Section I—Skeleton
The structure of birds, most of which can fly, has been highly modified to meet the demands of flight. The skeleton has a number of such modifications, most obviously perhaps in the forelimbs, which are adapted to form a bony frame for the wings (Figure 8.1).
Also, however, the skeleton has undergone changes to reduce weight, clearly an advantage in a flying animal, and mobility, which gives the wings a rigid support. Several bones of many birds are pneumatic—hollow and containing extensions of the respiratory system’s air sacs, described in more detail below (Figure 8.2).Skull, Mandible, and Hyoid Apparatus
The bones of the skull (Figures 8.3 and 8.4) are extensively fused to provide strength while minimizing weight. As the sutures are often obliterated, it is diffi-
FIGURE 8.1 Skeleton of the pigeon in left lateral view, superimposed on body outline.
FIGURE 8.2 Humerus of pigeon with proximal and distal ends sectioned to reveal internal structure.
cult to distinguish many of the bones in an adult individual. Attempting to identify each bone is, at this level of study, impractical, and it is more useful to examine various regions of the skull.
Note the large orbits. The often incomplete, bony septum between the orbits is formed by the mesethmoid. The sclerotic ring is a circle of small bones that support the eyeball. The postorbital process lies at the pos- teroventral margin of the orbit. The cranium, posterior to the orbits, is composed of paired frontals that cover most of the roof of the skull, parietals, smaller rectangular bones, and squamosals on the lateral wall of the cranium, and, posteroventrally, the occipital, which is formed from several bones fused into a single unit.
These cranial bones can usually be distinguished, although the sutures between them are often indistinguishable.The quadrate lies toward the ventral part of the orbit and is mobile in birds. It has a prominent orbital process, as well as an otic process, which contacts the cranium. Just ventral to this contact is a large, oval depression, the auditory meatus, which is bounded pos- teroventrally by the paroccipital process and leads into the middle ear. The bony region, pierced by various foramina, visible within the meatus contains the inner ear. The quadrate has a ventral process that articulates with the mandible to form the jaw joint.
The foramen magnum is the large opening in the occipital. At its anterior edge is the single occipital condyle. Anterior to the occipital condyle lies the basioccipital (Figure 8.4), one of the components of the occipital. The basisphenoid lies anterior to the basioccipital and has a tapered anterior end. The parasphenoid lies anterior to this tapered end of the basisphenoid. The basipterygoid processes, one on either side, extend anterolaterally from the posterior end of the parasphenoid and contact the pterygoid, each of which articulates anteriorly with a palatine.
Anterior to the orbit, a complex of bones form the upper jaw and support the bill (Figures 8.1, 8.3, 8.4). This complex is the maxilla, and it includes the nasals, premaxillae, and maxillae (in this sense, as single bony elements). From its dorsal contact with the frontal, each nasal sends out two slender processes, one contacting the maxilla, the other contacting the premaxilla. The latter is a large element forming most of the dorsal and ventral anterior part of the upper jaw. Near its dorsal articulation with the nasal, the premaxillae can, in life, bend or flex slightly dorsally in many birds. The maxilla forms most of the posterior part of the upper jaw ventrally and contacts the palatine posteriorly. Finally, note the zygomatic arch, a slender bridge between the maxilla anteriorly and the quadrate posteriorly.
It is formed almost entirely by the jugal; a small posterior contribution is made by the quadratojugal.The mandible or lower jaw is composed of various bones, but they are difficult to distinguish. The dentary forms nearly the anterior half of the mandible. Its posterior end coincides roughly with the mandibular foramen. Most of the lateral surface posterior to the foramen is formed by the supra-angular. The angular is a smaller bone ventral to the supra-angular. The articular is a small element that articulates with the quadrate of the skull. Two other bones are present but are on the medial surface of the mandible.
The hyoid apparatus (Figure 8.3) is a slender, elongated, Y-shaped structure that supports the tongue. It is formed by various elements, but they are difficult to distinguish and are not considered separately.
Postcranial Skeleton
Vertebrae
The vertebral column (Figure 8.1) normally includes 14 cervical, 5 thoracic, 6 lumbar, 2 sacral, and 15 caudal vertebrae. The column of the pigeon, as with most birds, is notable for its degree of fusion, with the exception of the cervical vertebrae. The atlas and axis are followed by 12 other cervical vertebrae, all fully mobile. The forelimbs of most birds are so specialized for flight that they are unavailable for other functions such as grooming or obtaining food. The long, mobile, S-shaped neck allows some of the functions usually performed by the forelimbs in other vertebrates. The last two cervicals bear small ribs that do not attach to the sternum (see below).
FIGURE 8.3 Skull of the pigeon in left lateral view. Inset figure shows elements in position, and large illustration indicates detail.
There are five thoracic vertebrae, the first four of which are fused together. The thoracics each bear a pair of ribs. The fifth thoracic is fused to the first of the six lumbar vertebrae, which are all fused together and incorporated into the synsacrum (see below), as are the two sacral vertebrae.
Of the 15 caudal vertebrae, the first five are incorporated into the synsacrum, the following six are free and mobile, and the last four are fused together to form the pygostyle (Figures 8.5 and 8.6). The extensive fusion of sections of the vertebral column posterior to the neck renders the trunk rather rigid. This inflexibility may be a feature that helps to reduce weight, as it decreases the need for extensive musculature to maintain a streamlined and rigid posture during flight.Ribs
There are several types of ribs (Figure 8.1). As noted above, ribs are associated with the last two cervical vertebrae. These ribs do not reach the sternum and are often referred to as floating ribs (or bicipital cervical ribs). The five ribs associated with the thoracic vertebrae are each formed from a robust, dorsal element, a vertebral rib, and a more slender, ventral element, a sternal rib. The vertebral rib, as its name implies, extends from the vertebra and articulates with the sternal rib, which in turn articulates with the sternum. In some specimens the last vertebral rib may articulate with the sternal rib of the preceding rib. Note the prominent, posteriorly projecting uncinate processes, which
FIGURE 8.4 Skull of the pigeon in ventral view.
overlap the subsequent vertebral rib and help brace the ribs.
Sternum
The body of the sternum (Figures 8.1 and 8.12) is a large, curved plate of bone. Its most prominent feature is an extremely large vertical plate, the carina or keel. The body articulates anteriorly with the procoracoids (see below) and more posteriorly with the sternal ribs. The large Caudolateral process projects posteriorly from behind the articular surfaces for the sternal ribs and helps form the sternal notch.
Pectoral Girdle and Forelimb
The pectoral girdle of birds is modified to produce a rigid and stable brace for the requirements of flight. These modifications are so pronounced that they usually are retained even in birds that are secondarily flightless.
For example, the scapula, procoracoid, and furcula are tightly bound near the shoulder joint; the procoracoid is a stout, elongated element bracing the forelimbs against the sternum.The scapula (Figures 8.1 and 8.12) is an elongated, blade-like bone that narrows anteriorly. Its anterior end forms part of the glenoid fossa, which articulates with the humerus.
The procoracoid (Figures 8.1, 8.10, and 8.12) is a stout bone. Its posterodorsal surface articulates with the scapula and completes the glenoid fossa. Dorsomedially, it articulates with the furcula (see below). The procoracoid widens ventrally and articulates with the body of the sternum, thus acting as a strut between the sternum and shoulder joint. The triosseal canal is a bony passage formed in many birds by three bones (hence its name), usually the scapula, procoracoid, and furcula, that serves as the passage for the tendon of the supracora- coideus muscle (see below). In the pigeon, however, the canal is formed only by the procoracoid. It is an oval opening located near the dorsal end of the procoracoid, just ventral to its articulation with the furcula.
The furcula (or wishbone) is a structure formed by the ventral fusion of the right and left clavicles and the median interclavicle. It is present in the pigeon, but in some species the clavicles remain unfused. In many mounted skeletons, a ligament extends between the ventral end of the furcula and the anterior end of the carina of the sternum.
The forelimb (Figure 8.1) consists of a stout proximal humerus, followed by the longer radius and ulna. The radius is the straighter, more slender bone. The ulna is bowed and has a short olecranon process distally. Its
FIGURE 8.5 Posterior part of vertebral column and pelvis of the pigeon in dorsal view.
posterior margin has several remigeal papillae, knoblike markings for the attachment of flight feathers.
The manus consists, as usual, of carpals, metacarpals, and phalanges, but these have been highly modified in birds. Two carpals remain unfused: the ulnare, a slender bone that articulates with the ulna, and the radiale, which articulates with the radius. These carpals are followed by the Carpometacarpus, an elongated element composed of several carpals, proximally, and three metacarpals fused together.There has been considerable debate over the homology of the digits of birds, with some researchers considering them homologous with digits 1, 2, and 3 (as is typical of theropod dinosaurs) and other researchers considering them homologous with digits 2, 3, and 4. Recent morphological and developmental analyses suggest that the digits of birds represent digits 1, 2, and 3. The two elongated structures of the manus are metacarpal II (robust and nearly straight) and metacarpal III (slender and bowed). Although it is difficult to discern, metacarpal I (the alular metacarpal) is fused into the proximal end of the carpometacarpus, along with the carpals. The phalanges are also highly modified. Those of the alular digit are represented by the short, triangular fused element, including phalanges 1 and 2, at the proximal end of the carpometacarpus. Phalanges 1 and 2 of digit 2 extend distally from metacarpal II. A small triangular element at the articulation between the car- pometacarpus and phalanx 1 of digit 2 is phalanx 1 of digit 3.
FIGURE 8.6 Posterior part of vertebral column and pelvis of the pigeon in left lateral view.
Pelvic Girdle and Hind Limb
The pelvis (Figures 8.1, 8.5, and 8.6) includes left and right innominate bones, each of which is formed by an ilium, ischium, and pubis. The ilium is the largest element, forming the dorsal half of the pelvis. It has two distinct regions: an anterior concave region and a posterior convex region (in dorsal view). The posterior part of the dorsal iliac crest separates these regions, just dorsal to the acetabulum, the depression that receives the head of the femur (see below). The crest continues posteriorly as the dorsolateral iliac crest. The ischium lies ventral to the posterior part of the ilium. The separation between these bones is marked roughly by the ilioischiadic foramen. The acetabulum is directly anterior to it. Note that the floor of the acetabulum has an opening, the acetabular fenestra. The curved pubis is a very slender and elongated bone extending posteroven- trally from the acetabulum, along the ventral margin of the ischium. Two other openings may be noted. The obturator foramen lies anteriorly between the pubis and ischium; the long and narrow ischiopubic fenestra lies more posteriorly.
A notable feature of birds is that the pelvis is solidly and extensively fused to the synsacrum, the posterior series of fused and expanded vertebrae (see above). The whole unit, pelvis and synsacrum together, form a rigid platform for muscles of the hind limb and tail, and is part of the system that helps a bird to maintain a stable, streamlined posture during flight.
The hind limb (Figure 8.1) includes several bones. The femur is the proximal bone. It is followed by the longer tibiotarsus, which is formed by fusion of the tibia and several tarsals. Articulating anteriorly between the femur and tibiotarsus is the small patella. A slender, splint-like fibula lies along the lateral surface of the tibiotarsus. Several tarsals and the 2nd, 3rd, and 4th metatarsals fuse together to form the tarsometatarsus, which bears a protuberance, the hypotarsus, on its pos- teroproximal surface. Metatarsal I articulates with the posterodistal surface of the tarsometatarsus. There are four digits in the pes, each ending in a claw. The first, or hallux, has two phalanges and is oriented posteriorly, while the three remaining digits point anteriorly. This arrangement, the most common among birds, represents the anisodactyl condition. Other arrangements include the zygodactyl (digits 1 and 4 are reversed) heterodactyl (digits 1 and 2 are reversed), syndactyl (digits 2 and 3 are fused together for much of their length), and pamprodactyl (digits 1 and 4 pivot between facing anteriorly and posteriorly) conditions. Digit 2 has three phalanges, digit 3 has four phalanges, and digit 4 has five phalanges.
Key Terms: Skeleton acetabular fenestra acetabulum angular articular auditory meatus basioccipital basipterygoid processes basisphenoid body of sternum bill (beak) carina (keel) carpals carpometacarpus caudal vertebrae caudolateral process cervical vertebrae dentary dorsal iliac crest dorsolateral iliac crest femur fibula foramen magnum frontals furcula glenoid fossa hallux humerus hypotarsus ilioischiadic foramen ilium innominate ischiopubic fenestra ischium jugal lumbar vertebrae mandible mandibular foramen maxilla (as a complex forming the upper jaw) maxillae (as single bony elements)
mesethmoid metacarpal I (alular
metacarpal) metacarpal II (major
metacarpal) metacarpal III (minor
metacarpal) metatarsal I metatarsals middle ear nasals obturator foramen occipital occipital condyle olecranon process orbits palatine parasphenoid parietals paroccipital patella pes phalanges postorbital process premaxilla procoracoid pterygoid pubis pygostyle quadrate quadratojugal radiale radius remigeal papillae ribs sacral vertebrae scapula sclerotic ring squamosals sternal notch sternal rib sternum
supra-angular
Supracoracoideus muscle
Synsacrum
tarsals tarsometatarsus thoracic vertebrae tibiotarsus
triosseal canal ulna
ulnare uncinate processes vertebral rib zygomatic arch