The Locomotor Skeleton
The Necessity for Animal Locomotion
Attention has already been called in a general way to the necessity for locomotion among animals as contrasted with plants.
The essential difference between plants and animals with reference to locomotion is that green plants by the aid of chlorophyll, which makes them green, are able to imprison the sun’s energy by building up into organic foods inorganic compounds that are universally distributed. In consequence they waste no energy in locomotion and have a generous supply of food available for growth and reproduction as well as a surplus for animals. Animals, on the contrary, without the Aladdin’s lamp of chlorophyll, must seek their food directly or indirectly, and usually with locomotor effort, wherever plants have made it. Otherwise they perish.
The chemical elements common to all protoplasm, and therefore the food of both animals and plants, are well-nigh universal in distribution in the form of carbon dioxide in the air, water, and various salts and substances in the soil (Fig. 521), while sunlight, the primal source of all energy possessed by organisms of any and every kind, shines alike upon both plants and animals. Since, however, plants alone can utilize the sunlight in transforming these elements into food, and since they can do this in a stationary position, they do not need to move about for their daily bread, while plant-dependent animals do.
Evolution of Locomotor Devices
Before skeletal muscles and locomotor levers were arrived at in vertebrates, many other devices for accomplishing motion and locomotion were tried out, more or less successfully, in the animal kingdom.
The inherent contractility of protoplasm is demonstrated even by the modest pseudopods of Amoeba. In the microscopic universe of a drop of water other kinds of protozoans also are seen to have speeded up their movements by employing cilia and flagella. Such structures are still retained among higher forms to produce motion even when they are no longer available in locomotion, as for example, cilia bringing food particles into the gullet of a sedentary clam, or removing particles from the respiratory passages of air-breathing animals.
The acrobatic Hydra, as described as early as 1744 in the remarkable Memoires of Tremblay, pioneer observer and experimenter with Lilliputian life, gaily progresses along the under side of the surface film of water by the method of turning somersaults (Fig. 522). Writhing worms and wiggling vertebrates of one kind or another fill in another chapter in the story of locomotor evolution, but it was when vertebrates emerged from water to land, and levers in the form of legs came upon the scene, that the greatest advance in locomotion was initiated. Once out of water animals could no longer go forward fin-fashion by lateral tailstrokes, for the air is not a sufficiently dense medium to make such strokes effective.
Considerable time elapsed during the transition from water to land before the lateral legs of primitive land vertebrates assumed a vertical position underneath the body, and sufficient strength and stability were developed to raise the body off the ground. Even then elongated animals, like salamanders and alligators, for example, made little attempt to bear the weight of the body on the legs. Since these appendages extend somewhat laterally, like oars from a boat, they were used principally to push the animal along, with the weight of the body resting on the ground (Fig. 523). After the weight-bearing function finally became established, nature tried many experiments with locomotor levers all the way from the sprawling plantigrade foot of amphibians, reptiles, and less specialized orders of mammals, to that of the wonderfully specialized horse, which stands stilted on the tips of single digits, one at the end of each leg (Fig. 524).
Kinds of Appendages
Vertebrate locomotor appendages, which are fewer and less specialized than those of invertebrates, may be paired or unpaired. The latter sort, confined to water animals, are the more primitive, taking the form of median fins, which *are either continuous, as in amphioxus, or broken up into separate dorsal, caudal, and ventral fins, as in fishes.
In addition to median fins fishes normally have two pairs of paired fins, namely, pectoral and pelvic, which are homologous with the locomotor appendages of land vertebrates.
Since paired fins take no part in bearing the weight of the body, supported as it is by the water medium, they are not placed in the same key positions as are the legs of a quadruped, but instead may appear on the sides of the body at widely varying points in different species. With the earliest development of a neck in land animals the pectoral appendages tended to shift backward, but in fishes particularly, the pelvic appendages are apt to move forward from the normal position. In a case as extreme as that of the cod, Gadus, the pelvic fins became placed even anterior to the pectoral fins, that is to say, the “hind legs” of a codfish are in front of its “front legs” (Fig. 525).
Both the unpaired and the paired fins of fishes are used primarily either for propulsion or to prevent rotation of the animal on its long axis and to steer it. Propulsion is usually taken care of by the caudal fin as part of the powerful tail. None of the vertebrates has more than two sets of paired appendages, while several have only one, for example, whales and sea cows with only pectorals, and that famous wingless New Zealand bird Apteryx, which possesses only the rudiments of a wing skeleton. A few vertebrates, notably snakes, caecilians, and legless lizards, lack appendages of any kind, although some snakes, pythons for example, have rudiments of the pelvic appendages.
Origin of the Girdles and Appendages
Concerning the origin of paired fins, the forerunners of all vertebrate appendages, the two most prominent theories have been Gegenbaur’s gill-arch theory, which now seems to have too little evidence to support it, and Thacher’s fin-fold theory, which fits in with the known facts of embryology and palaeontology as well as of comparative anatomy. According to the latter theory there was a median unpaired fold extending from the head along the entire length of the dorsal side of the animal, around the tip of the tail, and forward as far as the anus. In addition, along the ventrolateral regions of the trunk there was a pair of folds, converging posteriorly, which may or may not have met at the level of the anus and have joined the ventral part of the unpaired fold at that point. From this primitive plan, the set of individual fins, both paired and unpaired, may be derived by the dropping out of some portions and the increased development of others.
The embryonic development of one of the pelvic fins of a dogfish, which more or less parallels the evolution of paired appendages according to the fin-fold theory, may be divided into a series of arbitrary stages that pass continuously from one into the next. These stages are: (1) epidermal ridge; (2) fin fold; (3) mesenchymal invasion; (4) muscle-bud penetration; (5) cartilage formation; (6) concentration; (7) concrescence; and (8) union.
First an epidermal ridge appears as a narrow, longitudinal elevation, frequently extending over many more segments than will participate in the formation of the fin. In some elasmobranchs such a ventro-lateral ridge develops along the entire length of the trunk (Fig. 526).
In the anterior and posterior portions of the ridge region large fin folds of the body wall appear. From these folds, pectoral and pelvic fins, respectively, will develop, while the middle section of the ridge will disappear.
Mesenchymal invasion of the fold is soon followed by muscle-bud penetration during which one or two buds grow into the fold from each myotome adjacent to this region.
Between successive muscle buds cartilage formation, through the activity of mesenchymal cells, takes place, giving rise to more or less parallel rows of elongate radial cartilages (Fig. 527). At approximately the same time, a concentration, or crowding of structures, in the base of the fin occurs due to the failure of this basal region to keep pace, in its growth, with the rest of the fin and with the body proper. It is believed that in the course of evolution a concrescence, or fusion, of the crowded basal portions of the primitive radials gave rise to the large basal cartilages. In development these three stages are telescoped together, instead of following one after the other, so that by the time the procartilaginous stage is reached there is a continuous basal mass from which extend out finger-like processes in which the radials will develop (Fig. 528).
Up to this point the development of the median fins parallels rather closely that of the paired fins, as might be expected if all of these appendages are but localized enlargements of one continuous system. The basalia of the median fins extend into the body to come in contact with the vertebral column with which they articulate permanently. The basalia of the paired fins, in the absence of other hard skeletal parts in the ventral region of the body, undergo further modification. The most anterior basal enlarges and extends into the ventral body wall until it meets the corresponding part of the opposite side with which it fuses. As a result of the union of these two basals a transverse bar, a primitive girdle, is laid down (Fig. 527).
Homology and Adaptation
The paired appendages of vertebrates above the fishes are all built on the same plan, that is, of the same sequence of bones. This consists typically of a tripod of bones known as the girdle, which is intermediate between the appendage and the backbone; a large shaftlike bone, called either the humerus or femur, according to whether it occurs in the anterior or the posterior pair of appendages; two long bones side by side, the radius and ulna, or the tibia and fibula respectively; a complex of several small bones, making the wrist or ankle; a set of five long slender bones, forming the palm or the sole; and lastly, at the tip of each of the palm or sole bones, two, three, or more small cylindrical bones, placed end to end, known as the digits or phalanges. For a diagrammatic representation of this sequence of bones in the appendages of a land vertebrate, see Figure 529.
The principal joints or landmarks of the locomotor skeleton in man are indicated in Figure 530.
Each bone of any appendage has its counterpart not only in the appendage on the opposite side, but also in the appendage in front of, or behind it, as the case may be. The similarity from side to side is spoken of as bilateral homology, while anteroposterior correspondence of parts is called serial homology.
Not only may homology between the bones that make up the locomotor appendages of a single individual be established inter se, but the leg or arm bones of one vertebrate may be homologized with those of an entirely different species of quite unlike external aspect. For example, each bone in the flipper of a whale or a seal, as well as in the wing of a bird, or even in the foreleg of a horse or a dog, has its homologue in the human arm.
Although fundamentally alike, vertebrate appendages exhibit a great diversity, which is associated with the wide range of function that they perform. Climbing trees, burrowing in the ground, swimming in water, jumping, flying, running, standing, striking, lifting, and grasping things, as well as many other kinds of activity, call for particular modifications of the type.
The Comparative Anatomy of Girdles
Girdles in General
Excepting in elasmobranchs, the girdles, or intermediary bones between the body and the limbs, are originally made up of three bones on either side (Fig. 529), which meet in the form of a tripod at a common point where the free limb articulates. The triple character of the girdles is best seen in reptiles, especially in some extinct fossil forms, rather than in mammals where drastic modifications have taken place.
In the pectoral, or anterior girdle, there is usually no articular connection with the main axial skeleton. The girdle is laced to the anterior part of the thoracic basket by means of ligaments and muscles. It may articulate with the sternum, as for instance in man, but never with the backbone except in rays and in certain pterosaurs.
The pelvic, or posterior girdle, on the contrary, except in fishes, always articulates with the backbone, through the medium of the “sacral ribs”. This difference in attachment gives a greater range of motion to the pectoral appendages and a firmer support to the pelvic appendages, which in many cases, particularly in bipeds, bear the greater weight of the body.
The three girdle bones of each pectoral appendage occupy positions of serial homology with respect to the girdle bones of the pelvic appendages. Thus, one bone, respectively the scapula or the ilium, extends dorsally; another, the procoracoid or the pubis, is placed antero-ventrally; and a third, the coracoid or the ischium, postero-ventrally.
The articular cup for the front leg at the junction of the three pectoral girdle bones is called the glenoid cavity, while the corresponding articular fossa on the pelvic girdle for the reception of the hind leg by reason of its hollow shape has been named the acetabulum, or “vinegar cup.”
Although at first modeled in cartilage, all of these girdle parts afterwards become replaced by bone. They, therefore, belong to the category of replacing bones, similar to those of the inner skull. There are, however, certain additional bones of investing character in the pectoral girdle of fishes, as well as in other vertebrates including man, which put in their appearance without preliminary blue prints in cartilage. The principal one of these is the clavicle, which is substituted for, or takes over the work of, the procoracoid. The fact that it is not a transformed procoracoid but, instead, a new bone of entirely different origin, is demonstrated by the pectoral girdle of the European toad Bombinator (Fig. 531), in which the procoracoid and the clavicle are both found present at the same time.
Unlike the pectoral girdle the pelvic girdle has nothing corresponding to the thoracic basket with which to become involved. It is concerned solely with its hook-up to the vertebral column. Like its pectoral homologue it consists typically of three parts, a dorsal element, the ilium, and two ventral elements, of which the pubis is anterior and the ischium posterior, forming tripods on either side for the articulation of the hind legs (Fig. 529). All three pairs of pelvic girdle bones are replacing in character. Their typical relation to each other and to the backbone undergoes some striking modifications in the vertebrate series.
The pelvic girdle in fishes, when present, is very simple, as would be expected, serving merely as a support for the pelvic fins without making connection with the axial skeleton. In elasmobranchs and cartilaginous ganoids it is a flat central bar of cartilage (Fig. 532c), the origin of which is suggested by Pleuracanthus, a fossil elasmobranch (Fig. 532 a), as well as by Acipenser, a chondrostean (Fig. 532b), in which two enlarged cartilaginous plates approach each other on the ventral side of the body without uniting. In the Holocephali the two parts do not fuse but are connected by a ligament, and each bears an iliac process extending dorsally from the region of fin attachment.
The Dipnoi, as represented by Protopterus (Fig. 533), have a median ventral cartilaginous ischio-pubic plate of bilateral origin serving as the pelvic girdle, with six processes extending from it.
Stegocephalians (Fig. 534), pioneers among walking tetrapods, possessed a broad ischio-pubic plate similar to that of the Dipnoi, but with improvements in the form of bones, large ischia that replaced the cartilage in the posterior region of the plate and smaller pubes in the anterior part. In each pubis was a small pubic foramen through which the obturator nerve passed. Two separate iliac bones, which replaced the iliac processes, extended dorsally to reach the vertebral column.
Urodeles, in common with most modern amphibians, have bony ilia and ischia but cartilaginous pubes. The ilia reach the single sacral vertebra (except in Proteus and Amphiuma which have degenerate hind legs), joining it by means of a pair of small intermediate parts known as sacral ribs (Fig. 535), Pubic foramina are also present.
In some urodeles, for example Cryptobranchus, there appears, in the midventral linea alba, an independent Y-shaped ypsiloid cartilage that connects secondarily with the pelvic girdle.
Although considerable modification of the pelvic girdle takes place in most anurans due to their hoppipg and jumping methods of locomotion, the African toad, Xenopus (Fig, 536), shows a generalized pelvic girdle with three pairs of contributing bones all typically ossified from cartilaginous forerunners, and, in addition, the ypsiloid cartilage, which in this case is not forked but spatulate in shape.
In the frog Rana, however, the three pairs of pelvic elements forrn a U-shaped structure that connects the jumping legs With the single sacral vertebra. Ilia and ischia are bony, while the pubes are composed of calcified cartilage. The legs are articulated on either side of a found disc, which is made up of components from all three pelvic elements so welded together that the pubic foramen is obliterated entirely. From this disc springs upward a pair of swordlike extensions, the ilia, that reach the vertebral column which teeters up and down suspended between their tips, thus absorbing in part the shocks that would otherwise reach the brain when the jumping frog lands.
In reptiles all of the pelvic bones are well developed and distinct. In many there is a symphysis, or union, of both pubic and ischiac bones along the midventral line although frequently a large open space, the ischio-pubic fenestra, develops on either side between the pubis and ischium resulting usually in a complete separation of pubic and ischiac symphyses (Fig. 537). In crocodiles only an ischiac symphysis occurs, the pubic bones remaining slightly separated (Fig. 538).
A pubic foramen persists in Sphenodon, the plesiosaurs, and lizards; but in turtles and crocodiles it combines with the ischio-pubic fenestra into a common opening separated from its mate on either side by a median ligament, and is then termed the obturator foramen (foramen obturatum).
In crocodiles the pubis does not participate in the formation of the articular cup, or acetabulum, for the attachment of the hind leg. This cup is perforated by an acetabular foramen in crocodiles, birds, and monotremes, but not in mammals generally. Ichthyosaurs, which used their tails in swimming, as well as cetaceans and sirenians that have no use for hind legs, are characterized by a greatly reduced pelvis since locomotion is not dependent upon it.
Among the legless snakes the pythons alone retain a trace of the pelvic girdle, reminiscent of the remote past when the ancestors of snakes walked (Fig. 539).
Dinosaurs among the reptiles of the past gave prophecy of the modifications which characterize the pelvic girdles of birds. For example, the girdle of the fossil reptile Stegosaurus (Fig. 540) shows a spreading fan-shaped ilium, a long ischium extending posteriorly without a symphysis, and a backward-projecting pubis on either side that runs parallel to the ischium instead of meeting anteriorly and ventrally in a pubic symphysis. The place of a typical pubis in some instances is partly filled by an anterior prepubic process.
Modern birds exemplify all of these features, with the ilium enormously expanded and brought in contact with many vertebrae. The prepubic processes are reduced or absent (Fig. 541). In the embryo of the bird the pubic bones at first extend transversely, approaching each other as if a symphysis or junction were to follow (Fig. 542), but by the time the adult condition is reached, they have spread apart and come to project backward, as in Stegosaurus, thus allowing for an unobstructed passage of large eggs with breakable calcareous shells. Long before the expeditions to Mongolia that unearthed the famous dinosaur eggs now reposing in the American Museum of Natural History in New York City, the spreading pubic bones of these fossil reptilian giants made it possible to guess with reasonable certainty that in their day and generation they laid sizable eggs with calcareous shells.
The primitive character of the earliest known bird, Archaeopteryx, is clearly shown by its small pelvic girdle bones with distinct sutures between them and by the presence of an unbirdlike pubic symphysis (Fig. 543), as well as by the fact that the ilia connect with only six vertebrae, instead of the larger number characteristic of modern birds. The only other bird with a symphysis pubis is the African ostrich, Struthio, while an ischiac symphysis occurs only in the South American ostrich, Rhea, in which the symphysis lies dorsal to the digestive tract.
In mammals generally the three embryonic bones on either side of the pelvic girdle fuse together to form the single innominate bone (Fig. 544). Where the innominate bones of the two sides meet ventrally, the monotremes, marsupials, many rodents, insectivores, ungulates, and carnivores have a symphysis ischiaticum, as well as a symphysis pubis, but in primates, while the pubic bones unite in a symphysis, the ischia separate, forming two posterior skeletal projections that support the sitting animal. It would be extremely awkward for a cow, even if so minded, to “sit down” upon the single sharp ridge formed by the fusion of the two ischia. The large obturator foramen, formed by the union of pubic and ischio-pubic. foramina, is closed by a strong connective-tissue membrane except for a small passageway, at its anterior end, through which the obturator nerve and blood vessels pass.
The large fan-shaped ilium of man articulates, at an ear-shaped auricular surface, with the sacrum formed from five sacral vertebrae and their ribs. The two innominate bones, together with the sacrum and coccyx, form the pelvis, a somewhat funnel-shaped basin with a large anterior opening and a smaller posterior one. Through this bony halo must pass every mammal that is normally born into the world. In the female, the anterior parts of the ilia have a greater spread than in the male, giving as a result not only a shallower pelvic basin but broader hips. There are also distinguishable sexual differences in the posterior opening, which for obvious reasons is relatively larger in the female than in the male. Rauber gives the average comparative dimensions in man shown in Table IX, in which the letters refer to Figure 545.
The human pelvic girdle is for many reasons perhaps the most characteristic and distinctive part of the human skeleton, recording as it does drastic adaptations as the result of upright posture. Its triple composition is apparent embryologically for it is not until about the time of puberty that the three elements on either side become completely fused into the innominate bones, which together with the sacrum and coccyx of the vertebral column make up the pelvis. A firm, bony bowl immovably attached to the vertebral axis is thus formed in a position that not only provides attachment for the legs but also supports the viscera.
The spread of the iliac portion of the pelvis is greater among higher races than among primitive peoples, and in quadrupeds, where the weight of the viscera does not bear so directly on the pelvis, the iliac bones are narrower and do not flare so far apart.
The curving heads of the two femurs form, with the innominate bones, part of an arch which is completed above by the sacrum as a keystone, which resembles a wedge upside down. On this arch the weight of the entire body is supported. The faults of this mechanical curiosity, as pointed out by Meyer, are corrected by means of sacroiliac ligaments that extend from the sacrum to the upper edge of the ilium (Fig. 546). When the weight of the body presses down upon the sacrum it pulls upon these ligaments with the result that the iliac bones pinch together like a vise, thus holding the upside-down keystone firmly in its place. The greater the weight the more firmly the sacrum is held.
Monotremes and marsupials have an additional pair of pelvic replacing bones, called marsupial bones, the origin of which is unknown. It has been suggested that they may be transformed gastralia, or abdominal ribs. The fact that, unlike the abdominal ribs of reptiles, they are replacing instead of investing bones is not favorable to this supposition. Furthermore, no trace of them is found in placental mammals. Although they are doubtless useful in supporting the pouch of the female marsupial, they are not primarily utilized for that purpose, since they are equally well developed in both sexes. Whatever part they may play for their possessors, they are definitely of service to the comparative anatomist in enabling him to distinguish the skeleton of a marsupial from that of a placental mammal.
The acetabular, or cotyloid, bone, an additional small bony element which enters into the formation of the acetabulum in mammals (with the exception of monotremes, rodents, and bats), ossifies later than the other component parts of the pelvic girdle (Fig. 547).
The pectoral girdle has evolved further from the primitive set-up and is somewhat more complicated than the pelvic girdle, not only because of its secondary relations with the sternum and comparative freedom from the backbone, but also because investing as well as replacing bones take part in its formation.
It has its rise in the lower aquatic vertebrates, just posterior to the region weakened by the perforations of the gill slits. Hence the need for supplementary investing bones at this point was much greater than in the region of the pelvic girdle.
The ventral anchorage to the sternum of the clavicles, which in man are involved in providing an adequate support for the arms, is such that interference with the free respiratory movements of the ribs is largely removed.
Since there are no girdles of any kind either in amphioxus or the cyclostomes, the point of evolutionary departure for the pectoral girdle, as for so many other anatomical features, is found in the elasmobranch fishes, where a horseshoe-shaped bar of cartilage with its points extending upwards dorsally hooks under the “throat” just posterior to the gill arches. On either side of this inverted arch the paired pectoral fins articulate about midway from the tip to the ventral point of junction. The part above the attachment of the fin on either side (Fig. 548) is the scapular process, while that below, which joins the two halves of the arch ventrally, is the coracoid bar. In skates and rays, but not in dogfishes and sharks, the dorsal end of the scapular region may articulate with the vertebral column, thereby establishing connection with the axial skeleton, an unusual condition among vertebrates.
The pectoral girdle of ganoids, dipnoans, and teleosts begins with the formation of a pair of coracoscapular cartilages, which later become overlaid by investing bones. Primarily there are four of these investing bones in a more or less vertical row on each side of the body, namely, a ventral clavicle, then a large cleithrum, near the base of the fin, dorsal to which is a supracleithrum followed by a posttemporal which usually articulates with the posterior part of the skull. With the disappearance of clavicles in holosteans and teleosts, the cleithra tend to enlarge to meet ventrally. In teleosts, coracoid and scapula ossify from cartilage as distinct bones, although outside investing bones make up the bulk of the girdle.
The fossil stegocephalians (Fig. 549) unfortunately have only the bony parts of the pectoral girdles left to tell the tale, but these include paired clavicles and cleithra in addition to a median unpaired interclavicle between the ventral ends of the clavicles. The replacing girdle consists of a single pair of coracoscapular bones. The anterior appendage articulates on either side in a hallow, the glenoid cavityinstead of on a prominence as in elasmobranchs.
The highly specialized urodeles also have a single pair of coracoscapular bones although most of the girdle is cartilaginous, including a dorsal suprascapula and a ventral fanlike part of the coracoid which overlaps its fellow of the other side. Extending forward from the middle of the coracoscapular region is a cartilaginous procoracoid process of doubtful homology. In some cases, for example, Nee turns y the ossification does not extend into the coracoid, being limited to the ventral part of the scapula. Urodeles are without investing girdle bones.
Among the anurans the median margins of the coracoid and procoracoid cartilages coalesce on each side into an epicoracoidal cartilage. In toads the epicoracoids may overlap or slip past each other after the manner of the coracoids in urodeles, but in frogs they abut on each other or fuse into a common epicoracoidal plate. The procoracoid becomes strengthened externally by an overlying investing bone, the clavicle, which eventually takes its place. Both the cartilaginous coracoid and the scapula are replaced by bone, and even the supra-scapula in part, so that there finally result in the pectoral girdle of the frog the following paired bones: clavicles, coracoids, scapulas, and supra-scapulas, together with the cartilaginous epicoracoidal plate, of which parts only the clavicles are investing in character. The ventro-median ends of the clavicles and coracoids are embedded in the epicoracoidal plate, which also fuses with the sternal elements to form a continuous ventral structure.
The primitive reptiles, or cotylosaurs, in contrast with the primitive amphibians, had at least two bones, scapula and coracoid, in each half-girdle while in some cases a ventral pro Coracoid also ossified in front of the coracoid (Fig. 550). In all cotylosaurs there was a mid-ventral inter clavicle, a pair of clavicles, and usually a small pair of cleithra, all of which are investing bones reminiscent of the condition in stegocephalians. The therapsid reptiles, probably ancestral to the mammals, had all three pairs of replacing bones as well as clavicles and an interclavicle but usually lacked cleithra.
In general the pectoral girdle of modern reptiles is more bony than that of amphibians, consisting of replacing scapulas and coracoids together with investing interclavicle and clavicles but never cleithra or procoracoids. The pectoral girdle of turtles consists on either side of a tripod of rod-like bones which lacks the clavicle. The dorsally extending part of the tripod is the scapula, and the posterior ventral element, the coracoid, but the anterior ventral element, which was formerly taken to be the investing clavicle, is now known to be an outgrowth of the replacing scapula and is termed the acromion. It is homologous to the acromion process of the mammalian scapula (Fig. 551) with which the clavicle articulates. The interclavicle and the clavicles are now known to participate in the formation of the plastron, the ventral part of the turtles shell.
The pectoral girdle of turtles is peculiar in another way. The whole structure, as well as the pelvic girdle, is inside the ribs which form part of the shell, an arrangement not found among other vertebrates. In the embryos the girdles are still outside the ribs as usual, but with the modification of the ribs into costal plates that flatten out and unite edge to edge to contribute to the carapace, or dorsal part of the shell, the two girdles sink in and are covered over by the expanding ribs.
In crocodiles the clavicle, although appearing in the embryo, does not persist in the adult. The interclavicle is a simple rod in crocodiles but T-shaped in lizards. The coracoid and scapula of lizards are frequently fenestrated, that is, broken up by window-like parts. Pectoral girdles are missing in snakes and much reduced in the legless lizards.
Birds, whose extremely flexible necks tend to push back the anterior girdle bones towards the compact centralized region of the body, have a completely ossified pectoral girdle. The scapula becomes reduced to a narrow sword-like bone that lies close to the ribs along the dorsal surface of the thoracic basket; the coracoid is enlarged into a stout strut-like bone that braces against the upper edge of the sternum on either side; while the clavicles, by the medium of an inter clavicular element joint into a “wishbone,” or furcula, which in most cases also anchors onto the sternum, thus making a firm skeletal foundation for the attachment of the wings. The glenoid cavity, or the points on either side between which the body is suspended by the wings, is partly on the scapula and partly on the coracoid, thus insuring adequate articulation.
Ratites, or running birds, show adaptive differences, as compared with carinates, or flying birds, for in these forms both coracoid and scapula are reduced in size and anchylosed together, and the abbreviated clavicles fail to meet in a furcula. In Pachyornis, an extinct “moa,” the shoulder girdle is entirely absent, and in the living wingless Apteryx it is extremely rudimentary.
There are two types of pectoral girdles in mammals, as exemplified in primitive monotremes and in higher mammals. Monotremes retain the coracoids and have a lizard-like investing interclavicle intimately connected with the pectoral girdle, while the scapula is also quite unmammalian in appearance (Fig. 552). Other mammals lack the coracoid except in the form of the coracoid process, which may remain for some time as a separate skeletal element before its final fusion with the scapula. Since the scapulas are the sole bearers of the anterior appendages they become broadened usually into thin flat triangular bones, each characterized by a keel-like ridge, the spina scapulae, for the generous attachment of muscles (Fig. 551).
In mammals such as bats and primates, in which there is great power in the anterior appendages, the clavicles are strong and well developed, connecting the scapulas with the sternum. Diggers, climbers, and flyers belong to the collar-bone fraternity, while the ungulates, adapted for running, and the pinnipedes, sirenians, and cetaceans, aquatic mammals with appendages reduced to paddles, are either without a clavicle or have it much reduced. The clavicles of cats are merely degenerate splint-like floating bones, unattached at either end, so that the free blade-like scapulas may be seen slipping up and down past each other under the loose skin when these animals walk, making great freedom of motion possible for the quick stroke of the carnivorous paw.
The Free Appendages
The locomotor appendages of vertebrates may be separated into single median and paired lateral appendages. The former type reaches its highest manifestation in the unpaired fins of fishes.
The forerunner of the median appendages is seen in amphioxus, where a continuous fin, or integumental fold, supported by connective tissue, extends from the antero-dorsal region around the end of the tail, and ventrally to the right of the anus as far forward as the atrial pore. A similar continuous median fin is characteristic of most fishes in early embryonic stages. As development proceeds, portions of this continuous fin are absorbed, leaving isolated parts which form the various dorsal, caudal, anal, and ventral fins (Fig. 525). In general these median fins serve, like the centerboard of a sailboat, to maintain an even keel in water. The caudal fin also increases the effectiveness of the lateral stroke of the tail in sculling locomotion.
The paired horizontal fins of skates and rays are expanded, enabling these bottom-dwelling animals to move up and down as well as to swim forward.
The most primitive type of tail fin, found in amphioxus, cyclostomes, and amphibians, is protocercal (Fig. 553a), in which the vertebral column remains unbent and the inconspicuous flanges of the caudal fin are practically equal, dorsally and ventrally. In elasmobranchs and some ganoids the end of the skeletal axis curves upward (Fig. 553b), so that the flange of the caudal fin ventral to the vertebral column becomes considerably larger than the dorsal portion. This condition is termed heterocercal. The great majority of fishes, however, have a homocercal arrangement (Fig. 553c and c), that is, the upturned end of the skeletal axis becomes reduced while the dorsal flange again equals the ventral part. The diphycercal tail of living dipnoans is symmetrical externally while the skeletal axis is shortened so much that the upturned part, present in ancestors of these fishes, has been obliterated (Fig. 553e). In long-bodied fishes like squirming eels, the unnecessary tail fin becomes quite degenerate.
Frequently the caudal fin becomes deeply incised, as in the mackerel, Scomber (Fig. 553D), or more or less rounded, as in the “mummichug,” Fundulus (Fig. 553c).
Since all fins must have flexibility, this end is best accomplished by each fin acting as a whole, without the levers and joints that characterize the locomotor appendages of land vertebrates. To bring this about they are braced in position by skeletal elements which lie between the two walls of the fin fold. The most proximal of these supporting elements (basalia) connect with the girdle or, in the case of median fins, with the neural spines of the underlying vertebrae secondarily. The more distal elements (radialia), which may be either cartilage or bone, splice on to the basalia, thus extending the area of the fin. Radialia of bone may be regarded as derivatives of the bony scales of fishes. Frequently isolated basalia, usually situated directly in front of the fin proper, develop into defensive spines that are augmented by basal poison sacs.
In addition there is present in many fishes still a third kind of fin rays (actinotrichia), which are horny in texture, dermal in origin, and double in structure (Fig. 548), one half being derived from either side of the fold of skin constituting the fin. Actinotrichia may entirely replace the radialia, although in most fishes both radialia and basalia appear. The very primitive fin rays of amphioxus are gelatinous in character.
Amphibian larvae, as well as adult perennibranchs, have a caudal fin that may extend some distance anteriorly, but which differs from the caudal fin of fishes in being without skeletal support. Dorsal fins occur in cetaceans as they did in ichthyosaurs. Sirenians as well as cetaceans develop caudal appendages, usually spoken of as flukes, which are horizontal rather than vertical in arrangement. Like the caudal fins of amphibians, all these special appendages of mammals are unsupported by fin rays of any kind.
Lateral Appendages in General
Typically there are two pairs of lateral appendages in all vertebrates. They serve a great variety of uses aside from the primary function of locomotion.
Of vertebrates without paired appendages, the cyclostomes represent a primitive condition. Other legless vertebrates, such as caecilians, snakes, and certain lizards when adult, may be said to be reduced secondarily to this state, for some of them have appendages, at least in their early stages. Legs have been found, for instance, in the embryo of the apodous amphibian, Gymnophiona, by P. and F. Sarasin.
A few vertebrates have only anterior appendages. The list includes the chondrostean Calamoichthys; representatives of the teleost order of Apodes; the caudate Siren; the lizard Chirotes; the orders of Sirenia and Cetacea (although Kukenthal found hind legs in the embryo of one species of whales); and some other forms.
A smaller list of vertebrates, having only posterior appendages, includes pythons and boa-constrictors with rudimentary hind legs embedded in the skin; the lizards Pygopus and Pseudo pus, and possibly some other forms. The Australian burrowing “kiwi,” Apteryx, although regarded as wingless, shows vestigial anterior appendages.
The relative length of arms and legs in man as well as head and trunk varies with age (Fig. 554). Eventually the legs, which at first are shorter than the arms, come to be longer, so that it is not easy for man to assume the quadrupedal position. Such a change of relation during ontogeny is paralleled by the phylogenetic series of primates, as shown diagrammatically in Figure 555.
Embryonically the first part of the budding appendage that shows on the side of the human embryo turns out to be the distal part, that is, the future hand or foot (Fig. 556). This bud soon becomes scalloped, marking the future fingers or toes, and then, after a “web-footed” stage, the separate digits are finally established. Meanwhile the long bones of the arm or leg push out the terminal hand or foot, as the case may be, just as if these extremities were borne upon the end of an extending lever-like handle.
Different Pectoral Appendages
The pectoral appendages of fishes are of two general types, represented by the paired pectoral fins of elasmobranchs and the dipnoans. In the former a row of enlarged cartilages, or basalia, at the base of the fin, articulate with the girdle (Figs. 532A and 548). In the dipnoan type, there is a chain of skeletal elements with fin rays equally displayed on either side (Fig. 557).
Various attempts have been made to homologize the skeletons of the paired fins with the bones in the lateral appendages of tetrapods, but without universal satisfaction to comparative anatomists.
Beginning with the amphibians each lateral anterior appendage consists of the following sequence of bones, joined together as a system of levers: a single long bone, the humerus, articulating with the girdle; a pair of long bones, the radius and ulna; primarily three rows of wrist bones, ossa carpi; five palm bones, metacarpalia; and finally a set of digit bones, or phalanges, for each of the five fingers. The typical land appendage is therefore pentadactyl (penta, five; dactyl, digit). In primitive plan there are three wrist bones, or carpals, in the first row, two in the second, and five in the third (Figs. 529 and 558) while the five digits, beginning with the thumb, consist of two, three, four, five, and three phalanges respectively. (See Table X.)
In amphibians there are present four fingers instead of five although the number of digits on the hind foot is ordinarily not reduced (Fig. 559). A fusion of the radius and ulna into a single bone, the radio-ulna, takes place in anurans, while the middle one of the proximal row of carpal bones, the intermedium, is absent.
Among reptiles, Sphenodon has two central bones in the wrist (Fig. 558), but only one is common to other reptiles, except crocodiles which have none. The extinct ichthyosaurs and pleisosaurs had a great multiplication of phalanges to sustain their flipper-like appendages, while the fossil pterosaurs had an enormously elongated fourth finger to which was attached the stretched sail-like skin, serving as an organ of flight (Fig. 560).
The original quadrupedal character of birds is seen in nestlings, which scramble about the nest, using their undeveloped anterior appendages as legs. In adult birds complete emancipation of the anterior appendages from terrestrial locomotion appears with their extreme modification into wings. Not only are the long bones of the bird’s wing much lengthened, but the carpals are compacted together, and the fingers are reduced to three, two vestigial flanking a larger one, which furnishes a rigid support for the feathers of flight. Archaeopteryx points the way that this extreme evolution has taken by the presence of three well developed fingers on each wing. The tern, Sterna, embryonically shows four fingers (Fig. 561), but in all birds the tradition of a pentadactyl ancestry has been quite obliterated, even in their embryonic development.
The anterior appendages of mammals, which have a single, basic plan, exhibit a great variety of modifications, due to the diverse uses to which they are put. Climbing, digging, flying, striking, standing, running, grasping, and lifting are only a few of the many functions that make necessary structural adaptations. Nevertheless, even in the extremely modified flippers of the whale (Fig. 562), it is possible to homologize each of the transformed bones present with those of other mammals.
The human arm is a fore leg which has been freed from the work of locomotion and support, but the inherited system of levers and joints has been diverted to various other uses with conspicuous success. The function of the prehension of food, for example, is no Longer confined to the mouth and lips, as in many animals whose arms are still legs, nor are defensive structures, like horns or fangs, any longer necessary, since the swinging arms take the place of such organs of defence.
The entire arm is pivoted to the pectoral girdle by a ball-and-socket joint which allows great freedom of motion. Other joints between the separate arm bones, while limiting the range of motion in each instance, insure a gain in strength and effectiveness. Thus, at the elbow there is a hinge joint that moves in only one plane but which by means of this specialization is rendered all the more efficient. The joints of the wrist and hand are mostly hinge joints, moving likewise in one plane, but the rotation of the radius around the ulna (Fig. 563) brings the hinge action of the hand into any desirable plane.
All of the small wrist bones are irregular, many-sided structures held together by ligaments and so playing upon each other as to allow considerable motion. They fit together as a whole, forming a hollow trough with its convexity on the palmar side of the hand. Across this cavity the ligamentum carpi transversum stretches from side to side, and under the bridge thus formed the tendons, blood vessels, and nerves that supply the fingers go in safety.
The articulations of the wrist bones, as well as the other bones of the arm, are shown diagrammatically by dotted lines in Figure 564. It will be seen from this diagram that the entire hand is hung upon the radius which is enlarged at the carpal end to receive it. Although the radius takes some part in the articulation of the forearm to the humerus at the elbow joint, this function is mainly accomplished by the ulna, which is consequently enlarged at that end. Such an arrangement makes it possible for the distal end of the radius bearing the hand to rotate freely in a half circle, carrying the complex hand bones with it.
When the radius and ulna are parallel, the hand is palm up in an attitude of supplication. This is called supination. The opposite attitude of pronation occurs when the radius and ulna are crossed and the palm of the hand is turned down (Fig. 563). In all mammals except primates the radius and ulna remain permanently crossed.
Although centrale bones occur in most monkeys and some apes, they were not known in man until in 1874 they were discovered by Rosenberg in the human embryo. Their disappearance during the third fetal month is due to their fusion with other wrist bones.
Four small sesamoid bones, embedded in tendon, are regularly present on the palmar side of the hand. Two are at the metacarpophalangeal joint of the thumb, while one each is at the metacarpophalangeal joint of the index, and of the little finger. Frequently still other sesamoid nodules are found at the finger joints. A careful and extended study of a large series of human wrist bones, such as that made by Pfitzner, has revealed the presence in various situations of a great number of supernumerary wrist bones aside from the regular sesamoid bones. Figure 565 is a composite diagram from Pfitzner, showing the location of fifteen extra bones found in different human wrists, indicating that this region is still being extensively molded by evolutionary factors.
Syndactylism, or the growing of fingers together, brachydactylism, in which one phalanx of each digit is missing, and polydactylism, or the addition of extra fingers, all occur occasionally in man as well as in other vertebrates.
Different Pelvic Appendages
The sequence of bones in the pelvic appendages is homologous with that of the pectoral appendages, as shown in Figure 529 and in Table X, in which the synonyms of the names employed for the various parts are included. In birds and mammals the patella, a sesamoid ossification embedded in the extensor tendon over the knee, is generally present (Fig. 581), and a similar sesamoid, the brachial patella, rarely occurs at the elbow joint.
In general the chain of levers which the leg bones form acts as a “pusher” in locomotion, while that of the anterior appendage serves as a “puller” (Fig. 566). This is true both for quadrupeds progressing on the ground and for climbers in trees.
Elbows are bent backward and knees forward in quadrupeds, thus centralizing the long bones of the appendages under the body. The push or kick of the hind leg is more effective in locomotion than the pull of the front leg. It is the idea of the wheelbarrow rather than the drag-cart for carrying a load easily.
The differentiation between the anterior and posterior appendages in birds is very great. The legs assume the entire support of the body upon the ground, having become modified accordingly. The fibula becomes reduced and the several metatarsals fuse into a single bone, while the tarsals are reduced in number and solidly joined to other skeletal parts in the interest of increased firmness and strength, the proximal row fusing with the distal end of the tibia, and the distal row with the metatarsal, which brings the ankle joint between two rows of tarsal bones as in many reptiles.
The arrangement of levers in the leg of a bird combines the ability to walk and run with the possibility of sudden elevation in order to “hop off” in aviation. This latter accommodation is attained through the angle that the femur normally assumes with the tibiotarsus when not in flight. It will be seen (Fig. 567) that a bird is “sitting down” while it is still standing up, since the knees are directed forward horizontally, as in a sitting man. This position enables it, by straightening the legs suddenly, to rise enough from the ground or the perch to take to the air successfully. When a bird “squats” (Fig. 567B), the leg bones jackknife together, thus pulling the tendons attached to the toes taut and clinching the phalanges around the perch. To unlock the foot it is necessary for the body to be raised, thus straightening the leg and loosening the tendon which has been pulled tight over the ankle by the downward weight of the body in perching. When a bird perches, therefore, it is automatically locked for the time being upon the perch and can go to sleep without fear of falling off.
Among mammals the ankle joint is never between the rows of tarsal bones as in the reptiles and birds.
The difference between the hand and foot of man is greater than in any other animal. In apes the functions of grasping and support are partly shared by both the hand and foot (Figs. 568 and 569), whereas in man these two lines of activity have become entirely segregated, although some individuals have the ability to flex the toes enough to grasp awkwardly such an object as a handkerchief as well as to pick it up.
The ankle bones, which must support the weight of the body, form at least one half of the entire foot (Fig. 570), while the wrist bones do not make up more than one sixth of the grasping hand with its long fingers (Fig. 571). The longest toe is about one fourth the length of the foot while the longest finger is fully half the length of the hand.
The human foot is arranged practically at right angles to the leg (Fig. 570), while the hand hangs straight down at the end of the arm, making an angle of 180 degrees (Fig. 571). Moreover, the bending of the wrist towards the palm side is easily accomplished through an arc of at least 90 degrees, while the corresponding movement of the foot at the ankle is made with difficulty through a third of that distance, as shown diagrammatically in Figures 570 and 571.
On the other hand the swing away from the natural position in the opposite direction, which raises the foot up on the toes but accomplishes nothing useful for the grasping hand, is much freer and can extend through a larger arc in the case of the foot than in the hand. Rotation, which is easily accomplished by the hand by means of the way that the radius and ulna are hung from the humerus, is possible only in a slight degree in the foot. Since the tibia does not rotate on the fibula as the radius does on the ulna, the lateral swing of the big toe from right to left and back again is consequently limited.
In hoofed animals like the cow and horse, the specialization of a supporting leg and foot has gone much further than in man with the result that the rotary movement is entirely lost.
The human foot is plantigrade (Fig. 573), having not only phalanges and metatarsals, but even some of the tarsals, in contact with the ground. Birds and fissipede carnivores, for example cats and dogs, are digitigrade, because the ankle is lifted off the ground, while ungulates are unguligrade, that is, elevated on the tips of toes terminating in hoofs (Fig. 524), The unguligrade tapir of South America rests on the ends of four toes on each front foot and three on each hind foot. The pig walks on two toes with two degenerate toes hanging on either side (Fig. 572), that make an imperfect impression only when the animal walks over soft or muddy ground into which the feet sink. Artiodactyls generally are two-toed with the other toes in various degrees of degeneration, while perissodactyls, like the horse, are reduced to standing on the tip of a single toe on each foot. The horse’s ancestral gallery of family portraits shows all intermediate degrees of evolution from the five toes of Eohippus to the single toe of the modem horse. Flat-footed man would have a long road to travel before he reached the extreme stage of pedal evolution attained by the horse.
The bones of the human foot are arranged in the form of two arches, which act as springs or shock absorbers in locomotion. They also protect from pressure the nerves and blood vessels of the sole. The long arch rests upon the ground both at the heel and upon the ball of the foot or, in terms of the skeleton, upon the posterior end of the calcaneus and the distal ends of the metatarsals (Fig. 573). It has for a keystone the talus, or astragalus, which bears the weight of the body and is the only bone of the foot that articulates with the shank of the leg.
The smaller transverse arch (Fig. 574) extends from side to side through the distal ends of the sprawling metatarsals. In standing still the weight of the body rests principally upon the long arch, but when the center of gravity is thrown forward as in walking, the weight of the body shifts temporarily to the transverse arch every time one comes up on the ball of the foot or the toes. Then with the weight thrown forward the transverse arch tends to flatten, allowing the toes to grip the ground, and to pull the body forward effectually. This happens most perfectly in the case of the unrestricted bare foot that is not crowded into an unyielding hooflike shoe. It is obvious that high-heeled shoes throw the standing weight forward so that the long arch does not function properly, and the transverse arch, which should be reserved for springy locomotion, gets more than its share of burden-bearing. Any arch resting on two pillars spreads its weight over a larger area, making a more stable foundation than would be the case with a single column supporting the same amount of weight. The long arch of the foot is tipped up on end by the high-heeled shoe so that the line of gravity runs mostly through only one pillar instead of through two, in consequence of which it no longer functions as an arch, because the mechanical advantages which an arch possesses are thus sacrificed.
The awkwardness exhibited in walking on stilts or crutches is partly due to the absence of the double point of contact with the ground that is furnished by the arch. Again, tight shoes across the toes, that do not allow the transverse arch to spread properly in walking, prevent the proper pull on the ground by the toes and add greatly to the mechanical difficulties of locomotion. Human feet have never quite recovered from the effect of having the body tipped up on end with the entire responsibility of its support thrust upon them. In the evolutionary time at their disposal they have developed the best they could with the inherited materials with which they had to do, but it must nevertheless be confessed that the result is as yet only a makeshift foot. The various foot troubles of man are an eloquent confirmation of this statement.
Man needed to have a considerable part of the foot bent at right angles to the leg so that it would come into contact with the ground and thus prevent the upright body from tipping over forward. At the same time a part of the foot, the heel, had to be detailed to project in the other direction to prevent tipping backward.
The flatness of the foot, however, necessitated the formation of the arches just described which entailed adjustments in the case of every bone of the foot. That these adjustments at present are far from perfect is at once apparent when the arrangement of the bones of the foot is carefully scrutinized. The ankle bones, for example, together resemble a cairn of irregular stones piled one upon another, on the top of which is precariously balanced the weight of the body. Furthermore, the big calcaneus, or heel bone, is not squarely placed directly under the line of the center of gravity as a foundation stone should be, but is rather to the outside of this plumbline. That it is gradually being shoved under into a mechanically better position is shown in Figure 575, where is pictured the less satisfactory adjustment in the case of a primitive Australian and the still more primitive bow-legged ape. This outside lateral position of the calcaneus, like the run-over heel of a shoe, causes the weight of the body to veer over toward the inner or big-toe side of the foot. The long arch, moreover, is considerably higher and more effective on the inner side of the foot than it is on the outer, as any print of the normal bare foot in the sand demonstrates. The result is that the big toe is becoming larger while the little-toe side of the foot is degenerating.
The big toe is said to be relatively somewhat longer in the human male than in the female which, if true, would be evidence that the male, with his feet if not his head, has traveled a little further along the evolutionary highway than the female of the species.
The Human Hand
The human hand takes an important part with the large brain in placing man triumphant at the head of the animal creation. Without its aid the arts and sciences, which are the flower and expression of human civilization, would not have been possible.
The hand is first of all a universal grasping device, mounted on a movable arm, that can hold a tool or grip a weapon (Fig. 576). Without such artificial aids as tools and weapons man would still be a beast whose only substitutes for hands are specialized organs that are adapted for a narrow range of use, as for example, the goring horns of a bull or the chiseling teeth of a beaver. Once the hand is present that is capable of grasping artificial aids, the invention and utilization of all sorts of accessory devices goes forward with leaps and bounds, entirely unparalleled in the slow evolutionary process of adaptation by natural selection of bodily structures. As an evolutionary resource such a short cut to efficiency is an incalculable advantage to its possessor. Aside from man probably only the higher apes among animals make any attempt to use even so simple a tool or weapon as a stone or a stick. The idea of fashioning anything to be held in the hand for any purpose whatsoever belongs entirely to man.
The absolute dependence of man upon the opposable thumb, which has been significantly called “Wotan’s finger,” and the grasping hand that results is the key to most human activities. The thumbless spider monkey (Fig. 577) is only partly compensated by its prehensile tail.
What laborer works without his hands? What artisan, even in the “machine age,” can produce anything without in some stage of the process “fingering” it? The artist who creates a painting or a statue must hold brush or chisel. Even the prize-fighter clenches his fist with its tightly opposable thumb. The mechanical performance of all writing or printing, with everything that this means in the recording and communication of ideas, is primarily thumb-and-finger work, and the same is true of most of the daily activities that make up human life. The common phrase “he had a hand in it,” expresses exactly and literally the part dominant man has taken and continues to take in the world’s affairs.