GENERAL ACCOUNT OF THE SKELETON IN BIRDS.
EXOSKELETON.
The epidermal exoskeleton of birds is very greatly developed, feathers
constituting its most important part.
Three kinds of feathers are found, viz. (_a_) _pennae_ including
quills and coverts, (_b_) down feathers or _plumulae_, and (_c_)
_filoplumes_ which are rudimentary feathers. The structure of the
different kinds of feathers is described on pp. 303-306.
Sometimes a fourth class of feathers, the _semiplumae_, is recognised.
They have the stems of pennae, and the downy barbs and barbules of
plumulae.
In most birds the pennae are not uniformly distributed over the whole
surface of the body, but are confined to certain tracts, the
=pterylae=; while the intervening spaces or =apteria= are either bare
or covered only with down feathers. In some birds, however, such as
the Ratitae and the Penguins, pennae are evenly distributed over the
whole body.
In many birds the calamus or quill bears two vexilla or vanes, the
second of which, called the =aftershaft= or =hyporachis=, is generally
much the smaller, and is attached to the under surface of the main
vexillum. In the Moas, Emeu and Cassowary the two vexilla in the adult
bird are nearly equal in size; though in the nestling Emeu one is much
longer than the other. The aftershaft is very small in most Passeres
and gallinaceous birds, but is comparatively large in Parrots, Gulls,
Herons and most birds of prey. It is absent or extremely small in the
Ostrich, _Apteryx_, _Rhea_, Pigeons, Owls, Anseres, and others.
The quill feathers include two groups, the =remiges= or wing quills,
and the =rectrices= or tail quills. In most birds the primary remiges,
or those which are attached to the bones of the manus, are ten or
eleven in number, and are set in grooves in the bones, being firmly
attached to them. In the Ostrich however the primaries are little
specialised in character and are as many as sixteen in number. They
are also less definitely attached to the bones; as their ends do not
lie in grooves in the bones, but project beyond them.
The secondary quills or those attached to the ulna vary much in number
according to the length of the bone. The large dark quills in the
wings of Cassowaries are the secondaries.
The wing of Penguins is very little differentiated. It is covered at
the margin by overlapping scales which gradually merge into scale-like
feathers at the proximal end. The wing of the Penguin has nothing
comparable to the remiges of other birds.
In some birds, such as Herons (_Ardea_), there occur in places
plumulae of a peculiar kind, which grow persistently and whose summits
break off into fine powder as fast as they are formed. These feathers
are known as _powder-down_ feathers. They occur also in some Parrots
and are then scattered indiscriminately all over the body.
Other exoskeletal structures besides feathers are commonly well
developed. Thus the extremities of the jaws are sheathed in horny
=beaks= whose form varies enormously according to the special mode of
life.
In ducks and geese the beak with the exception of the anterior end is
soft, and its edges are raised into lamellae, while in the Mergansers
these lamellae become pointed processes supported by bony outgrowths.
These lamellae act as strainers. In Parrots and Hawks, on the other
hand, nearly the whole of the beak is hard.
The toes and tarso-metatarsus are usually featherless and are covered
either with granular structures or with well-formed scales. The toes
are nearly always provided with =claws=, and these vary in correlation
with the character of the beak. Claws[105] also sometimes occur on the
manus. Thus _Archaeopteryx_ and some Ostriches and Rheas have claws on
all three digits. Most Ostriches and Rheas, and many Anseres and birds
of prey, have them on the first two digits, while the Secretary bird
(_Gypogeranus_) and many fowls, ducks, and birds of prey, especially
kestrels, have a claw only on the pollex. In the Cassowary, Emeu,
Apteryx and some Ostriches and Rheas only the second digit is clawed.
Claws should not be confounded with =spurs=, which are conical horny
structures developed on bony outgrowths of the radial side of the
carpus, metacarpus, or metatarsus. They occur in a number of birds,
but are most commonly developed in gallinaceous birds, by which they
are used for fighting. A single spur occurs on the metacarpus in
_Megapodius_, in _Palamedea_, in _Parra jacana_ and in _Hoplopterus
spinosus_, the Spur-winged plover. The Derbian Screamer, _Chauna
derbiana_, has two metacarpal spurs, borne on the first and second
metacarpals. The Spur-winged goose, _Plectropterus gambensis_, has a
carpal spur borne on the radial carpal. Metatarsal spurs are quite
common.
The male Solitaire (_Pezophaps_) has large bony excrescences on the
wrist which may, like spurs, have been sheathed in horn and used for
fighting.
=Teeth= do not occur in any living birds, but conical teeth imbedded
in separate sockets are present in _Archaeopteryx_ and _Ichthyornis_,
while in _Hesperornis_ similar teeth occur implanted in continuous
grooves in the mandibles and maxillae, the premaxillae being toothless.
Except that teeth are partly dermal in origin, a dermal exoskeleton is
quite unrepresented in birds.
ENDOSKELETON.
Perhaps the most striking feature of the endoskeleton of birds is its
pneumaticity. In the embryo all the bones contain marrow, but as
growth proceeds this becomes replaced by air to a variable extent in
different forms. In all birds some part of the skeleton is pneumatic.
Many small birds and _Apteryx_ and Penguins among larger ones have air
only in the skull; in Pigeons air is present in all the bones except
the caudal vertebrae, the leg bones, and those of the antibrachium and
manus; in Hornbills every bone contains air.
[Illustration FIG. 62. THIRD CERVICAL VERTEBRA OF AN OSTRICH
(_Struthio camelus_). × 1. A anterior, B posterior, C dorsal view (A
and B after MIVART).
1. neural spine.
2. neural canal.
3. prezygapophysis.
4. postzygapophysis.
5. posterior articular surface of centrum.
6. anterior articular surface of centrum.
7. vertebrarterial canal.
8. hypapophysis.]
VERTEBRAL COLUMN.
The vertebral column of birds is readily divisible into a very mobile
cervical region, and an extremely rigid post-cervical region. In most
birds the vertebral centra are without terminal epiphyses, but these
structures are found in Parrots. The cervical vertebrae are generally
large and vary in number from eight or nine to twenty-three in Swans.
Except in some extinct forms, such as _Ichthyornis_ and _Apatornis_,
in which they are biconcave, the centra are characterised by having
saddle-shaped articulating surfaces, which in front are concave from
side to side and slightly convex from above downwards, while
posteriorly they are convex from side to side and concave from above
downwards. The atlas is small and ring-like, and its centrum is fused
with the axis forming the odontoid process. Cervical ribs are often
well developed, and in some of the Ratitae they remain for a long time
distinct from the vertebrae.
The thoracic vertebrae are distinguished from the cervical by the fact
that their true ribs are united to the sternum by means of sternal
ribs. This distinction, however, though convenient, is somewhat
arbitrary, as it has been shown that in the fowl and gannet, two pairs
of ribs which in the adult are free from the sternum, are connected
with it in the embryo. When, as in the Swans, the thoracic vertebrae
are not all fused together, they generally have saddle-shaped
articulating surfaces, but sometimes, as in the Penguins, Auks and
Plovers, the centra are convex in front and concave behind. The trunk
vertebrae generally have well-marked neural spines, while in the
Divers the anterior ones have peculiar bifurcating hypapophyses.
The trunk vertebrae are not readily divisible into thoracic and
lumbar. There are two true sacral vertebrae, but as development
proceeds a number of other vertebrae become fused with the true
sacrals, the whole forming a large compound sacrum. These pseudosacral
vertebrae generally include the lumbar, and some of the thoracic and
caudal vertebrae. Sixteen to twenty vertebrae or even more may be
included in the compound sacrum, and sometimes the whole of the trunk
vertebrae are fused together. In _Archaeopteryx_ however but five
vertebrae take part in the formation of the sacrum.
In _Archaeopteryx_ there are twenty long caudal vertebrae, of which
the last sixteen carry a pair of feathers apiece, but in all other
birds the tail is short and in the great majority of cases the
posterior vertebrae are fused together, forming the pygostyle. In the
Ratitae and Tinamidae a pygostyle is rarely or imperfectly developed.
In _Hesperornis_ there are twelve caudal vertebrae, six or seven of
which are united by their centra only, forming an imperfect pygostyle.
The free caudal vertebrae are generally amphicoelous.
THE SKULL.
The skull of all birds from _Archaeopteryx_ onwards is essentially
similar, differing from the skull of reptiles mainly in the extent to
which the cranium is arched, and its greater size in proportion to the
jaws.
Most of the bones of the cranium are pneumatic, and all show a marked
tendency to fuse together, and have their outlines obliterated by the
disappearance of the sutures. The several bones remain longest
distinguishable in the Ratitae and to a less extent in the Penguins.
The orbits are very large and lie almost entirely in front of the
cranium; they are separated by an interorbital septum which is
sometimes, as in _Chauna_ and _Scythrops_, very complete, sometimes,
as in Hornbills and the Common Heron, very slightly developed. As a
general rule the sclerotic is cartilaginous.
The anterior nares are almost always situated far back at the base of
the beak near the orbits, but in _Apteryx_ they are placed right at
its extremity. In _Phororhacos_ they are placed very high up on the
enormous beak and are not separated by any bony partition.
The skull of Parrots has some peculiarities. In some Parrots the
lachrymal sends back a process which meets the postorbital process of
the frontal and completes the orbit. In most birds the upper beak is
immovably fixed, but in some it is attached to the cranium, only by
the nasals and by flexible processes of the premaxillae, so that by
this means a kind of elastic joint is established and the beak is able
to be moved on the cranium. In the Parrots and _Opisthocomus_ there is
a regular highly movable joint.
In Cassowaries the fronto-nasal region of the skull is produced into
an enormous bony crest, and in Hornbills a somewhat similar structure
occurs. Although true teeth do not occur in any known bird except
_Archaeopteryx_, _Hesperornis_, and _Ichthyornis_, another extinct
bird, _Odontopteryx_, has the margins of both jaws provided with
forwardly-directed tooth-like serrations, formed of part of the actual
jawbone: a living hawk, _Harpagus_, too, has a deeply notched bill, to
which correspond serrations in the premaxillae.
A basi-pterygoid process of the basisphenoid abuts against the
pterygoid in Ratitae and in Tinamous, plovers, fowls, pigeons, ducks
and geese among Carinatae, recalling the arrangement met with in many
reptiles. The squamosal is sometimes, as in the fowl, united with the
postorbital process of the frontal. In the Carinatae the quadrate
articulates with the cranium by a double convex surface, in the
Ratitae by a single one. The premaxillae are always comparatively large
bones, the maxillae on the contrary are small, but give rise to
important inwardly-projecting maxillo-palatine processes.
The relations of the palatines, pterygoids, maxillae, and vomers vary
considerably, and on them Huxley has based a classification of
birds[106]. In the Ratitae and the Tinamous (Tinamidae), among
Carinatae the vomers unite and form a large broad bone, separating the
palatines and the pterygoids from the rostrum. Huxley uses the term
=Dromaeognathous= to describe this condition. In all other Carinatae
the vomers are narrow behind, and the palatines and pterygoids
converge posteriorly and articulate largely with the rostrum. Three
modifications of this condition are distinguished by Huxley, and
termed =Schizognathous=, =Ægithognathous=, and =Desmognathous=.
In the =Schizognathae= the vomers coalesce and form a narrow elongated
bone, pointed in front, separating the maxillo-palatine processes of
the premaxillae. Waders, fowls, penguins, gulls, some falcons and
eagles, American vultures, some herons and many owls have the
Schizognathous arrangement. In pigeons and sandgrouse there is no
vomer, but the other bones have the Schizognathous arrangement.
In the =Ægithognathae= the arrangement is the same as in the
Schizognathae, except that the vomers are truncated in front.
Passeres, swifts, woodpeckers, humming birds, rollers, hoopoes have
this arrangement.
In the =Desmognathae= (fig. 60, A) the maxillo-palatine processes
approach one another in the middle line, and either unite with the
vomers, or unite with one another, hiding the vomers. Thus a more or
less complete bony roof is formed across the palate. The vomers in
Desmognathae are small or sometimes absent. Ducks, storks, most
herons, most birds of prey and owls, pelicans, cormorants, parrots,
and flamingoes are Desmognathous.
The mandible, as in other Sauropsids, consists of a cartilage bone,
the articular, and a series of membrane bones, the dentary, splenial,
coronoid, angular, and supra-angular, developed round the unossified
Meckel's cartilage. The dentaries of the two rami are nearly always
fused together, but in _Ichthyornis_ and _Archaeopteryx_ the two rami
are but loosely united. There is often a fontanelle between the
dentary and the posterior bones, while the angle is sometimes, as in
the fowl, drawn out into a long curved process.
The hyoid apparatus (fig. 59, C) consists of a median portion, and a
pair of cornua. The median portion is composed of three pieces placed
end to end, and called respectively the os entoglossum, the basi-hyal,
and the uro-hyal. The os entoglossum is shown by development to be
formed by the union of paired structures and is probably homologous
with the hyoid arch of fishes. The basi-hyal and the long cornua, each
of which is composed of two or three pieces placed end to end, are
homologous with the first branchial arch of fishes, while the uro-hyal
is probably homologous with the second branchial arch of fishes. In
Woodpeckers the cornua are enormously long, and curve over the skull,
extending as far forwards as the anterior nares.
RIBS AND STERNUM.
Well-developed ribs are attached to the posterior cervical vertebrae
as well as to the thoracic vertebrae. The ribs generally have uncinate
processes and separate capitula and tubercula, but uncinate processes
are absent in _Chauna Palamedea_ and apparently in _Archaeopteryx_.
The sternum (fig. 63) is greatly developed in all birds. In the
embryo[107] it is seen to be derived from the union of right and left
plates of cartilage, formed by the fusion of the ventral ends of the
ribs. In the Ratitae and a few Carinatae, such as _Stringops_, it is
flat, but in the great majority of birds it is keeled, though the
development of the keel varies greatly. It is large in the flightless
Penguins, which use their wings for swimming. Traces of an
interclavicle may occur in the embryo.
PECTORAL GIRDLE.
[Illustration FIG. 63. SHOULDER-GIRDLE AND STERNUM OF
A. BLACK VULTURE (_Vultur cinereus_) × 1/3.
B. PEACOCK (_Pavo cristatus_) × 3/8.
C. PELICAN (_Pelicanus conspicillatus_) × 1/3. (All Camb. Mus.)
1. carina of the sternum.
2. coracoid.
3. scapula.
4. clavicle.
5. costal process.
6. surfaces for articulation with the sternal ribs.
7. xiphoid processes.
8. fontanelle.]
The pectoral girdle is also strongly developed in all Carinatae, but
is much reduced in Ratitae. In some Moas the sternum has no facet for
the articulation of the coracoid, and the pectoral girdle appears to
have been entirely absent; it is extremely small also in _Apteryx_.
Clavicles are generally well developed in the Carinatae, and small
ones are found also in _Hesperornis_, and in Emeus and Cassowaries. In
the other living Ratitae and in _Stringops_ they are absent. In some
Parrots, Owls and Toucans they do not meet one another ventrally.
Clavicles are especially stout in some of the birds of prey. They do
not generally touch the sternum, but sometimes, as in the Pelican
(fig. 63, C), Adjutant and Frigate bird, they are fused with it.
In all Ratitae the scapula and coracoid lie almost in the same
straight line with one another, in the Carinatae they are nearly at
right angles to one another.
ANTERIOR LIMB.
In the wing of nearly all birds the ulna is thicker than the radius,
but in _Archaeopteryx_ the two bones are equal in size. In the wing of
_Archaeopteryx_ there are three long digits with distinct metacarpals.
In all other birds the digits are modified, the metacarpals being
commonly fused and the phalanges reduced in number. In _Palamedea_ and
some other birds the metacarpus bears a bony outgrowth, which when
sheathed in horn forms a spur.
In most of the Ratitae and in the extinct Dodo (_Didus_) and Solitaire
(_Pezophaps_) the wing is very small, but the usual parts are
recognisable. In _Hesperornis_ apparently only the humerus is present;
in some Moas, in which the wing is imperfectly known, the presence of
the humerus is indicated by traces of a glenoid cavity. In most Moas
the wing is apparently completely absent. As compared with those in
other Ratitae, the wings of the Ostrich and Rhea are well developed.
In the Ostrich (fig. 64, B) and Rhea, as in nearly all Carinatae, the
manus has three digits, but in _Apteryx_ there is only a single digit,
the second. The Penguins (fig. 64, A) too among Carinatae have only
two digits, but in their case it is the pollex which is missing. In
the Ostrich the third digit has two phalanges, in all other living
birds it has only one phalanx.
PELVIC GIRDLE.
[Illustration FIG. 64. BONES OF THE RIGHT WING OF
A. A PENGUIN × 1/3. (Camb. Mus.)
B. OSTRICH (_Struthio camelus_) × 1/7. (Partly after PARKER.)
C. GANNET (_Sula alba_) × 1/3. (Camb. Mus.)
In C the distal phalanges of the pollex and second digit have been
omitted.
1. humerus.
2. radius.
3. ulna.
4. second metacarpal.
5. third metacarpal.
6. pollex.
7. second digit.
8. cuneiform.
9. sesamoid bone.]
Birds have a very large pelvis and its characters are constant
throughout almost the whole group. The ilium is very large, and is
united along its whole length with the sacral and pseudosacral
vertebrae. The ischium is broad and extends back parallel to the ilium
with which in most birds it fuses posteriorly, further forward the
ilio-sciatic foramen separates the two bones. In _Tinamus_,
_Hesperornis_, _Apteryx_ (fig. 65, B, 2), and _Struthio_, the ischia
are separate from the ilia along their whole length except at the
acetabulum; in _Phororhacos_, on the other hand, the two bones are
fused along almost their whole length. The bone usually called the
pubis in birds corresponds to the post-pubis of Dinosaurs and forms a
long slender rod (fig. 65, 3) lying parallel to the ischium. In many
birds the ischia and pubes are united at their distal ends. This is
the case in the Ostrich (fig. 65, D), in which the ilia and ischia are
widely separated. In many birds the pubis is drawn out in front into
the pectineal process, this is specially large in _Apteryx_ (fig. 65,
B, 5), and in the embryos of many birds. It is probably homologous
with the pre-pubis of Dinosaurs but in some birds is formed in part by
the ilium. The acetabulum in birds is always perforate.
In _Rhea_ (fig. 65, C, 2) and probably in _Archaeopteryx_ a symphysis
ischii occurs, and in the ostrich alone among birds there is a
symphysis pubis. In _Archaeopteryx_ all three bones of the pelvis are
distinct, but they are imperfectly known. In Ichthyornis they are also
distinct, in all other known birds they are fused together to a
greater or less extent.
[Illustration FIG. 65. PELVIC GIRDLE AND SACRUM OF
A. CASSOWARY (_Casuarius galeatus_) × 1/8.
B. OWEN'S APTERYX (_A. oweni_) × 1/2.
C. BROAD BILLED RHEA (_R. macrorhyncha_) × 1/6.
D. OSTRICH (_Struthio camelus_) × 1/10. (All Camb. Mus.)
1. ilium.
2. ischium.
3. pubis.
4. acetabulum.
5. pectineal process.]
POSTERIOR LIMB.
The tibia is always well developed and has a very strong cnemial
crest. The proximal tarsals are fused with its distal end, the whole
forming a compound bone, the tibio-tarsus. There is frequently an
oblique bar of bone crossing the anterior face of the tibio-tarsus at
the distal end, just above the articular surface of the
tarso-metatarsus, this is absent in Ostriches and _Æpyornis_. The
fibula though in the embryo and in _Archaeopteryx_ equal in length to
the tibia, is in the adult of other birds always imperfect, its
proximal end is often fused with the tibia, and its distal end is
commonly atrophied. In the Penguins however the distal end is
complete. The distal tarsals fuse with the second, third and fourth
metatarsals, forming a compound bone, the tarso-metatarsus. The first
metatarsal is nearly always free but occasionally as in _Phaëthon_ it
is fused with the others. No adult bird has more than four digits in
the pes. In the Penguins the metatarsals are separate, and in many
birds larger or smaller gaps exist between the fused metatarsals. In
most birds the third metatarsal is curved so as not to lie in the same
plane as the others, but in the Penguins they all three lie in the
same plane. The metatarsals are clearly separated in _Archaeopteryx_.
In Gallinaceous birds the tarso-metatarsus bears a bony outgrowth
which is sheathed in horn and forms a spur.
In most birds the first four toes are present while the fifth is
always absent. The first toe commonly has two phalanges, the second
three, the third four, and the fourth five. In Swifts the third and
fourth toes have only three phalanges. Many birds, such as all Ratitae
except _Apteryx_, have only three toes, the hallux being absent; in
the Ostrich the second toe is also gone with the exception of a small
metatarsal, so that the foot retains only the third and fourth digits,
the third being much the larger of the two and bearing a claw, while
the fourth is clawless.
In the Swifts, Cormorants, and Penguins, all four toes are directed
forwards. In most birds the hallux is directed backwards, and the
other toes forwards. In the Owls the fourth toe can be directed
backwards as well as the hallux, while in Parrots, Cuckoos,
Woodpeckers, and Toucans the fourth toe is permanently reversed. In
Trogons the second toe is reversed in addition to the hallux, but not
the fourth.
FOOTNOTES:
[105] W.K. Parker, _Phil. Trans._ vol. 179, p. 385, 1888; and _Ibis_,
1888, p. 124.
[106] See T.H. Huxley, "On the Classification of Birds," _P.Z.S._
1867.
[107] B. Lindsay, _P.Z.S._ 1885, p. 684.