE
12
synsacrum was enlarged with the incorporation of more 
than eight vertebrae and the pelvic elements were fused, 
with the ilium, ischium and pubis more or less parallel. 
These features would help ‘strengthen the fuselage’ for 
travel through either air or water. As in present-day pad-
dling waterfowl, the cnemial crest on the tibia was large 
(in this case derived from the patella), the femur was 
short and held horizontal and the paddling leg movement 
was predominantly a function of the stifle joint.
Stage 6 – add a deeper keel bone, a complete 
triosseal canal and fused tibiotarsus and 
tarsometatarsus for controlled, powered flight 
and safer landing (Carinatae/Ichthyornithiformes)
Ichthyornis and Apatornis were toothed birds of the 
late Cretaceous period in North America that were also 
first described by O.C. Marsh in 1880. They resembled 
present-day gulls and terns and had expanded brains 
and salt glands. The sternum had a large carina and 
there was a triosseal canal, the humerus had an enor-
mous deltoid crest and a brachial depression at the 
distal end. Both the tibiotarsus and the tarsometatarus 
were fused (Fig. 1.26).
Stage 7 – add skull bone fusion (Neornithes/
Gobipipus and modern birds)
By the close of the Mesozoic era Enantiornithines were 
found on all continents, Hesperornithiformes were swim-
ming in northern hemisphere seas and Ichthyornithiformes 
were found along the shore lines. While the location 
of their ancestral population is unclear, modern birds 
(Neornithes) in which the individual bones in the skull 
were fused were beginning to appear globally in the fos-
sil record. In North America transitional shorebirds 
were emerging in coastal areas, and in Eurasia there was 
Gobipipus, a land bird known from late Cretaceous 
Mongolia. Its fossilized nests included an egg containing 
a precocious chick on the point of hatching. In the south-
ern hemisphere, swimming off an island near western 
Antarctica in a shallow marine environment alongside 
plesiosaurs was Polarornis, the oldest loon (Gaviiformes). 
As in hair, nails and scales, feathers grow by proliferation and differentiation
of keratinocytes. These keratin-producing cells in the epidermis, or outer
skin layer, achieve their purpose in life when they die, leaving behind a
mass of deposited keratin. Keratins are filaments of proteins that
polymerize to form solid structures. Feathers are made of beta-keratins,
which are unique to reptiles and birds. The outer covering of the growing
feather, called the sheath, is made of the softer alpha-keratin, which is
found in all vertebrates and makes up our own skin and hair.
Condensation
of cells Placode
EpidermisDermis
Feather growth begins with the
placode, a thickening of the
epidermis over a condensation
of cells in the dermis.
The placode then forms a unique
elongated tube, the feather germ.
Proliferation of cells in a ring around the
feather germ creates the follicle (detail below),
the organ that generates the feather. At the
base of the follicle, in the follicle collar,
the continuing production of keratinocytes
forces older cells up and out, eventually
forming the entire, tubular feather. 
Feather germ
Epidermis
of follicle
Dermis
of follicle
Follicle
Follicle collar Follicle cavity
Dermal
pulp
Fig 1.17 Feather formation (after Prum & Brush 2004, with permission from Patricia J. Wynne).
13
CHAPTER 1: THE DEVELOPMENT OF AVIAN SPECIES
Alongside fossil evidence, evidence from nuclear and 
mitochondrial DNA hybridization is now placing the ori-
gin of modern birds in the late Cretaceous period, with 
more than 13 extant modern orders emerging prior to the 
K-T boundary disaster.
Tertiary birds
The Cretaceous–Tertiary (K-T) boundary, 65 mya, was 
marked by a global extinction event, thought to have 
been triggered by a meteorite whose main crash site 
was in present-day Gulf of Mexico. As with other ani-
mals, it is likely that birds living near the impact would 
have had little chance of surviving the initial explosion, 
fires and the ensuing long dark winter. Birds living at 
higher latitudes might have been better adapted to the 
cool, dark conditions and could provide bird popula-
tions from which other areas could be repopulated. 
The ability to fly, swim, wade or walk would have 
The outermost epidermal layer becomes 
the feather sheath, a temporary structure 
that protects the growing feather. 
Meanwhile the internal epidermal layer 
becomes partitioned into a series of 
compartments called barb ridges, 
which subsequently grow to 
become the barbs of the feather. 
In a pennaceous feather the barb 
ridges grow helically around the 
collar until they fuse to form the 
rachis ridge. Subsequent barb 
ridges fuse to the rachis ridge. 
In a plumulaceous feather (not 
shown), barb ridges do not grow 
helically, and a simple rachis 
forms at the base of the feather. 
As growth proceeds, the feather 
emerges from its superficial sheath. 
The feather then unfurls to obtain 
its planar shape. When the feather 
reaches its final size, the follicle 
collar forms the calamus, a simple 
tube at the base of the feather. 
Helical growth 
Rachis ridge 
Barb
ridge
Rachis
ridge
Calamus 
Newly forming 
barb ridge 
Follicle collar 
Artery 
Sheath 
Rachis 
ridge 
Barb 
ridge 
Fig 1.18 Feather formation (after Prum & Brush 2004, with permission from Patricia J. Wynne).
Fig 1.19 Mononykus. There have been a number of finds in recent 
years of feathered, bird-like theropod dinosaurs. Mononykus, a 
feathered, non-flighted theropod dinosaur from the late Cretaceous 
period in China, had avian skull characteristics. Model from the 
‘Dinosaurs of China’ exhibition, Melbourne Museum, 2005.
HANDBOOK OF AVIAN MEDICINE
14
Fig 1.20 Archaeopteryx. Even when it lived in Europe 150 mya, Archaeopteryx was a relic species. This early bird was not strongly built, it had teeth, 
separate bony fingers on its hands, no sternum, a long tail and multiple metatarsal bones. However, it also had typical flight feathers, a strap-like scapula 
set at an acute angle with a large reflexed coracoid and a rudimentary furcula. It was capable of gliding but taking off from the ground would have been 
difficult. (Engraving by Zittel 1887.)
15
CHAPTER 1: THE DEVELOPMENT OF AVIAN SPECIES
Fig 1.21 Pectoral girdle structure in volant birds. Because extended 
wings have an aerofoil configuration (see Box 1.1), birds can rely on the 
force of lift to maintain altitude while in flight and they do not need strong 
muscles to raise their wings on the upstroke. However, they do need 
strong muscles for the downstroke and to generate thrust. The tendon of 
the supracoracoideus (deep pectoral) muscle acts like a pulley, travelling 
from muscle attached to the sternum, through the triosseal canal (see 
arrow) to insert on the head of the humerus and raise and extend the 
wing. The overlying superficial pectoral muscle provides power for the 
downstroke and forward thrust. The strap-like scapula and strut-like 
coracoid are firmly attached and form part of the triosseal canal. In 
conjunction with the supracoracoideus, they help to maintain the aerofoil 
configuration of the wing. The spring-like furcula, the third bone of the 
triosseal canal, makes the downstroke easier and also provides support 
for the shoulder.
Fig 1.22 Cervical subluxation in a sulphur-crested cockatoo. To 
compensate for not having hands, birds have long necks with many 
heterocoeleus (saddle-shaped) vertebrae which enable the head and 
beak to be moved in all directions and used as a universal tool. This 
leaves them vulnerable to neck injury, for example as occurred here 
when this bird caught his head in cage wire then tried to pull it out. 
Fig 1.23 The cervical subluxation of the sulphur-crested cockatoo 
was reduced by manipulation and the neck placed in a brace attachedto a body harness (as shown) for several weeks. He made a full 
recovery.
Fig 1.24 Alula. When extended, the alula (‘thumb’) (see arrow) acts as a 
‘slot’, maintaining laminar air flow over the dorsal surface of the wing as 
the bird slows and hence enables a smoother, more accurate landing at 
slow speeds.
aided dispersal. Enantiornithines, Hesperornithiformes 
and Ichthyornithiformes did not survive the extinction 
event, nor did the pterosaurs, but Neornithes birds sur-
vived and went on to fill ecological niches on land, sea 
and air across the globe (Figs 1.28, 1.29).
Perhaps there were soft tissue differences, for instance 
in brain development, navigational ability or instinctive 
behaviour, nesting or migration patterns, that gave the 
Neornithes an edge over the archaic birds. Both DNA 
and fossil evidence indicate that all modern birds fall 
into this monophyletic clade but the bony differences 
between the Ichthyornithiformes and the Neornithes 
do not seem to be dramatic enough to account for the 
HANDBOOK OF AVIAN MEDICINE
16
Neornithes’ global dominance. Neornithes subsequently 
split into Palaeognathae (the ratites and tinamous) and 
Neognathae (all other modern birds). Palaeognathae 
palate structure shows features similar to primitive 
archosaurs while in the Neognathae there is a develop-
ment of a flexible joint between the pterygoid and pala-
tine. There are also differences in sternal structure, with 
the neognaths generally showing deeper carinae enabling 
stronger flight.
Relationships amongst the living orders of neognaths 
have been problematic to unravel and are still much 
debated. Present-day southern hemisphere continents 
now have the largest diversity of endemic bird families 
(South America: 31, Australia: 15 and Africa: 6) (see 
Fig. 1.32). Early modern bird fossils from at least five 
groups, including the stone curlew, penguin, transitional 
wader and magpie goose/duck, have now been 
found dating to around 66 mya from Vega Island, off 
Antarctica. Molecular and palaeogeological evidence 
dates New Zealand’s endemic parrot and passerine 
lineages to before the islands’ split from Gondwana, 
over 80 mya. These findings lend support for a south-
ern hemisphere origin for modern birds perhaps around 
100 mya. Table 1.2 gives estimates for early avian diver-
gences based on molecular data for these groups cali-
brated against penguin fossils from North Canterbury, 
New Zealand dating to 62 mya and supported by the 
more recent bird fossil finds from Vega Island mentioned 
above.
Land connections between South America, Antarctica 
and Australia continued from the K-T boundary until 
c. 35–33 mya, while intermittent, much more tenuous, 
Fig 1.25 Hesperornis. The Hersperornithiformes were specialized, toothed, flightless, foot-propelled diving birds that lived in northern hemisphere 
waters in Cretaceous times. Like modern diving birds their bodies were streamlined and strengthened by ossified uncinate processes on the ribs 
and fusion of vertebrae to form the synsacrum. They had large cnemial crests derived from the patella and paddling leg motion was predominately a 
function of the stifle joint. The group did not survive the K-T boundary extinction event 65 mya. (From Marsh 1872.)
17
CHAPTER 1: THE DEVELOPMENT OF AVIAN SPECIES
island chain connections existed between Antarctica and 
the east coast of Africa via the Keuguelen plateau over 
the same period. While still speculative, these connec-
tions could have provided a corridor for modern birds 
to populate Africa and Eurasia from the south after the 
65 mya K-T disaster. Alternatively, some orders, such as 
Strigiformes (owls), may have re-emerged from remnant 
high latitude northern populations.
Fig 1.26 Ichthyornis. The Ichthyorniformes were toothed, gull-like shorebirds of late Cretaceous times in North America. They had many features 
in common with modern volant birds including a large sternum, a pectoral girdle structure with a triosseal canal, fused major metacarpus and fused 
tibiotarsus and tarsometatarsus. The group did not survive the K-T boundary extinction event 65 mya. (From Marsh 1872.)
Fig 1.27 Left: mammalian long bone. Right: avian long bone. Unlike non-avian reptile bones, bird bones have evolved for lightness and strength: they 
are pneumatic with thin cortices and wide medullas that are crossed by strategically placed trabeculae for reinforcement. This produces challenges for 
avian orthopaedic surgeons as such bones splinter easily and do not lend themselves to fixation with plates and screws. On the other hand, bird wings 
fold snugly against the body. Braille or figure-of-eight bandages and tie-in techniques for fracture repair are some of the procedures that have been 
developed because of these unique features of avian patients.
HANDBOOK OF AVIAN MEDICINE
18
In the warm, subtropical, Palaeocene times (65–
53 mya), the era that followed the demise of non-avian 
dinosaurs, an ‘evolutionary relay’ seemed to develop as 
birds and mammals competed for dominance. There 
are fossil records from France of Gastronis, an early 
ratite. Strigiformes emerged in North America and 
bony-toothed Pelicaniformes were found globally. Most 
spectacularly, giant flightless birds of the Gruiformes 
(crane, rail and bustard) family rose to become domi-
nant herbivores (e.g. Diatryma of North America 
and Europe) and predators (e.g. the phorusrhacids of 
South America). As time moved on, these large flight-
less birds were vulnerable to emerging apex predators 
amongst the placental mammals, who could move rap-
idly on land, raid nests for eggs and attack the adults 
with their sharp teeth and claws (Fig. 1.30). Flightless 
birds disappeared from the fossil record in Eurasia and 
North America as the placental mammals took over 
but, as evidenced by the present-day distribution of 
ratites, flightless birds were able to hold their own on 
land masses where placental mammal predators had not 
reached. Stratigraphic evidence suggests that recent-day 
palaeognaths:
 l the Tinamidae of South America
 l the kiwis and extinct moas of New Zealand
 l the extinct elephant birds of Madagascar
 l the emu and cassowaries of Australia
 l the ostrich of Africa and
 l the rhea of South America
derived from smaller ancestors that could, with difficulty, 
fly/swim or wade across the bodies of water that sepa-
rated the southern hemisphere land masses (Fig. 1.31). 
The distances involved were much shorter than exist 
today. Of these birds, only ostriches initially co-evolved 
with large placental mammal predators.
Sphenisciformes (penguins), probably derived from 
a loon-like ancestor, are known only from the southern 
hemisphere with Antarctica their stronghold. Fossils 
of giant penguin-like birds have been found in South 
Australia dating to the Eocene epoch (Vickers-Rich 
1996). While loons are known to have been present 
in Antarctic regions in the late Cretaceous and early 
Tertiary periods they are now only found in the north-
ern hemisphere. Perhaps proto loon species were out-
competed by the emerging penguins or pinnipeds (seals) 
or adversely affected by local climate change.
Of the present-day orders of Neognathae birds there 
is general consensus that the ‘Galloanserae’ were an 
Figs 1.28 and 1.29 Apart from birds, winged flight has evolved independently in two other vertebrate groups: pterosaurs and bats:
In pterosaurs the fifth digit became elongated and supported a membranous skin fold. Pterosaurs did not survive the KT boundary extinction event. In 
bats, flying mammals that emerged in the Tertiary Period, skin folds form between elongated digits. Photos taken at the British Museum and Melbourne 
Museum, 2005.
Fig 1.30 Florida 2 million years ago. Large flightless land birds related 
to Gruiformes (cranes and bustards) and Anseriformes (waterfowl) 
emerged as dominant herbivores and predators following the demise of 
the non-avian dinosaurs at the time of the K-T boundarydisaster around 
65 mya. They became extinct as sharp-toothed placental mammal 
predators emerged. South America was a later-day stronghold of the 
giant land birds as it was largely isolated from these placental mammals 
until the development of the Panama land bridge 2.5 mya. Titanis, 
illustrated here, moved from South to North America at this time but the 
species was subsequently wiped out in both places. Illustration by Carl 
Buell, Florida Museum of Natural History.
19
CHAPTER 1: THE DEVELOPMENT OF AVIAN SPECIES
early offshoot and derived from common ancestry. This 
group includes:
 l the Anseriformes: screamers of South America, 
ducks, geese and other waterfowl and
 l the Galliformes: chickens, quail and pheasants.
The remaining Neognathae, the Neoaves, fall into 
three main groups:
 1. The Gruiformes (cranes).
 2. The Chardriormorphae, a shorebird-derived 
complex that, in addition to present-day 
shorebirds, gave rise to the ‘Ciconiimorphae’:
 – Phoenicopteriformes (flamingoes)
 – Ciconiiformes (storks)
 – Pelicaniformes (cormorants, shags, pelicans)
 – Gaviformes (loons)
 – Sphenisciformes (penguins)
 and the ‘Columbimorphae’:
 – Turniciformes (button quail)
 – Pteroclidiformes (sand grouse)
 – Columbiformes (doves and pigeons)
 – Psittaciformes (parrots and cockatoos).
 3. ‘The land bird assemblage’, which gave rise to:
 – Opisthocimiformes (hoatzins)
 – Falconiformes
 – Cuculiformes (cuckoos)
 – Musphagiformes (touracos)
 – Strigiformes (owls)
 – Caprimulgiformes (goatsuckers, frogmouths)
 – Apodiformes (swifts and hummingbirds)
 – Bucerotiformes (hornbills)
 – Piciformes (woodpeckers)
 – Passeriformes, which now comprise over half 
of present-day bird species.
The Piciformes were amongst the last modern 
bird orders to emerge in the fossil record, with first 
recordings currently dating to the Oligocene epoch, 
53–36 mya.
La Grande Coupure c. 33 mya
Following the K-T crisis, another critical biogeogra- 
phical event for evolving avifauna was La Grande 
Coupure – the great cut, so coined by the Swiss pal-
aeontologist Hans Stehlin. Beginning about 60 mya, 
Australia began to unzip itself from Antarctica as tec-
tonic plate movement slowly drew the continent north-
wards. By 40 mya, India had crashed into southern Asia 
and the Himalayan mountains began rising, as they 
continue to do today. The Drake Passage between South 
America and Antarctica opened c. 35 mya and finally, 
c. 33 mya, a long submarine rise that stretched from 
Australia to Antarctica severed, allowing bottom water 
of the Antarctic circumpolar current to flood between 
the two continents for the first time. This caused glo-
bal cooling and strengthened coastal and trade winds. 
The effect was magnified as polar ice caps expanded, 
winds strengthened, temperatures dropped and global 
cold water currents carried rich marine food sources 
northwards (Flannery 2000). While present-day orders 
of birds emerged prior to La Grande Coupure, it was 
after this time that a dramatic expansion of volant bird 
families occurred.
North and South America were rejoined by the 
Panama land bridge c. 2.5 mya and with this there was 
interchange of bird and animal species from the two con-
tinents. Large flightless birds made their way briefly to 
North America from the south but, in the end they were 
wiped out (Fig. 1.30). Apex placental mammal predators, 
the large cats, bears and canids, were probably the cause 
of their extinction. These, however, were exceptions; glo-
bally birds thrived under diverse circumstances, including 
Ice Age conditions during the Pleistocene epoch.
Fig 1.31 Mainland and dwarf emus. Fossil evidence suggests that 
ratites were once found globally, probably descendant from small, 
flighted ancestors resembling present-day tinamous. In historical 
times their stronghold has been the southern hemisphere. There have 
been many examples of island extinctions of ratites coinciding with the 
arrival of humans, e.g. the moas of New Zealand, the elephant birds of 
Madagascar and, as illustrated here, the dwarf emus of the Bass Strait 
Islands of Australia. These emus were isolated when global sea levels 
rose 14 000 years ago and they developed into dwarf forms on several 
islands. They were easily caught and became extinct shortly after the 
arrival of Europeans. This specimen was brought to France as a live bird 
in 1804 and was stuffed when it died. There are no specimens of dwarf 
emus left in Australia. (Photo by Elliot Forsyth.)
HANDBOOK OF AVIAN MEDICINE
20
The end of the Ice Age brought the global expan-
sion of humans, who have had a devastating effect on 
bird diversity. Around the world, local extinction of 
bird species has followed the arrival of humans and our 
domestic dogs, cats, rats, livestock and machines. The 
scale of these extinctions has been enormous, especially 
for island populations. It is estimated that over 2000 
species of birds have disappeared from the islands of 
the Pacific since the arrival of the Polynesians and the 
Europeans. Large flightless birds have been particularly 
vulnerable. The moas of New Zealand, the elephant 
bird of Madagascar, and the dodo of Mauritius are 
just a few examples. Continental birds, like the passen-
ger pigeon, Carolina parakeet and great auk, have also 
suffered extinctions. From a peak of over 12 000 spe-
cies before the start of this human-induced crisis there 
are currently around 9650 living species. The number 
of avian species worldwide continues to diminish 
(Fig. 1.33).
Behavioural and soft tissue adaptations
Fossils can tell only part of the story of avian evolution. 
Behavioural, urogenital and other soft tissue adaptations 
were critical in the emergence of structure and function 
of modern birds. These features leave little trace in the 
Palaearctic
Shares 48 families with
the Nearctic.
69 families, 1 endemic
Oriental
66 families, 1 endemic
Ethiopian
67 families, 6 endemic
Australian
Approx 83 families, 15 endemic
Neotropical
86 families, 31 endemic
Nearctic
62 families, 1 endemic
Fig 1.32 Present-day global distribution of bird families. South America and Australia currently have the largest number of endemic bird families but 
fossil evidence suggests birds such as the megapodes and psittacines were formerly present elsewhere. Present-day distribution lends support to a 
Gondwana/southern hemisphere origin for modern birds.
Fig 1.33 Carolina parakeet (Conuropsis carolinensis), the only indigenous 
parrot species in eastern United States, became extinct in the early 
1900s from habitat loss, hunting by farmers who considered them a pest 
species and possibly from disease. Currently numerous other parrot 
species throughout the world are also threatened or endangered. Avian 
veterinarians have a role to play in reversing this trend. Stuffed specimen, 
Audubon Exhibition, Museum of Natural History, Nantes, France, 2005.
stratographic record, so estimation of the time of emer-
gence of these features can be difficult. However, they 
are reflected in anatomy, physiology, behaviour, diver-
sity and distribution of present-day bird species.
21
CHAPTER 1: THE DEVELOPMENT OF AVIAN SPECIES
Reproductive adaptations
Birds’ reptilian ancestors had two ovaries and laid large 
clutches of eggs (Fig. 1.34). These eggs were incubated 
in nests on the ground in warm, moist conditions and 
gave rise to precocial young. Crocodilians still nest in 
this manner. For early birds, using body heat to shorten 
the incubation time (and later developing specialized 
brood patches) would have been an advantage in reduc-
ing risk of predation and enhancing survival of their 
young, particularly in cool climates. It would have also 
favoured birds having small clutches to incubate against 
the parents’ bodies. Ducks or swans that nest in reeds 
or build floating nests might be a model for this type of 
incubation. Alternatively, feathered, partially endother-
mic avian ancestors may have nested in burrowsas, for 
example, some penguins (another ancient avian family) 
do today (Kavanau 1987).
The ability of early birds to use their own body heat 
to speed up the incubation process may have been 
advantageous in the short term in enabling birds to make 
use of nest sites in tree hollows, branches or bushes. The 
evolution of avian incubation also required a change in 
egg structure to enable the embryos to survive in con-
ditions with lower humidity (Fig. 1.35). Laying small 
clutches of eggs individually rather than as a simultaneous 
clutch, as in reptiles, eliminated a need for two ovaries 
and birds’ bodies could be aerodynamically streamlined 
to contain a single ovary and oviduct. The emergence 
of medullary bone lay-down of calcium in egg-laying 
females would have assisted this process. Flight and the 
avian reproductive ‘package’ developed hand in hand 
(Figs 1.36, 1.37, 1.38).
Eggshell structure
For both birds and reptiles an excretory system based 
on the production of insoluble urates (rather than 
soluble urea) enabled waste material to be compart-
mentalized within the egg but away from the develop-
ing embryo in a non-toxic form. The development of 
insoluble urates gave birds the capacity to lay eggs that 
could survive out of water. Both the non-avian thero-
pod dinosaurs and the Enantiornithines produced egg-
shells with an internal mammillary layer composed of 
numerous, tightly packed conical knobs. External to 
this was the thicker, squamate or spongy zone com-
posed of calcite crystals arranged on a protein matrix. 
Neoaves also have these layers, but in addition there is 
also an external zone composed of smooth, shiny, pro-
tein cuticle and the spongy zone has vertical palisades 
separated by minute pore canals. With these innova-
tions, modern bird eggs were less prone to desiccation 
and parent birds were better able to exploit nesting sites 
above the ground (Fig. 1.39).
Fig 1.34 Radiograph of turtle on the point of lay. Reptiles lay large 
clutches of soft eggs concurrently and the eggs are incubated in soil. 
Avian ancestors evolved to lay eggs one at a time as birds would not be 
able to fly and carry such a large number of eggs internally. (Photo by 
Anne Fowler.)
Fig 1.35 Cockatiels with an egg. Endothermy and feathers enhanced 
the capacity for birds to incubate eggs against their bodies compared 
with their dinosaur ancestors. Dinosaur nest-protecting behaviour could 
have gradually become modified into egg-incubating behaviour. Smaller 
clutch sizes would allow eggs to be incubated against the body and the 
incubation period, and hence the risk of nest predation, to be reduced. 
Brood patches, vascular areas that develop on the ventrum of egg-
incubating birds, also assist in maintaining warmth and shortening the 
incubation period.
HANDBOOK OF AVIAN MEDICINE
22
While primitive birds hatched large, downy feathered, 
precocial young (as evidenced by Gobipipus, ratites, 
Anseriformes and Galliformes), it is possible for altri-
cial (small, featherless, helpless) chicks to be produced 
from smaller eggs relative to the size of the adult bird.
For some species, benefits of this appear to offset the 
greater parental care required to rear altricial young 
(e.g. Columbiformes, Psittaciformes and Passeriformes).
Respiratory adaptations
Crocodilians have multi-chambered lungs with com-
plex, branching bronchi leading into high-density 
parenchyma. There is neither diaphragm nor alveoli. 
Birds also lack a diaphragm and have air capillaries 
rather than alveoli and there is extensive development 
of the air sacs which provide a reservoir of air for 
release into the air capillaries and into pneumatic bones. 
These features generally make for lighter bodyweight 
and efficient respiration, both of which are cornerstones 
for leaping, running, swimming or flight. Penguins 
and emus have paleopulmonic parabronchi in which 
airflow is caudocranial, unidirectional and linked with 
air sacs. Other birds also have neopulmonic parabron-
chial networks, in which airflow is bi-directional, in 
addition to paleopulmonic parabronchi. Birds’ abdomi-
nal muscles and intercostal muscles act as a diaphragm 
for the whole coelomic cavity with both inspiration and 
expiration. The cone-shaped skeletal torso of modern 
birds appears to function as a bellows-like apparatus in 
Fig 1.38 Radiograph, medullary bone lay-down and a collapsed egg. 
As a means to store calcium to satisfy their high metabolic calcium 
requirements during egg laying, birds have evolved a mechanism 
for oestrogen-dependent medullary bone lay-down (‘polyosteotic 
hyperosteosis’). Increased long bone density is seen in both normal, 
reproductively active females as well as those showing pathology, such 
as illustrated here. In males it may be an indication of an oestrogen-
producing Sertoli cell tumour of the testicle.
Figs 1.36 and 1.37 Egg binding in a lorikeet. Compared with their dinosaur ancestors, laying eggs one at a time and having smaller clutch sizes would 
have facilitated parent birds being able to fly to seek food while caring for their offspring. However, large, heavily calcified eggs that can be incubated 
above ground without desiccation can also be difficult to pass, as shown with this egg-bound lorikeet. Warmth, calcium and fluid therapy are medical 
treatments that can be helpful to relieve egg binding from a large egg. If not resolved, egg implosion or salpingotomy may be needed to treat the 
reproductive problem.
23
CHAPTER 1: THE DEVELOPMENT OF AVIAN SPECIES
breathing while at the same time streamlining and light-
ening birds’ bodies for swimming, gliding or flight.
Digestive adaptations
Avian digestive systems reflect diet diversity, weight con-
straints of powered flight and evolutionary origin. For 
example, while all present-day birds lack teeth, large 
caeca are present in the Galliformes and Anseriformes 
(closely related, generally herbivorous, families) but are 
reduced or absent in Columbiformes, Psittaciformes and 
Passeriformes. In the absence of teeth, a muscular ven-
triculus with grit is used as an alternative for grinding 
food.
‘The flight package’ of modern birds
In volant birds the centre of gravity needs to be below 
the extended wings rather than above them. With rota-
tion of the coracoid to the front of the chest and the 
scapula to the flat of the back, the glenoid socket of the 
scapulo-humeral joint moved to a dorsolateral position. 
This positioning of the scapula facilitates the attachment 
of the wing and it is also seen in mammalian climbers, 
including primates. However, in the avian model the 
scapula is strap-like, narrow and fixed, compared with 
the broad triangular scapula of climbing animals. Once 
in flight, birds do not require strong muscles to raise 
their wings as lift performs this function, but they require 
strong muscles for the down beat – a function performed 
by the superficial pectoral muscles. The tendon of the 
deep pectoral muscle (supracoracoid) passes through the 
triosseous canal and inserts on the humerus, thereby assist-
ing in lift by adjusting curvature of the dorsal aerofoil 
surface of the wing through an indirect effect on the 
patagial membranes and by altering the angle of attack 
of the wing.
In addition to the change in the centre of gravity, 
reduction and fixation of the scapula and emergence 
of the supracoracoid/triosseous canal pulley system, 
skeletal refinements useful for flapping flight in birds 
include:
 l swivel carpal joints for wing folding
 l the enlargement of the coracoid
 l development of flight feathers with asymmetrical, 
closed pennaceous vanes
 l enlargement of the ulna to which secondary wing 
feathers attach
 l fused clavicles forming the furcula
 l pneumatic bones
 l fusion and strengthening of bones of the limbs, 
spine and synsacrum
 l development of the alula
 l shortening of the tail to become the pygostyle
 l development of uncinate processes on the ribs
 l development