The development of avian species

CHAPTER 1: THE DEVELOPMENT OF AVIAN SPECIES

The development of avian species Patricia Macwhirter Fossil evidence since the 1800s has suggested that birds are descended from reptilian ancestors. More recent evidence places avian species as descendants of the theropod 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 feathers along with changes in thermoregulation, reproduction, nesting behaviour, respiration, renal function, vision and musculoskeletal structure. Bird bones are fragile and do not preserve well, so it is not surprising 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 cladogram 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 evolution (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 diversification 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, crocodileshaped amphibians called labyrinthodonts dominated

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 intermingled, enabling a vastly increased pool of natural variation and selection pressures that favoured organisms able to reproduce independently of an aquatic environment. 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 lateral openings on the side of the cranium posterior to the orbit. Tortoises and turtles have been traditionally classified 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 avidiapsid cranium in which the two lateral cranial openings merged into a single opening, allowing for cranial kinesis (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 progressed. These included the progenitors of turtles, lizards 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 question. Molecular evidence (Table 1.2), places the emergence 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 Possible evolutionary steps between ectothermic reptiles 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:

which features were included in the definition of ‘bird’. Phylogenetic analysis and analysis of fossils with possible pro-avian features suggest that birds are embedded in the bipedal dinosaur class Theropoda, probably descendant from the Maniraptora, a group that also gave rise to dromaeosaurs. A dromaeosaur with a birdlike furcula (clavicle) has been found in Montana but theropod dinosaurs occurred across Pangaea, and therefore a Eurasian or American origin for the earliest birds could both be consistent with existing fossil evidence (Chatterjee 1997, Martin 2002) (Fig. 1.14).



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 l

Archaeopteryx

Aves

1

Protoavis

Ornithothoraces

2

Enantiornithes

Pygostylia

3

Hesperornithiformes

Ornithurae

4

Ichthyornithiformes

Carinatae

5

Neornithes

Fig 1.1  Aves cladogram.



CHAPTER 1: THE DEVELOPMENT OF AVIAN SPECIES

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



the establishment of the Panama land bridge, c. 2.5 mya, 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.

l

For any species, evolution is not linear but rather a continuum of a much-branching tree. Genome, lifetime 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, physiology 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.

Table 1.1  Earth’s palaeogeological timeline (authorities vary regarding exact dates) Geological

Period

Epoch

era

Commenced – million of years ago

Cenozoic

Quaternary Tertiary

Holocene

1.6

Pliocene

5

Miocene

23

Oligocene

36

Eocene

53

Palaeocene Mesozoic

Palaeozoic

0.01

Pleistocene

Stage 1 – a bipedal stance, swivel wrist joint and long forelimbs (Maniraptora/Dromaeosaurs)

65

Cretaceous

145

Jurassic

205

Triassic

250

Permian

290

Carboniferous

360

Devonian

405

Silurian

436

Ordovician

510

Cambrian

560

l

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 forearms might assist in clinging to branches when ascending trees or if parachuting down from branches to other

Proterozoic

Siberia

China

ga

n Pa ea 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

Laurasia

Go

nd

wa

na

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.

Tet hys S

ea

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.

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:

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. l

Compared with other theropod dinosaurs, dromaeosaurs were small and the pubic foot of the pelvis was caudally, rather than cranially, directed. Compared with their larger, more land-bound relations, these features 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

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 climates 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 containing 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 independent 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, filaments 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 feathers 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 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 feathers, 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.

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).

As dynamic pressure increases, static pressure decreases

Static pressure

Dynamic pressure

Relative airflow

Downwash Chord line

Bemoulli’s Theorem: Dynamic pressure + static pressure = total pressure Fig 1.6  Aerofoil cross-section (see Box 1.1).

Box 1.2 Emergence of sexual reproduction 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 examining the 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

CHAPTER 1: THE DEVELOPMENT OF AVIAN SPECIES 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).

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.

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.

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 furcula (‘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 

handbook of avian medicine

Box 1.4 Tarsal joint structure in the Crurotarsi and Ornithodira 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 A Crurotarsal (rotary) joint (Crocodyliformes)

Tibia

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). B Mesotarsal (hinge) joint (theropod dinosaurs and Aves)

Tibia

Tibia

Tibiotarsus

Astragalus

Calcaneum

Plantigrade stance

Heel

Digitigrade stance Astragalus

Calcaneum

Femur

Femur

Digits

Digits

v

Fibula

i ii iv iii

i

v ii iv iii

Distal tarsal Calcaneum

Fibula Calcaneum Distal tarsal

Tarsometatarsus

Fig 1.11  Comparative tarsal joint structure (see B.4).

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.

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 surrounded 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 structure 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 feathers, suggesting that the bird was endothermic. In common with Archaeopteryx, Confuciusornis had a retroverted pubis and a reversed hallux. It also had a large premaxilla with a nasofrontal hinge and an edentulous (toothless)

CHAPTER 1: THE DEVELOPMENT OF AVIAN SPECIES

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

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 a supracoracoideus 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 scientists doubt its validity. It had a spring-like furcula joined ventrally by a hypocleidium, dorsally directed glenoids, strut-like coracoids and a sternum. Rudimentary triosseal 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 suggest 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 separate metacarpal bones. Protoavis had large eyes, stereoscopic vision, a partially 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 saddleshaped (heterocoelous), enabling the head to be moved in all directions and the beak to be used as a universal 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. 

handbook of avian medicine

Ceratosaurs

Theropoda

1

Allosaurs

Tetanurae

2

Ornithomimosaurs

Coelurosauria

3

Dromaeosaurs

Maniraptora

4

Archaeopteryx

Aves

5

Other birds Fig 1.14  Cladistic relationships of the major groups of theropod dinosaurs (after Gauthier  1986).

Protoavis showed fusion of the ilium and ischium caudally, features that would have strengthened the pelvis and helped to withstand the impact of landing from a height. There were renal fossas indicating that the kidneys were streamlined into the pelvis. The ischium and pubis were open ventrally without a symphysis, which 10

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 proximal 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,

CHAPTER 1: THE DEVELOPMENT OF AVIAN SPECIES

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, such as this, are the habitat in which early birds are believed to have evolved. 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.

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 scapula, 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 formation 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 incubated 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 tarsometatarsus. 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 features 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 geographically isolated areas in the absence of predators, it did not fly. The uncinate processes on the ribs were ossified. The 11

handbook of avian medicine 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.

Feather germ

Condensation of cells

Placode

The placode then forms a unique elongated tube, the feather germ. Dermis of follicle Dermis

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.

Follicle

Epidermis

Feather growth begins with the placode, a thickening of the epidermis over a condensation of cells in the dermis.

Dermal pulp

Epidermis of follicle

Follicle collar

Follicle cavity

Fig 1.17  Feather formation (after Prum & Brush 2004, with permission from Patricia J. Wynne).

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 paddling 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 enormous deltoid crest and a brachial depression at the 12

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 swimming 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 fossil 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 southern hemisphere, swimming off an island near western Antarctica in a shallow marine environment alongside plesiosaurs was Polarornis, the oldest loon (Gaviiformes).

CHAPTER 1: THE DEVELOPMENT OF AVIAN SPECIES

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.

Sheath

Rachis ridge

Barb ridge

Barb ridge

Rachis ridge

Helical growth

Calamus

Rachis ridge

Newly forming barb ridge Follicle collar

Artery

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.

Fig 1.18  Feather formation (after Prum & Brush 2004, with permission from Patricia J. Wynne).

Alongside fossil evidence, evidence from nuclear and mitochondrial DNA hybridization is now placing the origin 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

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.

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 animals, 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 populations from which other areas could be repopulated. The ability to fly, swim, wade or walk would have 13

handbook of avian medicine

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.)

14

CHAPTER 1: THE DEVELOPMENT OF AVIAN SPECIES

Fig 1.21  Pectoral girdle structure in volant birds. Because extended wings have an aerofoil configuration (see B.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.

aided dispersal. Enantiornithines, Hesperornithiformes and Ichthyornithiformes did not survive the extinction event, nor did the pterosaurs, but Neornithes birds survived 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

Fig 1.23  The cervical subluxation of the sulphur-crested cockatoo was reduced by manipulation and the neck placed in a brace attached to 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.

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 15

handbook of avian medicine

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.)

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 development of a flexible joint between the pterygoid and palatine. 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 16

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 southern hemisphere origin for modern birds perhaps around 100 mya. Table 1.2 gives estimates for early avian divergences based on molecular data for these groups calibrated 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,

CHAPTER 1: THE DEVELOPMENT OF AVIAN SPECIES

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.

island chain connections existed between Antarctica and the east coast of Africa via the Keuguelen plateau over the same period. While still speculative, these connections 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. 17

handbook of avian medicine

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.

amongst the placental mammals, who could move rapidly 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:

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 boundary disaster 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.

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 dominant herbivores (e.g. Diatryma of North America and Europe) and predators (e.g. the phorusrhacids of South America). As time moved on, these large flightless birds were vulnerable to emerging apex predators

18



the Tinamidae of South America 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 l l

derived from smaller ancestors that could, with difficulty, fly/swim or wade across the bodies of water that separated 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 northern hemisphere. Perhaps proto loon species were outcompeted 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

CHAPTER 1: THE DEVELOPMENT OF AVIAN SPECIES – 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.

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.)

early offshoot and derived from common ancestry. This group includes:

the Anseriformes: screamers of South America, ducks, geese and other waterfowl and l the Galliformes: chickens, quail and pheasants. l

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)

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 biogeographical event for evolving avifauna was La Grande Coupure – the great cut, so coined by the Swiss palaeontologist Hans Stehlin. Beginning about 60 mya, Australia began to unzip itself from Antarctica as tectonic plate movement slowly drew the continent northwards. 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 global 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 continents. 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; globally birds thrived under diverse circumstances, including Ice Age conditions during the Pleistocene epoch.

19

handbook of avian medicine

Palaearctic Shares 48 families with the Nearctic. 69 families, 1 endemic

Oriental 66 families, 1 endemic

Nearctic 62 families, 1 endemic

Neotropical 86 families, 31 endemic

Ethiopian 67 families, 6 endemic

Australian Approx 83 families, 15 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.

The end of the Ice Age brought the global expansion 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 passenger pigeon, Carolina parakeet and great auk, have also suffered extinctions. From a peak of over 12 000 species 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 20

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 emergence of these features can be difficult. However, they are reflected in anatomy, physiology, behaviour, diversity and distribution of present-day bird species.

CHAPTER 1: THE DEVELOPMENT OF AVIAN SPECIES

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.)

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 reducing 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 endothermic avian ancestors may have nested in burrows as, 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 conditions 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

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 eggincubating birds, also assist in maintaining warmth and shortening the incubation period.

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 compartmentalized within the egg but away from the developing 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 theropod dinosaurs and the Enantiornithines produced eggshells with an internal mammillary layer composed of numerous, tightly packed conical knobs. External to this was the thicker, squamate or spongy zone composed 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, protein cuticle and the spongy zone has vertical palisades separated by minute pore canals. With these innovations, modern bird eggs were less prone to desiccation and parent birds were better able to exploit nesting sites above the ground (Fig. 1.39). 21

handbook of avian medicine

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.

While primitive birds hatched large, downy feathered, precocial young (as evidenced by Gobipipus, ratites, Anseriformes and Galliformes), it is possible for altricial (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

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 oestrogenproducing Sertoli cell tumour of the testicle.

22

Crocodilians have multi-chambered lungs with complex, 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 parabronchial networks, in which airflow is bi-directional, in addition to paleopulmonic parabronchi. Birds’ abdominal 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

CHAPTER 1: THE DEVELOPMENT OF AVIAN SPECIES External zone Squamate zone

Mammillary layer A. Nonavian theropod eggshell

B. Enantiornithine eggshell

C. Ratite eggshell

D. Neognath eggshell

Fig 1.39  Eggshell structure in early and modern birds. Both birds and theropod dinosaurs produced eggs with an internal mammillary layer and an external, thicker spongy layer of calcite crystals arranged on a protein matrix. In addition to this, modern bird eggs have an external layer of a protein cuticle and vertical palisades separated by minute pore canals. This innovation aided in respiration and minimized the risk of eggs desiccating when kept in nests above the ground.

breathing while at the same time streamlining and lightening birds’ bodies for swimming, gliding or flight.

Digestive adaptations Avian digestive systems reflect diet diversity, weight constraints 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 ventriculus 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 rotation 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 assisting 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:

swivel carpal joints for wing folding 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 of the keeled sternum l replacement of teeth with lighter beaks. l l

These changes could be seen to gradually emerge through dromaeosaurs, troodontids Archaeopteryx, Protoavis, Enantiornithines, Hesperornithiformes, Ichthyornithi-formes and Neornithes, but the upsurge and expansion of birds capable of controlled, manoeuv­ rable, flapping flight occurred when the ‘whole package’ of musculoskeletal, soft tissue, reproductive and behavioural features was refined and became widespread. The ‘package’ was versatile, however, and did not just depend on flapping flight. This is evidenced by the diversity of present-day bird species that range in size from the hovering 6.3 cm bee hummingbird of Cuba (3 g) to the flightless 2.5 m tall ostrich (135 kg) of Africa. 23

handbook of avian medicine

Fig 1.40  Being bitten by a flying dinosaur. Passeriformes, such as this Gouldian finch (Erythrura gouldiae), now comprise over half of the species of birds in the world. Like many other species, Gouldian finches in the wild are threatened by disease, habitat clearance and human activity in their range. We are currently witnessing the greatest number of global extinctions since the K-T boundary disaster of 65 mya and our species is the cause. The future of birds is in human hands.

Our generation of humans is the first generation of living, thinking, beings who, working collectively, have been able to unlock the story of over 200 million years of bird evolution. In a practical sense, understanding the developmental stages in the ‘flying dinosaur’ model helps us to understand diverse avian anatomy and physiology and so aids in day-to-day veterinary practice. In a wider sense the story is humbling. Our own species has been given the keys to this amazing story, yet at the same time we have thoughtlessly orchestrated the greatest mass extinctions since the K-T boundary disaster of 65 million years ago. We need to appreciate the diversity of life-forms with which we share the planet, temper the massive destructive powers we hold and act as responsible custodians to halt this unsustainable trend (Fig. 1.40).

References Chatterjee S 1997 The rise of birds, 225 million years of evolution. Johns Hopkins University Press, Baltimore, MD, p 1–224 De Duve C 1995 Vital dust, the origin and evolution of life on Earth. Basic Books, New York, p 1–8 Flannery T 2000 The eternal frontier. Text Publishing Company, Melbourne Gauthier J 1986 Saurischian monophyly and the origin of birds. In: Padian K (ed) The origin of birds and evolution of flight. California Academy of Sciences Memoir, San Francisco, p 1–55 Harrison G L, McLenachan P A, Phillips M J et al 2004 Four new avian mitochondrial genomes help get to basic evolutionary questions in the Late Cretaceous. Molecular Biology and Evolution 21(6):974–983 Kavanau J L 1987 Lovebirds, cockatiels and budgerigars, behaviour and evolution. Science Software Systems, Los Angeles, p 373–640

long J, Schouten P 2008 Feathered dinosaurs: the origin of birds. CSIRO Publishing, Melbourne, p 151–165 Marsh O C 1872 Notice of a new and remarkable fossil bird. American Journal of Science 4:344 Martin L 2002 An early archosaurian origin for birds. IOC Proceedings, Beijing, p 9 Prum R, Brush A 2004 Which came first, the feather or the bird? Scientific American, Special edition, p 72–82 Vickers-Rich P 1996 The Mesozoic and Tertiary history of birds on the Australian Plate. In: Vickers-Rich P, Monoghan J M, Baird R F, Rich T H (eds) Vertebrate palaeontology of Australasia. Monash University Publications, Melbourne, p 721–808

Suggested reading

Simkiss K 1963 Bird flight. Hutchinson Educational, London, p 13–46 Vickers-Rich P, Hewitt-Rich T 1993 Wildlife of Gondwana. Reed, Sydney Warheit K 2001 The seabird fossil record and the role of paleontology in understanding seabird community structure. In: Schreiber E A, Burger J (eds) Biology of marine birds. CRC Press, Boca Raton, p 17–56 Wilson B 1979 Birds, Readings from Scientific American. W H Freeman, San Francisco, p 1–148

Baird R 1996 Avian fossils from the Quaternary of Australia. In: Vickers-Rich P, Monoghan J M, Baird R F, Rich T H (eds) Vertebrate palaeontology of Australasia. Monash University Publications, Melbourne, p 809–870 Sereno P 2002 Birds as dinosaurs. IOC Proceedings, Beijing, p 10

24